The Extended Phenotype The Gene as the Unit of Selection
Richard D a w k i n s University of Oxford
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The Extended Phenotype The Gene as the Unit of Selection
Richard D a w k i n s University of Oxford
Oxford University Press
Oxford
University
London
Press,
Glasgow
Delhi
Bombay
Kuala
Hong
Dar es Salaam
Melbourne
Auckland in
associates
Beirut
Berlin
Oxford is
a
trade
6DP
Tokyo
Town
Mexico
mark
OX2
Karachi
Kong
Cape
Ibadan
Oxford
Toronto Madras
Singapore
and
Street,
York
Calcutta
Lumpur
Nairobi
Walton
New
City
of Oxford
Nicosia
University
Published in the United States by Oxford University P r e s s , New
Press
York
Acknowledgements pp.
141
142
'The
COLLECTED by
Donald
Watt.
Reproduced &
by
Windus
16
permission also
Inc.
by
Copyright
©
hardcover Freeman
issued as
British
by
Laura
THE
HUXLEY Laura
edited
Huxley.
Huxley
of Harper
by
Rudyard
of Doubleday
Richard edition
and
an
Library
Dawkins,
1971
of Mrs.
Hymn'
1982
W. First
©
by permission
permission
Original H.
Song' from
ALDOUS
and &
Chatto
Row,
(USA)
'McAndrew's
reproduced
Philosopher's OF
Copyright
Ltd,
Publishers, p.
Fifth
POETRY
published
Cataloguing
Extract
Company
Inc.
Dawkins
Company
Oxford
Kipling.
&
by
Limited
University in
Press paperback
Publication
1983
Data
Richard
The
extended
1.
Evolution
I.
Title
phenotype. 2.
575-12
Gene expression
QH.W
ISBN All
rights
reserved.
No part
of this publication
may
be
reproduced,
stored in a retrieval system, or transmitted, in any form or by any means, electronic, the
Filmset Eta
mechanical,
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permission in
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Printed Richard Bungay,
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otherwise,
without
Preface
T h e first c h a p t e r d o e s s o m e o f t h e w o r k o f a P r e f a c e , i n e x p l a i n i n g w h a t the b o o k d o e s a n d d o e s n o t set o u t t o a c c o m p l i s h , s o I c a n b e b r i e f h e r e . It is n o t a t e x t b o o k , n o r an i n t r o d u c t i o n to an e s t a b l i s h e d field.
It is a
p e r s o n a l l o o k a t t h e e v o l u t i o n o f life, a n d i n p a r t i c u l a r a t t h e l o g i c o f n a t u r a l s e l e c t i o n a n d t h e l e v e l i n t h e h i e r a r c h y o f life a t w h i c h n a t u r a l s e l e c t i o n c a n b e said t o a c t . I h a p p e n t o b e a n e t h o l o g i s t , b u t I h o p e p r e o c c u p a t i o n s w i t h a n i m a l b e h a v i o u r will not b e too n o t i c e a b l e . T h e i n t e n d e d scope o f the b o o k is w i d e r . T h e r e a d e r s for w h o m I a m m a i n l y w r i t i n g a r e m y p r o f e s s i o n a l c o l l e a g u e s , evolutionary
biologists,
ethologists
and
sociobiologists,
ecologists,
and
philosophers and humanists interested in e v o l u t i o n a r y science, including, of course,
graduate
and
undergraduate
students
in
all
these
disciplines.
T h e r e f o r e , a l t h o u g h this b o o k i s i n s o m e w a y s t h e s e q u e l t o m y p r e v i o u s b o o k , The Selfish Gene, it a s s u m e s t h a t t h e r e a d e r h a s p r o f e s s i o n a l k n o w l e d g e o f e v o l u t i o n a r y b i o l o g y a n d its t e c h n i c a l t e r m s . O n t h e o t h e r h a n d i t i s p o s s i b l e to e n j o y a p r o f e s s i o n a l b o o k as a s p e c t a t o r , e v e n if n o t a p a r t i c i p a n t i n the p r o f e s s i o n . S o m e l a y p e o p l e w h o r e a d this b o o k i n d r a f t h a v e b e e n k i n d e n o u g h , o r p o l i t e e n o u g h , t o c l a i m t o h a v e l i k e d it. I t w o u l d g i v e m e g r e a t satisfaction t o b e l i e v e t h e m , a n d I h a v e a d d e d a g l o s s a r y o f t e c h n i c a l t e r m s w h i c h I h o p e m a y h e l p . I h a v e also t r i e d t o m a k e t h e b o o k a s n e a r a s p o s s i b l e to being enjoyable to read. T h e resulting tone m a y possibly irritate some serious p r o f e s s i o n a l s . I v e r y m u c h h o p e n o t , b e c a u s e s e r i o u s p r o f e s s i o n a l s a r e the p r i m a r y a u d i e n c e t o w h o m I w i s h t o s p e a k . I t i s a s i m p o s s i b l e t o p l e a s e e v e r y b o d y i n l i t e r a r y s t y l e a s i t i s i n a n y o t h e r m a t t e r o f taste, a n d s t y l e s t h a t g i v e the most positive pleasure to s o m e p e o p l e are often the most a n n o y i n g to others. C e r t a i n l y the tone of the b o o k is not c o n c i l i a t o r y or a p o l o g e t i c — s u c h is not the w a y o f a n a d v o c a t e t h a t s i n c e r e l y b e l i e v e s i n his c a s e — a n d I m u s t p a c k all a p o l o g y i n t o t h e P r e f a c e . S o m e o f t h e e a r l i e r c h a p t e r s r e p l y t o criticisms of my previous book, w h i c h m i g h t recur in response to the present
vi
Preface
o n e . I a m s o r r y t h a t this i s n e c e s s a r y , a n d I a m s o r r y i f a n o t e o f e x a s p e r a t i o n c r e e p s i n f r o m t i m e t o t i m e . I trust, a t l e a s t , t h a t m y e x a s p e r a t i o n r e m a i n s g o o d h u m o u r e d . I t i s n e c e s s a r y t o p o i n t t o p a s t m i s u n d e r s t a n d i n g s a n d try t o forestall
their
repetition,
but
I
would
not
wish
to
give
an
aggrieved
impression that m i s u n d e r s t a n d i n g has b e e n w i d e s p r e a d . It has been confined to n u m e r i c a l l y v e r y limited quarters, b u t in s o m e cases rather v o c a l ones. I a m g r a t e f u l t o m y c r i t i c s for f o r c i n g m e t o t h i n k a g a i n a b o u t h o w t o e x p r e s s difficult m a t t e r s m o r e c l e a r l y . I a p o l o g i z e to readers w h o m a y find a favourite and relevant w o r k missing from the b i b l i o g r a p h y . T h e r e are those c a p a b l e o f c o m p r e h e n s i v e l y and exhaustively s u r v e y i n g the literature of a large field, but I h a v e never been a b l e t o u n d e r s t a n d h o w t h e y m a n a g e it. I k n o w t h a t t h e e x a m p l e s I h a v e c i t e d are a small subset of those that could h a v e been cited, and are sometimes the w r i t i n g s or r e c o m m e n d a t i o n s of my friends. If the result a p p e a r s biased, w e l l , of course it is biased, a n d I am sorry. I think nearly e v e r y b o d y must be s o m e w h a t b i a s e d i n this k i n d o f w a y . A b o o k i n e v i t a b l y reflects the c u r r e n t p r e o c c u p a t i o n s of the author, and t h e s e p r e o c c u p a t i o n s a r e l i k e l y t o h a v e b e e n a m o n g the t o p i c s o f his m o s t r e c e n t p a p e r s . W h e n t h o s e p a p e r s a r e s o r e c e n t t h a t i t w o u l d b e a n artificial contrivance
to
change
the words,
I
h a v e not hesitated
to reproduce a
p a r a g r a p h almost v e r b a t i m here and there. T h e s e paragraphs, w h i c h will be f o u n d i n C h a p t e r s 4 , 5 , 6 a n d 1 4 , a r e a n i n t e g r a l p a r t o f t h e m e s s a g e o f this book, a n d to o m i t t h e m w o u l d be just as artificial as to m a k e gratuitous changes in their w o r d i n g . T h e o p e n i n g sentence of C h a p t e r
1
d e s c r i b e s the b o o k a s a w o r k o f
u n a b a s h e d a d v o c a c y b u t , w e l l , p e r h a p s I a m j u s t a little bit a b a s h e d ! W i l s o n ( 1 9 7 5 , p p . 28—29) h a s r i g h t l y c a s t i g a t e d t h e ' a d v o c a c y m e t h o d ' i n a n y s e a r c h for s c i e n t i f i c t r u t h , a n d I h a v e t h e r e f o r e d e v o t e d s o m e o f m y f i r s t c h a p t e r t o a p l e a o f m i t i g a t i o n . I c e r t a i n l y w o u l d n o t w a n t s c i e n c e t o a d o p t the l e g a l s y s t e m i n w h i c h p r o f e s s i o n a l a d v o c a t e s m a k e t h e best c a s e t h e y c a n for a p o s i t i o n , e v e n i f t h e y b e l i e v e i t t o b e false. I b e l i e v e d e e p l y i n t h e v i e w o f life t h a t this b o o k a d v o c a t e s , a n d h a v e d o n e so, a t least i n p a r t , for a l o n g t i m e , c e r t a i n l y since the time of my first published paper, in w h i c h I c h a r a c t e r i z e d a d a p t a t i o n s a s f a v o u r i n g ' t h e s u r v i v a l o f the a n i m a l ' s g e n e s . . . '
(Dawkins
1 9 6 8 ) . T h i s b e l i e f — t h a t i f a d a p t a t i o n s a r e t o b e t r e a t e d a s 'for t h e g o o d o f s o m e t h i n g , that s o m e t h i n g is the g e n e — w a s the f u n d a m e n t a l assumption of m y p r e v i o u s b o o k . T h e present b o o k goes further. T o d r a m a t i z e i t a bit, i t a t t e m p t s t o free t h e selfish g e n e f r o m t h e i n d i v i d u a l o r g a n i s m w h i c h h a s b e e n its c o n c e p t u a l p r i s o n . T h e p h e n o t y p i c effects o f a g e n e a r e t h e tools b y w h i c h i t l e v e r s i t s e l f i n t o t h e n e x t g e n e r a t i o n , a n d these tools m a y ' e x t e n d ' far o u t s i d e t h e b o d y i n w h i c h t h e g e n e sits, e v e n r e a c h i n g d e e p i n t o t h e n e r v o u s systems of other organisms. S i n c e it is not a factual position I am a d v o c a t i n g , b u t a w a y of seeing facts,
I
wanted
to w a r n
the reader not to expect
Preface
vii
' e v i d e n c e ' i n the n o r m a l sense o f t h e w o r d . I a n n o u n c e d t h a t t h e b o o k w a s a work of a d v o c a c y , because I was anxious not to disappoint the reader, not to l e a d h e r o n u n d e r false p r e t e n c e s a n d w a s t e h e r t i m e . T h e l i n g u i s t i c e x p e r i m e n t o f t h e last s e n t e n c e r e m i n d s m e t h a t I w i s h I h a d h a d the c o u r a g e t o i n s t r u c t the c o m p u t e r t o f e m i n i z e p e r s o n a l p r o n o u n s at r a n d o m t h r o u g h o u t the text. T h i s is not o n l y b e c a u s e I a d m i r e the current awareness of the m a s c u l i n e bias in o u r l a n g u a g e . W h e n e v e r I w r i t e I h a v e a particular imaginary reader in mind
(different i m a g i n a r y r e a d e r s o v e r s e e
a n d 'filter' t h e s a m e p a s s a g e i n n u m e r o u s s u c c e s s i v e r e v i s i o n s ) a n d a t least half my
imaginary
readers
are,
like
at
least
half my
friends,
female.
U n f o r t u n a t e l y i t i s still t r u e i n E n g l i s h t h a t t h e u n e x p e c t e d n e s s o f a f e m i n i n e pronoun,
where
a
neutral
meaning
is
intended,
attention of most readers, of either sex.
I
p r e v i o u s p a r a g r a p h w i l l s u b s t a n t i a t e this.
seriously
distracts
the
b e l i e v e the e x p e r i m e n t of the W i t h regret,
therefore,
I
have
f o l l o w e d the s t a n d a r d c o n v e n t i o n i n this b o o k . F o r m e , w r i t i n g is almost a social activity, a n d I am grateful to the m a n y friends w h o h a v e , s o m e t i m e s u n w i t t i n g l y , p a r t i c i p a t e d t h r o u g h d i s c u s s i o n , argument and moral support.
I cannot thank them all by n a m e .
Marian
S t a m p D a w k i n s has not o n l y p r o v i d e d sensitive a n d k n o w l e d g e a b l e criticism o f the w h o l e b o o k i n several drafts. S h e has also k e p t m e g o i n g b y b e l i e v i n g i n the p r o j e c t e v e n t h r o u g h t h e t i m e s w h e n I lost m y o w n c o n f i d e n c e . A l a n Grafen a n d M a r k R i d l e y , officially m y g r a d u a t e students, r e a l l y , i n their different w a y s , m y m e n t o r s a n d g u i d e s t h r o u g h d i f f i c u l t t h e o r e t i c a l t e r r i t o r y , have
influenced
the
book
immeasurably.
In
the
first
draft
their
names
seemed to creep in on almost every p a g e , a n d it w a s only the p a r d o n a b l e g r u m b l i n g s of a referee that c o m p e l l e d me to banish to the P r e f a c e my a c k n o w l e d g m e n t o f debt t o t h e m . C a t h y K e n n e d y m a n a g e s t o c o m b i n e close f r i e n d s h i p for m e w i t h d e e p s y m p a t h y for m y b i t t e r e s t c r i t i c s . T h i s h a s p u t her in a u n i q u e position to advise m e , especially o v e r the earlier c h a p t e r s w h i c h a t t e m p t t o r e p l y t o c r i t i c i s m . I f e a r t h a t s h e w i l l still n o t l i k e t h e t o n e o f these c h a p t e r s , b u t s u c h i m p r o v e m e n t a s t h e r e m a y b e i s l a r g e l y d u e t o h e r influence and I am v e r y grateful to her. I w a s p r i v i l e g e d t o h a v e t h e first d r a f t c r i t i c i z e d i n its e n t i r e t y b y J o h n Maynard
Smith,
David
C.
Smith, John
Krebs,
Paul
Harvey,
and
Ric
C h a r n o v , a n d the f i n a l d r a f t o w e s m u c h t o a l l o f t h e m . I n a l l c a s e s I a c t e d o n their a d v i c e , e v e n if I
d i d n o t a l w a y s t a k e it.
Others kindly criticized
chapters
special
Hansell
in
their
own
fields:
Michael
the
chapter
on
a r t e f a c t s , P a u l i n e L a w r e n c e t h a t o n p a r a s i t e s , E g b e r t L e i g h t h a t o n fitness, A n t h o n y H a l l a m the section o n p u n c t u a t e d e q u i l i b r i a , W . F o r d D o o l i t t l e that o n selfish D N A , a n d D i a n e D e S t e v e n b o t a n i c a l s e c t i o n s . T h e b o o k w a s f i n i s h e d a t O x f o r d , b u t b e g u n d u r i n g a visit t o t h e U n i v e r s i t y o f F l o r i d a a t Gainesville on a sabbatical leave kindly granted by the U n i v e r s i t y of O x f o r d a n d the W a r d e n a n d F e l l o w s o f N e w C o l l e g e . I a m g r a t e f u l t o m y m a n y
viii
Preface
F l o r i d a n friends for g i v i n g m e s u c h a p l e a s a n t a t m o s p h e r e i n w h i c h t o w o r k , especially
Jane
Brockmann,
who
also
provided
helpful
criticism
of
p r e l i m i n a r y d r a f t s , a n d D o n n a G i l l i s , w h o also d i d m u c h o f t h e t y p i n g . I b e n e f i t e d , t o o , f r o m a m o n t h ' s e x p o s u r e t o t r o p i c a l b i o l o g y a s the grateful guest of the S m i t h s o n i a n
I n s t i t u t i o n i n P a n a m a d u r i n g t h e w r i t i n g o f the
b o o k . F i n a l l y , it is a pleasure o n c e a g a i n to thank M i c h a e l R o d g e r s , formerly o f O x f o r d U n i v e r s i t y Press a n d n o w o f W . H . F r e e m a n a n d C o m p a n y , a 'Ks e l e c t e d ' e d i t o r w h o r e a l l y b e l i e v e s i n his b o o k s a n d i s t h e i r tireless a d v o c a t e . Oxford June
Richard Dawkins 1981
Contents
1 Necker
Cubes
2 Genetic
Determinism
3 Constraints
and
on
Buffaloes 1 and
Gene
Perfection
Selectionism 9
30
4 A r m s Races and Manipulation
55
5 The Active Germ-Line Replicator
81
6 Organisms, Groups and M e m e s : Replicators or Vehicles? 97 7 Selfish Wasp or Selfish Strategy? 8 Outlaws
and
Modifiers
118
133
9 Selfish DNA, Jumping Genes, and a Lamarckian Scare 10 An Agony in Five Fits 179 11 The Genetical Evolution of Animal Artefacts 195 12 Host Phenotypes of Parasite Genes 13 Action at a Distance
228
14 Rediscovering the O r g a n i s m Glossary
283
250
209
156
T h e Extended Phenotype
1 Necker C u b e s and Buffaloes
T h i s is a w o r k of u n a b a s h e d a d v o c a c y . I w a n t to a r g u e in favour of a particular w a y of looking at animals and plants, and a particular w a y of w o n d e r i n g w h y they do the things that they d o . W h a t I am a d v o c a t i n g is not a n e w t h e o r y , n o t a h y p o t h e s i s w h i c h c a n b e v e r i f i e d o r falsified, n o t a m o d e l w h i c h c a n b e j u d g e d b y its p r e d i c t i o n s . I f i t w e r e a n y o f t h o s e t h i n g s , I a g r e e with Wilson
(1975, p.
28)
that the ' a d v o c a c y m e t h o d ' w o u l d
be inap-
propriate a n d reprehensible. But it is not a n y of those things. W h a t I am a d v o c a t i n g i s a p o i n t o f v i e w , a w a y o f l o o k i n g a t f a m i l i a r facts a n d i d e a s , and a w a y of asking new questions about them. A n y reader w h o expects a c o n v i n c i n g n e w t h e o r y i n t h e c o n v e n t i o n a l sense o f t h e w o r d i s b o u n d t o b e left, t h e r e f o r e , w i t h a d i s a p p o i n t e d 'so w h a t ? ' f e e l i n g . B u t I a m n o t t r y i n g t o c o n v i n c e a n y o n e of the truth of any factual proposition. R a t h e r , I am t r y i n g to show the r e a d e r a w a y of seeing b i o l o g i c a l facts. T h e r e i s a w e l l - k n o w n v i s u a l i l l u s i o n c a l l e d the N e c k e r C u b e . I t c o n s i s t s o f a line d r a w i n g w h i c h t h e b r a i n i n t e r p r e t s a s a t h r e e - d i m e n s i o n a l c u b e . B u t there are t w o possible orientations of the p e r c e i v e d equally
compatible
with
the
two-dimensional
image
cube, on
and the
both are
paper.
We
u s u a l l y b e g i n b y s e e i n g o n e o f the t w o o r i e n t a t i o n s , b u t i f w e l o o k for s e v e r a l s e c o n d s t h e c u b e 'flips o v e r ' i n t h e m i n d , a n d w e see t h e o t h e r a p p a r e n t o r i e n t a t i o n . A f t e r a few m o r e s e c o n d s t h e m e n t a l i m a g e f l i p s b a c k a n d i t continues to alternate as l o n g as we look at the picture. T h e point is that neither of the t w o perceptions of the c u b e is the correct or 'true' o n e . T h e y a r e e q u a l l y c o r r e c t . S i m i l a r l y t h e v i s i o n o f life t h a t I a d v o c a t e , a n d l a b e l w i t h the n a m e o f t h e e x t e n d e d p h e n o t y p e , i s n o t p r o v a b l y m o r e c o r r e c t t h a n the o r t h o d o x v i e w . I t i s a different v i e w a n d I s u s p e c t t h a t , a t l e a s t i n s o m e r e s p e c t s , it p r o v i d e s a d e e p e r u n d e r s t a n d i n g . B u t I d o u b t t h a t t h e r e is a n y experiment that could be done to prove my claim. T h e p h e n o m e n a that I shall c o n s i d e r — c o e v o l u t i o n , arms races, m a n i p u l a t i o n o f hosts b y p a r a s i t e s , m a n i p u l a t i o n o f t h e i n a n i m a t e w o r l d b y l i v i n g t h i n g s , e c o n o m i c ' s t r a t e g i e s ' for m i n i m i z i n g costs a n d m a x i m i z i n g b e n e f i t s — 1
2
N e c k e r C u b e s and Buffaloes
are all familiar e n o u g h , a n d are a l r e a d y the subject of intensive study. W h y , then, should the busy reader bother to go o n ? It is tempting to borrow S t e p h e n G o u l d ' s w i n n i n g l y i n g e n u o u s a p p e a l at the b e g i n n i n g of a more substantial v o l u m e ( 1 9 7 7 a ) a n d simply say, 'Please read the b o o k ' a n d y o u w i l l f i n d o u t w h y i t w a s w o r t h b o t h e r i n g t o d o s o . U n f o r t u n a t e l y I d o not h a v e t h e s a m e g r o u n d s for c o n f i d e n c e . I c a n o n l y s a y t h a t , a s o n e o r d i n a r y biologist
studying
animal
behaviour,
I
have
found
that
the
viewpoint
r e p r e s e n t e d b y t h e l a b e l ' e x t e n d e d p h e n o t y p e ' h a s m a d e m e see a n i m a l s a n d t h e i r b e h a v i o u r d i f f e r e n t l y , a n d I t h i n k I u n d e r s t a n d t h e m b e t t e r for it. T h e e x t e n d e d p h e n o t y p e m a y n o t c o n s t i t u t e a t e s t a b l e h y p o t h e s i s i n itself, b u t i t s o far c h a n g e s t h e w a y w e see a n i m a l s a n d p l a n t s t h a t i t m a y c a u s e u s t o t h i n k o f t e s t a b l e h y p o t h e s e s t h a t w e w o u l d o t h e r w i s e n e v e r h a v e d r e a m e d of. L o r e n z ' s ( 1 9 3 7 ) d i s c o v e r y t h a t a b e h a v i o u r p a t t e r n c a n b e t r e a t e d like a n a n a t o m i c a l o r g a n w a s n o t a d i s c o v e r y i n t h e o r d i n a r y sense. N o e x p e r i m e n t a l results w e r e a d d u c e d i n its s u p p o r t . I t w a s s i m p l y a n e w w a y o f s e e i n g facts that
were
already
commonplace,
yet
it
dominates
modern
ethology
( T i n b e r g e n 1 9 6 3 ) , a n d it seems to us t o d a y so o b v i o u s that it is hard to understand that it ever needed 'discovering'. Similarly, D ' A r c y Thompson's ( 1 9 1 7 ) celebrated c h a p t e r ' O n the theory of t r a n s f o r m a t i o n s . . . ' is widely r e g a r d e d a s a w o r k o f i m p o r t a n c e a l t h o u g h i t d o e s n o t a d v a n c e o r test a h y p o t h e s i s . I n a sense i t i s o b v i o u s l y n e c e s s a r i l y t r u e t h a t a n y a n i m a l f o r m can
be
turned
into
a
related
form
by
a
mathematical
transformation,
a l t h o u g h it is not o b v i o u s that the transformation will be a simple one. In a c t u a l l y d o i n g i t for a n u m b e r o f s p e c i f i c e x a m p l e s , D ' A r c y T h o m p s o n i n v i t e d a 'so w h a t ? ' r e a c t i o n f r o m a n y o n e f a s t i d i o u s e n o u g h t o insist t h a t science p r o c e e d s o n l y b y the falsifying o f specific hypotheses. I f w e read D ' A r c y T h o m p s o n ' s c h a p t e r a n d t h e n ask o u r s e l v e s w h a t w e n o w k n o w t h a t we did
not k n o w
before,
the a n s w e r m a y w e l l b e not m u c h .
But our
i m a g i n a t i o n is fired. We go b a c k a n d look at animals in a n e w w a y ; and we think about
theoretical problems,
in
this c a s e t h o s e o f e m b r y o l o g y a n d
p h y l o g e n y and their interrelations, in a new w a y . I a m , of course, not so p r e s u m p t u o u s as to c o m p a r e the present modest w o r k w i t h the masterpiece of a g r e a t b i o l o g i s t . I u s e t h e e x a m p l e s i m p l y to d e m o n s t r a t e t h a t it is possible for a t h e o r e t i c a l b o o k t o b e w o r t h r e a d i n g e v e n i f i t d o e s n o t a d v a n c e t e s t a b l e h y p o t h e s e s b u t s e e k s , i n s t e a d , t o c h a n g e t h e w a y w e see. A n o t h e r g r e a t biologist o n c e r e c o m m e n d e d that to understand the actual we must c o n t e m p l a t e the possible: ' N o practical biologist interested in sexual reproduction
would
be
led
to
work
out
the
detailed
consequences ex-
p e r i e n c e d b y o r g a n i s m s h a v i n g t h r e e o r m o r e s e x e s ; y e t w h a t else s h o u l d h e d o i f h e w i s h e s t o u n d e r s t a n d w h y t h e sexes a r e , i n f a c t , a l w a y s t w o ? ' ( F i s h e r 1930a, p . i x ) . W i l l i a m s ( 1 9 7 5 ) , M a y n a r d S m i t h (1978a) and others h a v e t a u g h t u s t h a t o n e o f t h e c o m m o n e s t , m o s t u n i v e r s a l f e a t u r e s o f life o n E a r t h , sexuality
itself,
should
not
be
accepted
without
question.
Indeed,
its
N e c k e r C u b e s and Buffaloes
3
e x i s t e n c e turns o u t t o b e p o s i t i v e l y s u r p r i s i n g w h e n set a g a i n s t t h e i m a g i n e d possibility of asexual r e p r o d u c t i o n . To i m a g i n e a s e x u a l r e p r o d u c t i o n as a h y p o t h e t i c a l p o s s i b i l i t y i s n o t difficult, s i n c e w e k n o w i t i s a r e a l i t y i n s o m e animals and plants. B u t are there other cases w h e r e o u r i m a g i n a t i o n r e c e i v e s n o s u c h p r o m p t i n g ? A r e t h e r e i m p o r t a n t facts a b o u t life t h a t w e h a r d l y notice simply
because we
lack
the
imagination
to
visualise
alternatives
w h i c h , like Fisher's three sexes, m i g h t h a v e existed in some possible w o r l d ? I shall try t o s h o w t h a t t h e a n s w e r i s y e s . Playing with an imaginary world, in order to increase our understanding of the actual w o r l d , is the t e c h n i q u e of ' t h o u g h t e x p e r i m e n t ' . It is m u c h used by p h i l o s o p h e r s . F o r i n s t a n c e in a c o l l e c t i o n of essays on Mind (ed.
Glover
1976),
The Philosophy of
various authors i m a g i n e surgical operations in
which one person's brain is transplanted into another person's b o d y , and t h e y use t h e t h o u g h t e x p e r i m e n t t o c l a r i f y t h e m e a n i n g o f ' p e r s o n a l i d e n t i t y ' . A t times philosophers' t h o u g h t e x p e r i m e n t s are p u r e l y i m a g i n a r y a n d w i l d l y i m p r o b a b l e , b u t this d o e s n ' t m a t t e r g i v e n t h e p u r p o s e for w h i c h t h e y a r e m a d e . A t o t h e r t i m e s t h e y a r e i n f o r m e d , t o a g r e a t e r o r lesser e x t e n t , b y facts from t h e r e a l w o r l d , for i n s t a n c e t h e facts o f s p l i t - b r a i n e x p e r i m e n t s . Consider
another
thought
experiment,
this
time
from
evolutionary
b i o l o g y . W h e n I w a s a n u n d e r g r a d u a t e o b l i g e d t o w r i t e s p e c u l a t i v e essays o n 'the origin o f the C h o r d a t e s ' a n d other topics o f r e m o t e p h y l o g e n y , o n e o f m y tutors r i g h t l y tried t o s h a k e m y faith i n t h e v a l u e o f s u c h s p e c u l a t i o n s b y suggesting that a n y t h i n g c o u l d , in principle, e v o l v e into a n y t h i n g else. E v e n insects c o u l d e v o l v e i n t o m a m m a l s , i f o n l y t h e r i g h t s e q u e n c e o f s e l e c t i o n pressures w e r e p r o v i d e d i n the r i g h t o r d e r . A t t h e t i m e , a s m o s t z o o l o g i s t s w o u l d , I d i s m i s s e d t h e i d e a a s o b v i o u s n o n s e n s e , a n d I still, o f c o u r s e , d o n ' t b e l i e v e t h a t the r i g h t s e q u e n c e o f s e l e c t i o n p r e s s u r e s e v e r w o u l d b e p r o v i d e d . N o r d i d m y t u t o r . B u t a s far a s t h e p r i n c i p l e i s c o n c e r n e d , a s i m p l e t h o u g h t experiment shows it to be nearly incontrovertible. We need only prove that t h e r e exists a c o n t i n u o u s series of s m a l l steps l e a d i n g f r o m an i n s e c t , s a y a s t a g b e e t l e , t o a m a m m a l , s a y a s t a g . B y this I m e a n t h a t , s t a r t i n g w i t h t h e beetle, we could lay out a sequence of hypothetical animals, e a c h one as s i m i l a r t o t h e p r e v i o u s m e m b e r o f t h e series a s a p a i r o f b r o t h e r s m i g h t b e , a n d the s e q u e n c e w o u l d c u l m i n a t e i n a r e d d e e r s t a g . T h e proof is easy, p r o v i d e d only that we a c c e p t , as e v e r y o n e does, that b e e t l e a n d d e e r h a v e a c o m m o n a n c e s t o r , h o w e v e r far b a c k . E v e n i f t h e r e i s n o o t h e r s e q u e n c e o f steps f r o m b e e t l e t o d e e r , w e k n o w t h a t a t least o n e sequence must be obtained by simply tracing the beetle's ancestors b a c k to the c o m m o n a n c e s t o r , t h e n w o r k i n g f o r w a r d s d o w n t h e o t h e r l i n e t o t h e deer. We
have
proved
that
there
exists
a
trajectory
of stepwise
change
connecting beetle to deer and, by implication, a similar trajectory from a n y modern a n i m a l to any other m o d e r n animal. In principle, therefore, we m a y
4
N e c k e r C u b e s and Buffaloes
p r e s u m e t h a t a series o f s e l e c t i o n p r e s s u r e s c o u l d b e a r t i f i c i a l l y c o n t r i v e d t o p r o p e l a l i n e a g e a l o n g o n e of these trajectories.
It was a q u i c k thought
e x p e r i m e n t a l o n g t h e s e lines t h a t e n a b l e d m e t o s a y , w h e n d i s c u s s i n g D ' A r c y T h o m p s o n ' s t r a n s f o r m a t i o n s , t h a t ' I n a sense i t i s o b v i o u s l y n e c e s s a r i l y true that a n y a n i m a l form c a n be turned into a related form by a m a t h e m a t i c a l t r a n s f o r m a t i o n , a l t h o u g h it is n o t o b v i o u s t h a t t h e t r a n s f o r m a t i o n w i l l be a simple
one.'
In
this
book
I
shall
make
frequent
use
of the
thought-
e x p e r i m e n t t e c h n i q u e . I w a r n t h e r e a d e r o f this i n a d v a n c e , s i n c e scientists are s o m e t i m e s a n n o y e d by the lack of realism in such forms of reasoning. T h o u g h t e x p e r i m e n t s are not supposed to be realistic. T h e y are supposed to clarify our thinking a b o u t reality. O n e f e a t u r e o f life i n this w o r l d w h i c h , l i k e s e x , w e h a v e t a k e n for g r a n t e d and m a y b e should not, is that living matter comes in discrete p a c k a g e s called organisms.
In
particular,
biologists
interested
in
functional
explanation
u s u a l l y a s s u m e t h a t t h e a p p r o p r i a t e u n i t for d i s c u s s i o n i s t h e i n d i v i d u a l o r g a n i s m . T o us, ' c o n f l i c t ' u s u a l l y m e a n s c o n f l i c t b e t w e e n o r g a n i s m s , e a c h o n e s t r i v i n g t o m a x i m i z e its o w n i n d i v i d u a l 'fitness'. W e r e c o g n i z e s m a l l e r u n i t s s u c h a s c e l l s a n d g e n e s , a n d l a r g e r u n i t s s u c h a s p o p u l a t i o n s , societies a n d e c o s y s t e m s , b u t t h e r e i s n o d o u b t t h a t the i n d i v i d u a l b o d y , a s a discrete u n i t o f a c t i o n , e x e r t s a p o w e r f u l h o l d o v e r the m i n d s o f z o o l o g i s t s , e s p e c i a l l y those interested in the a d a p t i v e significance of a n i m a l b e h a v i o u r . O n e of my a i m s i n this b o o k i s t o b r e a k t h a t h o l d . I w a n t t o s w i t c h e m p h a s i s from the i n d i v i d u a l b o d y a s f o c a l u n i t o f f u n c t i o n a l d i s c u s s i o n . A t t h e v e r y least I w a n t t o m a k e u s a w a r e o f h o w m u c h w e t a k e for g r a n t e d w h e n w e l o o k a t life as a collection of discrete i n d i v i d u a l organisms. The
thesis
that
I
shall
s u p p o r t is
this.
It
is
legitimate
to
s p e a k of
a d a p t a t i o n s a s b e i n g 'for t h e b e n e f i t o f s o m e t h i n g , b u t t h a t s o m e t h i n g i s best n o t s e e n as t h e i n d i v i d u a l o r g a n i s m . It is a s m a l l e r u n i t w h i c h I c a l l the a c t i v e , g e r m - l i n e r e p l i c a t o r . T h e m o s t i m p o r t a n t k i n d o f r e p l i c a t o r i s the ' g e n e ' or small g e n e t i c f r a g m e n t . R e p l i c a t o r s are not, of course, selected d i r e c t l y , b u t b y p r o x y ; t h e y a r e j u d g e d b y t h e i r p h e n o t y p i c effects. A l t h o u g h for s o m e p u r p o s e s i t i s c o n v e n i e n t t o t h i n k o f t h e s e p h e n o t y p i c effects a s being p a c k a g e d together in discrete 'vehicles' such as individual organisms, this i s n o t f u n d a m e n t a l l y n e c e s s a r y . R a t h e r , t h e r e p l i c a t o r s h o u l d b e t h o u g h t o f a s h a v i n g extended p h e n o t y p i c effects, c o n s i s t i n g o f a l l its effects o n the w o r l d a t l a r g e , n o t j u s t its effects o n t h e i n d i v i d u a l b o d y i n w h i c h i t h a p p e n s to be sitting. To return to the a n a l o g y of the N e c k e r C u b e , the mental flip that I want t o e n c o u r a g e c a n b e c h a r a c t e r i z e d a s f o l l o w s . W e l o o k a t life a n d b e g i n b y seeing a collection of interacting individual organisms. We know that they c o n t a i n smaller units, a n d we k n o w that they are, in turn, parts of larger c o m p o s i t e units, but w e f i x our g a z e o n the w h o l e organisms. T h e n suddenly t h e i m a g e f l i p s . T h e i n d i v i d u a l b o d i e s a r e still t h e r e ; t h e y h a v e n o t m o v e d ,
Necker
but
they seem
to
have
gone
transparent.
We
Cubes
see
and
through
Buffaloes
them
to
5
the
r e p l i c a t i n g f r a g m e n t s o f D N A w i t h i n , a n d w e see t h e w i d e r w o r l d a s a n arena
in
which
these
genetic
fragments
play
out
their
tournaments
of
m a n i p u l a t i v e skill. G e n e s m a n i p u l a t e t h e w o r l d a n d s h a p e i t t o assist t h e i r replication. It happens that they h a v e 'chosen' to do so largely by m o u l d i n g m a t t e r i n t o l a r g e m u l t i c e l l u l a r c h u n k s w h i c h w e c a l l o r g a n i s m s , b u t this m i g h t n o t h a v e b e e n so. F u n d a m e n t a l l y , w h a t i s g o i n g o n i s t h a t r e p l i c a t i n g m o l e c u l e s e n s u r e t h e i r s u r v i v a l b y m e a n s o f p h e n o t y p i c effects o n t h e w o r l d . It is only incidentally
true
that
those p h e n o t y p i c
effects
happen
to
be
p a c k a g e d up into units c a l l e d i n d i v i d u a l o r g a n i s m s . We
do
not
phenomenon
at it
present
is.
We
appreciate
are
the
accustomed
organism to
for
asking,
the
remarkable
of any
widespread
b i o l o g i c a l p h e n o m e n o n , ' W h a t i s its s u r v i v a l v a l u e ? ' B u t w e d o n o t s a y , ' W h a t i s t h e s u r v i v a l v a l u e o f p a c k a g i n g life u p i n t o d i s c r e t e u n i t s c a l l e d o r g a n i s m s ? ' W e a c c e p t i t a s a g i v e n f e a t u r e o f t h e w a y life is. A s I h a v e already noted, the o r g a n i s m b e c o m e s the a u t o m a t i c subject of o u r questions a b o u t the s u r v i v a l v a l u e o f o t h e r t h i n g s : ' I n w h a t w a y d o e s this b e h a v i o u r p a t t e r n b e n e f i t the i n d i v i d u a l d o i n g i t ? I n w h a t w a y d o e s this m o r p h o l o g i c a l structure benefit the i n d i v i d u a l it is a t t a c h e d t o ? ' It has
become
a kind
of 'central
theorem'
(Barash
1977)
of m o d e r n
ethology that organisms are e x p e c t e d to b e h a v e in such a w a y as to benefit their
own
inclusive
fitness
(Hamilton
1964a,b),
rather
than
to
benefit
a n y o n e , o r a n y t h i n g , else. W e d o n o t ask i n w h a t w a y t h e b e h a v i o u r o f t h e left h i n d l e g b e n e f i t s t h e left h i n d l e g . N o r , n o w a d a y s , d o m o s t o f u s ask h o w the b e h a v i o u r o f a g r o u p o f o r g a n i s m s , o r t h e s t r u c t u r e o f a n e c o s y s t e m , benefits
that
group
or
ecosystem.
We
treat
groups
and
ecosystems
as
collections of warring, or uneasily cohabiting, organisms; a n d we treat legs, k i d n e y s , a n d cells a s c o o p e r a t i n g c o m p o n e n t s o f a s i n g l e o r g a n i s m . I a m n o t necessarily objecting to
this f o c u s o f a t t e n t i o n o n
individual
organisms,
m e r e l y c a l l i n g a t t e n t i o n t o i t a s s o m e t h i n g t h a t w e t a k e for g r a n t e d . P e r h a p s we
should
stop
taking
it
for
granted
and
start
wondering
about
the
i n d i v i d u a l o r g a n i s m , a s s o m e t h i n g t h a t n e e d s e x p l a i n i n g i n its o w n r i g h t , just a s w e f o u n d s e x u a l r e p r o d u c t i o n t o b e s o m e t h i n g t h a t n e e d s e x p l a i n i n g i n its o w n right. A t this p o i n t a n a c c i d e n t o f t h e h i s t o r y o f b i o l o g y n e c e s s i t a t e s a t i r e s o m e digression. T h e p r e v a i l i n g o r t h o d o x y o f m y p r e v i o u s p a r a g r a p h , the c e n t r a l d o g m a of individual organisms w o r k i n g to m a x i m i z e their o w n r e p r o d u c t i v e success, t h e p a r a d i g m o f ' t h e selfish o r g a n i s m ' , w a s D a r w i n ' s p a r a d i g m , a n d it is d o m i n a n t today. O n e m i g h t i m a g i n e , therefore, that it had h a d a g o o d run for its m o n e y a n d s h o u l d , b y n o w , b e r i p e for r e v o l u t i o n , o r a t l e a s t constitute a solid-enough bastion to withstand iconoclastic pinpricks such as a n y t h a t this b o o k m i g h t d e l i v e r . U n f o r t u n a t e l y , a n d this i s t h e h i s t o r i c a l accident I m e n t i o n e d , a l t h o u g h it is true that there has s e l d o m b e e n a n y
N e c k e r C u b e s a n d Buffaloes
6
t e m p t a t i o n t o t r e a t u n i t s s m a l l e r t h a n t h e o r g a n i s m a s a g e n t s w o r k i n g for their o w n benefit, the s a m e has not a l w a y s been true of larger units. T h e i n t e r v e n i n g y e a r s s i n c e D a r w i n h a v e s e e n a n a s t o n i s h i n g r e t r e a t from his individual-centred
stand,
a
lapse
into
sloppily
unconscious
group-
selectionism, ably d o c u m e n t e d by W i l l i a m s (1966), Ghiselin (1974a) and o t h e r s . A s H a m i l t o n ( 1 9 7 5 a ) p u t it, ' . . . a l m o s t t h e w h o l e field o f b i o l o g y s t a m p e d e d in the d i r e c t i o n w h e r e D a r w i n h a d g o n e c i r c u m s p e c t l y or not at a l l ' . I t i s o n l y i n r e c e n t y e a r s , r o u g h l y c o i n c i d i n g w i t h t h e b e l a t e d rise t o f a s h i o n o f H a m i l t o n ' s o w n i d e a s ( D a w k i n s 1 9 7 9 b ) , t h a t t h e s t a m p e d e has b e e n h a l t e d a n d t u r n e d . W e p a i n f u l l y s t r u g g l e d b a c k , h a r a s s e d b y s n i p i n g from a Jesuitically until
we
sophisticated finally
and
regained
dedicated Darwin's
neo-group-selectionist
ground,
the
position
rearguard, that
I
am
c h a r a c t e r i z i n g b y t h e l a b e l ' t h e selfish o r g a n i s m ' , t h e p o s i t i o n w h i c h , i n its m o d e r n f o r m , is d o m i n a t e d by t h e c o n c e p t of i n c l u s i v e fitness. Yet it is this h a r d - w o n fastness
that
I
m a y seem to
be a b a n d o n i n g here,
abandoning
a l m o s t b e f o r e i t i s p r o p e r l y s e c u r e d ; a n d for w h a t ? F o r a f l i c k e r i n g N e c k e r C u b e , a m e t a p h y s i c a l c h i m e r a called the e x t e n d e d p h e n o t y p e ? N o , t o r e n o u n c e t h o s e g a i n s i s far f r o m m y i n t e n t i o n . T h e p a r a d i g m o f the selfish o r g a n i s m i s v a s t l y p r e f e r a b l e t o w h a t H a m i l t o n ( 1 9 7 7 ) h a s c a l l e d 'the old,
departing
paradigm
of adaptation
for
the
benefit
of the
species'.
' E x t e n d e d p h e n o t y p e ' is misunderstood if it is taken to h a v e a n y connection w i t h a d a p t a t i o n a t t h e l e v e l o f t h e g r o u p . T h e selfish o r g a n i s m , a n d the selfish g e n e w i t h its e x t e n d e d p h e n o t y p e , a r e t w o v i e w s o f t h e s a m e N e c k e r C u b e . T h e r e a d e r w i l l n o t e x p e r i e n c e t h e c o n c e p t u a l f l i p - o v e r t h a t I seek t o assist u n l e s s h e b e g i n s b y l o o k i n g a t t h e r i g h t c u b e . T h i s b o o k i s a d d r e s s e d t o those that a l r e a d y a c c e p t the currently fashionable selfish-organism view of life, r a t h e r t h a n a n y f o r m o f ' g r o u p b e n e f i t ' v i e w . I a m n o t s a y i n g t h a t t h e selfish o r g a n i s m v i e w i s n e c e s s a r i l y w r o n g , b u t m y a r g u m e n t , i n its s t r o n g f o r m , i s t h a t i t i s l o o k i n g a t the m a t t e r t h e w r o n g w a y u p . I o n c e o v e r h e a r d an e m i n e n t C a m b r i d g e ethologist say to an eminent Austrian ethologist (they were a r g u i n g about behaviour d e v e l o p m e n t ) : ' Y o u k n o w , w e r e a l l y a g r e e . I t i s j u s t t h a t y o u say i t w r o n g . ' G e n t l e ' i n d i v i d u a l s e l e c t i o n i s t ' , w e r e a l l y d o a l m o s t a g r e e , a t least i n c o m p a r i s o n t o the g r o u p s e l e c t i o n i s t s . I t i s j u s t t h a t y o u see i t w r o n g ! B o n n e r ( 1 9 5 8 ) , discussing single-celled organisms, said ' . . . w h a t special u s e t o t h e s e o r g a n i s m s a r e n u c l e a r g e n e s ? H o w d i d t h e y arise b y s e l e c t i o n ? ' This is a g o o d e x a m p l e of the kind of i m a g i n a t i v e , r a d i c a l question that I t h i n k w e o u g h t t o a s k a b o u t life. B u t i f t h e thesis o f this b o o k i s a c c e p t e d , the particular question should be turned upside d o w n . Instead of asking of what use n u c l e a r g e n e s a r e t o organisms, w e s h o u l d ask w h y genes c h o s e t o g r o u p t h e m s e l v e s t o g e t h e r i n n u c l e i , a n d i n o r g a n i s m s . I n the o p e n i n g lines o f the same work, B o n n e r says: 'I do not propose to say a n y t h i n g new or original in these lectures. B u t I am a g r e a t b e l i e v e r in s a y i n g familiar, w e l l - k n o w n
N e c k e r C u b e s a n d Buffaloes
7
things b a c k w a r d s a n d inside out, h o p i n g that from s o m e n e w v a n t a g e p o i n t the o l d facts w i l l t a k e o n a d e e p e r s i g n i f i c a n c e . I t i s l i k e h o l d i n g a n a b s t r a c t painting upside d o w n ; I do not say that the m e a n i n g of the picture will suddenly be clear, but s o m e of the structure of the c o m p o s i t i o n that w a s hidden m a y show itself
(p.
I).
I c a m e a c r o s s this after w r i t i n g m y o w n
Necker C u b e passage, and was delighted to find the same v i e w s expressed by so respected an author. T h e trouble with my Necker Cubes, and with Bonner's abstract painting, is that, as analogies, they m a y be too timid a n d u n a m b i t i o u s . T h e a n a l o g y o f the N e c k e r C u b e e x p r e s s e s m y minimum h o p e for this b o o k . I a m p r e t t y confident that to look
a t life i n t e r m s o f g e n e t i c r e p l i c a t o r s p r e s e r v i n g
t h e m s e l v e s b y m e a n s o f t h e i r e x t e n d e d p h e n o t y p e s i s a t least a s s a t i s f a c t o r y a s t o l o o k a t i t i n t e r m s o f selfish o r g a n i s m s m a x i m i z i n g t h e i r i n c l u s i v e fitness. I n m a n y c a s e s t h e t w o w a y s o f l o o k i n g a t life w i l l , i n d e e d , b e e q u i v a l e n t . A s I shall s h o w , ' i n c l u s i v e f i t n e s s ' w a s d e f i n e d i n s u c h a w a y a s t o t e n d t o m a k e ' t h e i n d i v i d u a l m a x i m i z e s its i n c l u s i v e f i t n e s s ' e q u i v a l e n t t o ' t h e g e n e t i c replicators m a x i m i z e their s u r v i v a l ' . At least, therefore, the biologist s h o u l d try b o t h w a y s o f t h i n k i n g , a n d c h o o s e t h e o n e h e o r s h e p r e f e r s . B u t I s a i d this w a s a m i n i m u m h o p e . I s h a l l discuss p h e n o m e n a , ' m e i o t i c d r i v e ' for instance, w h o s e e x p l a n a t i o n is l u c i d l y written on the se c on d face of the c u b e , b u t w h i c h m a k e n o sense a t all i f w e k e e p o u r m e n t a l g a z e f i r m l y f i x e d o n t h e o t h e r f a c e , t h a t o f t h e selfish o r g a n i s m . M o v i n g f r o m m y m i n i m u m h o p e t o my wildest d a y d r e a m , it is that w h o l e areas of b i o l o g y , the s t u d y of a n i m a l communication, ecology,
indeed
animal all
artefacts,
interactions
parasitism between
and and
symbiosis, within
community
organisms,
will
eventually b e i l l u m i n a t e d i n n e w w a y s b y the d o c t r i n e o f the e x t e n d e d p h e n o t y p e . As is the w a y w i t h a d v o c a t e s , I shall try to m a k e the strongest c a s e I c a n , a n d this m e a n s t h e c a s e for t h e w i l d e r h o p e s r a t h e r t h a n t h e m o r e cautious m i n i m u m expectations. I f these g r a n d i o s e h o p e s a r e e v e n t u a l l y r e a l i z e d , p e r h a p s a less m o d e s t a n a l o g y t h a n the N e c k e r C u b e w i l l b e p a r d o n e d . C o l i n T u r n b u l l ( 1 9 6 1 ) t o o k a p y g m y friend, K e n g e , o u t o f t h e forest for t h e f i r s t t i m e i n his life, a n d t h e y climbed a m o u n t a i n together a n d looked out o v e r the plains. K e n g e s a w s o m e b u f f a l o ' g r a z i n g l a z i l y s e v e r a l m i l e s a w a y , far d o w n b e l o w . H e t u r n e d t o m e and said. " W h a t insects are t h o s e ? " . . . A t f i r s t I h a r d l y u n d e r s t o o d , t h e n I r e a l i z e d t h a t in t h e forest v i s i o n is so l i m i t e d t h a t t h e r e is no g r e a t n e e d t o m a k e a n a u t o m a t i c a l l o w a n c e for d i s t a n c e w h e n j u d g i n g s i z e . O u t h e r e i n t h e p l a i n s , K e n g e w a s l o o k i n g for t h e f i r s t t i m e o v e r a p p a r e n t l y u n e n d i n g miles of unfamiliar grasslands, w i t h not a tree w o r t h the n a m e to g i v e h i m a n y basis for c o m p a r i s o n . . . W h e n I t o l d K e n g e t h a t t h e i n s e c t s w e r e buffalo, he roared w i t h l a u g h t e r a n d told me not to tell s u c h stupid lies . . . ' ( p p . 2 2 7 - 2 2 8 ) . T h i s b o o k as a w h o l e , t h e n , is a w o r k of a d v o c a c y , b u t it is a p o o r a d v o c a t e
N e c k e r C u b e s a n d Buffaloes
t h a t l e a p s p r e c i p i t a t e l y t o his c o n c l u s i o n w h e n t h e j u r y a r e s c e p t i c a l . T h e second face of my N e c k e r C u b e is unlikely to click into clear focus until near t h e e n d o f t h e b o o k . E a r l i e r c h a p t e r s p r e p a r e t h e g r o u n d , a t t e m p t t o forestall c e r t a i n risks o f m i s u n d e r s t a n d i n g , d i s s e c t t h e first f a c e o f t h e N e c k e r C u b e i n v a r i o u s w a y s , p o i n t u p r e a s o n s w h y t h e p a r a d i g m o f t h e selfish i n d i v i d u a l , i f not a c t u a l l y i n c o r r e c t , c a n l e a d to difficulties. Parts of some early chapters are frankly retrospective and even defensive. R e a c t i o n t o a p r e v i o u s w o r k ( D a w k i n s 1 9 7 6 a ) s u g g e s t s t h a t this b o o k i s l i k e l y t o r a i s e n e e d l e s s fears t h a t i t p r o m u l g a t e s t w o u n p o p u l a r ' - i s m s ' — ' g e n e t i c d e t e r m i n i s m ' a n d 'adaptationism'. I m y s e l f a d m i t to b e i n g irritated by a book that p r o v o k e s me into m u t t e r i n g ' Y e s b u t . . .' on e v e r y p a g e , w h e n the author c o u l d e a s i l y h a v e f o r e s t a l l e d m y w o r r y b y a little c o n s i d e r a t e e x p l a n a t i o n e a r l y o n . C h a p t e r s 2 a n d 3 t r y t o r e m o v e a t least t w o m a j o r s o u r c e s o f ' y e s buttery' at the outset. C h a p t e r 4 o p e n s t h e c a s e for t h e p r o s e c u t i o n a g a i n s t t h e selfish o r g a n i s m , a n d begins to hint at the s e c o n d aspect of the N e c k e r C u b e . C h a p t e r 5 opens t h e c a s e for t h e ' r e p l i c a t o r '
as the f u n d a m e n t a l unit of natural selection.
C h a p t e r 6 r e t u r n s t o t h e i n d i v i d u a l o r g a n i s m a n d s h o w s h o w n e i t h e r it, n o r a n y other m a j o r c a n d i d a t e e x c e p t the small genetic fragment, qualifies as a true replicator. R a t h e r , the individual organism should be thought of as a ' v e h i c l e ' for r e p l i c a t o r s . C h a p t e r 7 is a d i g r e s s i o n on r e s e a r c h m e t h o d o l o g y . C h a p t e r 8 raises s o m e a w k w a r d a n o m a l i e s for t h e selfish o r g a n i s m , a n d C h a p t e r 9 continues the theme.
Chapter
10 discusses v a r i o u s notions of
'individual fitness', and concludes that they are confusing, and probably dispensable. Chapters
11,
12 and
1 3 are the heart o f the book. T h e y d e v e l o p , b y
g r a d u a l d e g r e e s , t h e i d e a o f t h e e x t e n d e d p h e n o t y p e itself, t h e s e c o n d face o f the N e c k e r C u b e .
Finally, in Chapter
1 4 , w e t u r n b a c k w i t h refreshed
c u r i o s i t y t o t h e i n d i v i d u a l o r g a n i s m a n d ask w h y , after a l l , i t i s s u c h a salient l e v e l i n t h e h i e r a r c h y o f life.
•
2 Genetic D e t e r m i n i s m and Gene Selectionism
L o n g after his d e a t h , t e n a c i o u s r u m o u r s p e r s i s t e d t h a t A d o l f H i t l e r h a d b e e n s e e n a l i v e a n d w e l l i n S o u t h A m e r i c a , o r i n D e n m a r k , a n d for y e a r s a s u r p r i s i n g n u m b e r o f p e o p l e w i t h n o l o v e for t h e m a n o n l y r e l u c t a n t l y accepted that he w a s d e a d ( T r e v o r - R o p e r 1 9 7 2 ) . In the First W o r l d W a r a story t h a t a h u n d r e d Scotland
thousand Russian troops had
'with snow on
their boots'
been seen l a n d i n g in
b e c a m e widely current,
apparently
because o f the m e m o r a b l e vividness o f that s n o w ( T a y l o r 1 9 6 3 ) . I n o u r o w n time
myths
such
as
that
of computers
persistently
sending
householders
e l e c t r i c i t y bills for a m i l l i o n p o u n d s ( E v a n s 1 9 7 9 ) , o r o f w e l l - h e e l e d w e l f a r e scroungers
with
two
expensive
cars
parked
outside
their
government-
subsidized council houses, are familiar to the point of cliche. T h e r e are some falsehoods, or half-truths, that seem to e n g e n d e r in us an a c t i v e desire to b e l i e v e t h e m a n d pass t h e m o n e v e n i f w e find t h e m u n p l e a s a n t , m a y b e i n p a r t , p e r v e r s e l y , because w e find t h e m u n p l e a s a n t . C o m p u t e r s a n d e l e c t r o n i c ' c h i p s ' p r o v o k e m o r e t h a n t h e i r fair s h a r e o f such m y t h - m a k i n g ,
perhaps because c o m p u t e r technology advances at a
speed w h i c h i s l i t e r a l l y f r i g h t e n i n g . I k n o w a n o l d p e r s o n w h o h a s i t o n g o o d authority that 'chips' are u s u r p i n g h u m a n functions to the extent not o n l y of 'driving tractors' but even of 'fertilizing w o m e n ' . G e n e s , as I shall show, are the s o u r c e o f w h a t m a y b e
an
even larger mythology
than computers.
I m a g i n e t h e result o f c o m b i n i n g t h e s e t w o p o w e r f u l m y t h s , t h e g e n e m y t h a n d the c o m p u t e r m y t h ! I b e l i e v e t h a t I m a y h a v e i n a d v e r t e n t l y a c h i e v e d some such unfortunate synthesis in the m i n d s of a few readers of my p r e v i o u s book,
and
the
result
was
comic
misunderstanding.
Happily,
such
mis-
understanding was not widespread, but it is w o r t h trying to a v o i d a repeat of it here, and that is o n e purpose of the present c h a p t e r . I shall e x p o s e the myth of genetic d e t e r m i n i s m , a n d e x p l a i n w h y it is necessary to use l a n g u a g e that c a n b e u n f o r t u n a t e l y m i s u n d e r s t o o d a s g e n e t i c d e t e r m i n i s m . A r e v i e w e r of W i l s o n ' s ( 1 9 7 8 )
On Human Nature, w r o t e :
' . . . a l t h o u g h he
does n o t go as far as R i c h a r d D a w k i n s (The Selfish Gene . . . ) in p r o p o s i n g s e x 9
10
G e n e t i c D e t e r m i n i s m and G e n e S e l e c t i o n i s m
l i n k e d g e n e s for " p h i l a n d e r i n g " , for W i l s o n h u m a n m a l e s h a v e a g e n e t i c tendency towards p o l y g y n y , females towards constancy (don't blame your m a t e s for s l e e p i n g a r o u n d , l a d i e s , it's n o t t h e i r f a u l t t h e y a r e g e n e t i c a l l y p r o g r a m m e d ) . G e n e t i c d e t e r m i n i s m c o n s t a n t l y c r e e p s i n a t the b a c k d o o r ' (Rose
1 9 7 8 ) . T h e r e v i e w e r ' s clear i m p l i c a t i o n is that the authors he is
c r i t i c i z i n g b e l i e v e in the existence of genes that force h u m a n males to be irremediable infidelity.
philanderers
The
who
cannot
r e a d e r i s left w i t h
therefore
be
the impression
blamed
that
for
marital
those authors are
protagonists in the 'nature or nurture' debate, and, moreover, died-in-thewool hereditarians with male chauvinist leanings. I n fact humans.
my original
passage about
'philanderer males'
w a s not about
It w a s a simple m a t h e m a t i c a l m o d e l of some unspecified animal
( n o t t h a t it m a t t e r s , I h a d a b i r d in m i n d ) . It w a s n o t e x p l i c i t l y (see b e l o w ) a m o d e l o f g e n e s , a n d i f i t h a d b e e n a b o u t g e n e s t h e y w o u l d h a v e b e e n sexl i m i t e d , n o t s e x - l i n k e d ! I t w a s a m o d e l o f ' s t r a t e g i e s ' i n t h e sense o f M a y n a r d Smith
( 1 9 7 4 ) . T h e ' p h i l a n d e r e r ' s t r a t e g y w a s p o s t u l a t e d , n o t a s the w a y
males b e h a v e , but as one of t w o hypothetical alternatives, the other being t h e ' f a i t h f u l ' s t r a t e g y . T h e p u r p o s e o f this v e r y s i m p l e m o d e l w a s t o illustrate the kinds of conditions under w h i c h philandering might be favoured by n a t u r a l s e l e c t i o n , a n d t h e k i n d s o f c o n d i t i o n s u n d e r w h i c h faithfulness m i g h t b e f a v o u r e d . T h e r e w a s n o p r e s u m p t i o n that p h i l a n d e r i n g w a s m o r e likely i n m a l e s t h a n f a i t h f u l n e s s . I n d e e d , t h e p a r t i c u l a r r u n o f t h e s i m u l a t i o n that I published
culminated
i n a m i x e d m a l e p o p u l a t i o n i n w h i c h faithfulness
slightly p r e d o m i n a t e d ( D a w k i n s 1976a, p.
1 6 5 , a l t h o u g h see S c h u s t e r &
S i g m u n d 1 9 8 1 ) . T h e r e is not just one misunderstanding in Rose's remarks, but multiple c o m p o u n d e d misunderstanding. T h e r e is a w a n t o n eagerness to misunderstand.
It bears the stamp of snow-covered Russian jackboots, of
little b l a c k m i c r o c h i p s m a r c h i n g to usurp the m a l e role and steal o u r tractord r i v e r s ' j o b s . It is a m a n i f e s t a t i o n of a p o w e r f u l m y t h , in this c a s e the g r e a t gene myth. T h e g e n e m y t h i s e p i t o m i z e d i n R o s e ' s p a r e n t h e t i c little j o k e a b o u t l a d i e s n o t b l a m i n g t h e i r m a t e s for s l e e p i n g a r o u n d .
It is the m y t h of 'genetic
d e t e r m i n i s m ' . E v i d e n t l y , for R o s e , g e n e t i c d e t e r m i n i s m i s d e t e r m i n i s m i n the full p h i l o s o p h i c a l s e n s e o f i r r e v e r s i b l e i n e v i t a b i l i t y .
H e a s s u m e s t h a t the
e x i s t e n c e o f a g e n e ' f o r ' X i m p l i e s t h a t X c a n n o t b e e s c a p e d . I n the w o r d s o f another critic of 'genetic determinism', G o u l d
( 1 9 7 8 , p . 238), ' I f w e are
p r o g r a m m e d t o b e w h a t w e a r e , t h e n these traits a r e i n e l u c t a b l e . W e m a y , a t best, c h a n n e l t h e m , but we c a n n o t c h a n g e t h e m either by will, e d u c a t i o n , or culture.' T h e v a l i d i t y o f t h e d e t e r m i n i s t p o i n t o f v i e w a n d , s e p a r a t e l y , its b e a r i n g o n a n i n d i v i d u a l ' s m o r a l r e s p o n s i b i l i t y for his a c t i o n s , h a s b e e n d e b a t e d b y p h i l o s o p h e r s a n d t h e o l o g i a n s for c e n t u r i e s p a s t , a n d n o d o u b t w i l l b e for centuries to c o m e . I suspect that both R o s e and G o u l d are determinists in
Genetic D e t e r m i n i s m and Gene Selectionism
11
that t h e y b e l i e v e i n a p h y s i c a l , m a t e r i a l i s t i c basis for a l l o u r a c t i o n s . S o a m I . We w o u l d also p r o b a b l y all three agree that h u m a n nervous systems are so c o m p l e x that in practice we c a n forget a b o u t d e t e r m i n i s m a n d b e h a v e as if w e h a d free w i l l . N e u r o n e s m a y b e a m p l i f i e r s o f f u n d a m e n t a l l y i n d e t e r m i n a t e physical events. T h e only point I wish to m a k e is that, w h a t e v e r v i e w one t a k e s o n the q u e s t i o n o f d e t e r m i n i s m , t h e i n s e r t i o n o f t h e w o r d ' g e n e t i c ' i s not g o i n g t o m a k e a n y d i f f e r e n c e . I f y o u a r e a f u l l - b l o o d e d d e t e r m i n i s t y o u w i l l b e l i e v e t h a t all y o u r a c t i o n s a r e p r e d e t e r m i n e d b y p h y s i c a l c a u s e s i n t h e past, a n d y o u m a y o r m a y n o t a l s o b e l i e v e t h a t y o u t h e r e f o r e c a n n o t b e h e l d responsible
for
your sexual
infidelities.
But,
be
that
as
it
may,
what
difference c a n it possibly m a k e w h e t h e r some of those p h y s i c a l causes are genetic? W h y a r e g e n e t i c d e t e r m i n a n t s t h o u g h t t o b e a n y m o r e i n e l u c t a b l e , o r blame-absolving, than 'environmental' ones? T h e belief that genes are s o m e h o w super-deterministic,
in comparison
with environmental causes, is a m y t h of extraordinary tenacity, and it c a n g i v e rise t o r e a l e m o t i o n a l distress. I w a s o n l y d i m l y a w a r e o f this u n t i l i t w a s m o v i n g l y b r o u g h t h o m e t o m e i n a q u e s t i o n session a t a m e e t i n g o f t h e A m e r i c a n A s s o c i a t i o n for t h e A d v a n c e m e n t o f S c i e n c e i n 1 9 7 8 . A y o u n g w o m a n asked the lecturer, a p r o m i n e n t 'sociobiologist', w h e t h e r there w a s a n y e v i d e n c e for g e n e t i c sex d i f f e r e n c e s i n h u m a n p s y c h o l o g y . I h a r d l y h e a r d the l e c t u r e r ' s a n s w e r , s o a s t o n i s h e d w a s I b y t h e e m o t i o n w i t h w h i c h t h e q u e s t i o n w a s p u t . T h e w o m a n s e e m e d t o set g r e a t s t o r e b y t h e a n s w e r a n d was almost in tears. A f t e r a m o m e n t of g e n u i n e a n d i n n o c e n t bafflement the explanation
hit m e .
Something or somebody,
certainly not
the eminent
s o c i o b i o l o g i s t himself, h a d m i s l e d h e r i n t o t h i n k i n g t h a t g e n e t i c d e t e r m i n a t i o n i s for k e e p s ; s h e s e r i o u s l y b e l i e v e d t h a t a ' y e s ' a n s w e r t o h e r q u e s t i o n w o u l d , i f c o r r e c t , c o n d e m n h e r a s a f e m a l e i n d i v i d u a l t o a life o f f e m i n i n e pursuits, c h a i n e d t o t h e n u r s e r y a n d t h e k i t c h e n sink. B u t if, u n l i k e m o s t o f us, she is a d e t e r m i n i s t in t h a t s t r o n g C a l v i n i s t i c sense, s h e s h o u l d be e q u a l l y upset w h e t h e r t h e c a u s a l f a c t o r s c o n c e r n e d a r e g e n e t i c o r ' e n v i r o n m e n t a l ' . W h a t does it ever m e a n to say that s o m e t h i n g d e t e r m i n e s s o m e t h i n g ? Philosophers, possibly w i t h justification, m a k e h e a v y w e a t h e r of the c o n c e p t of c a u s a t i o n , b u t to a w o r k i n g b i o l o g i s t c a u s a t i o n is a r a t h e r s i m p l e s t a t i s t i c a l concept. O p e r a t i o n a l l y we c a n never demonstrate that a particular observed e v e n t C c a u s e d a p a r t i c u l a r r e s u l t R , a l t h o u g h i t w i l l often b e j u d g e d h i g h l y likely. W h a t b i o l o g i s t s i n p r a c t i c e u s u a l l y d o i s t o e s t a b l i s h statistically t h a t events o f class R r e l i a b l y f o l l o w e v e n t s o f class C . T h e y n e e d a n u m b e r o f p a i r e d i n s t a n c e s o f t h e t w o classes o f e v e n t s i n o r d e r t o d o s o : o n e a n e c d o t e i s not e n o u g h . E v e n t h e o b s e r v a t i o n t h a t R e v e n t s r e l i a b l y t e n d to f o l l o w C e v e n t s after a relatively fixed time interval provides o n l y a w o r k i n g hypothesis that C events c a u s e R e v e n t s . T h e h y p o t h e s i s i s c o n f i r m e d , w i t h i n t h e l i m i t s o f t h e statistical m e t h o d , o n l y i f t h e C e v e n t s a r e d e l i v e r e d b y a n experimenter r a t h e r
12
G e n e t i c D e t e r m i n i s m and G e n e S e l e c t i o n i s m
t h a n s i m p l y n o t e d b y a n o b s e r v e r , a n d a r e still r e l i a b l y f o l l o w e d b y R e v e n t s . It is not necessary that e v e r y C should be followed by an R, nor that every R s h o u l d b e p r e c e d e d b y a C ( w h o has n o t h a d t o c o n t e n d w i t h a r g u m e n t s s u c h as 'smoking c a n n o t cause l u n g cancer, because I knew a non-smoker w h o d i e d o f it,
and
a
h e a v y s m o k e r w h o i s still g o i n g s t r o n g a t n i n e t y ' ? ) .
S t a t i s t i c a l m e t h o d s a r e d e s i g n e d t o h e l p u s assess, t o a n y s p e c i f i e d l e v e l o f probabilistic confidence,
w h e t h e r t h e results w e o b t a i n
really indicate a
causal relationship. If, t h e n , it w e r e t r u e t h a t t h e possession of a Y c h r o m o s o m e h a d a c a u s a l i n f l u e n c e o n , s a y , m u s i c a l a b i l i t y o r f o n d n e s s for k n i t t i n g , w h a t w o u l d this mean?
It
would
mean
that,
in s o m e specified
population
and
in some
s p e c i f i e d e n v i r o n m e n t , a n o b s e r v e r i n possession o f i n f o r m a t i o n a b o u t a n individual's
sex
would
be
able
to
make
a
statistically
more
accurate
p r e d i c t i o n a s t o t h e p e r s o n ' s m u s i c a l a b i l i t y t h a n a n o b s e r v e r i g n o r a n t o f the p e r s o n ' s s e x . T h e e m p h a s i s i s o n t h e w o r d ' s t a t i s t i c a l l y ' , a n d let u s t h r o w i n an
'other things being e q u a l '
for g o o d
measure. T h e observer might be
p r o v i d e d w i t h s o m e a d d i t i o n a l information, say on the person's e d u c a t i o n or u p b r i n g i n g , w h i c h w o u l d l e a d h i m t o r e v i s e , o r e v e n r e v e r s e , his p r e d i c t i o n based on sex.
I f f e m a l e s a r e s t a t i s t i c a l l y m o r e l i k e l y t h a n m a l e s t o enjoy
k n i t t i n g , this d o e s n o t m e a n t h a t a l l f e m a l e s e n j o y k n i t t i n g , n o r e v e n that a majority do. It is also fully c o m p a t i b l e w i t h the v i e w that the reason females enjoy knitting
is
that
society
brings
them
up
to
enjoy
knitting.
If society
s y s t e m a t i c a l l y t r a i n s c h i l d r e n w i t h o u t p e n i s e s t o k n i t a n d p l a y w i t h dolls, a n d t r a i n s c h i l d r e n w i t h p e n i s e s t o p l a y w i t h g u n s a n d t o y soldiers, a n y resulting differences in m a l e a n d female preferences are strictly speaking genetically
determined
differences!
They
are
determined,
through
the
m e d i u m o f s o c i e t a l c u s t o m , b y t h e fact o f possession o r n o n - p o s s e s s i o n o f a p e n i s , a n d t h a t i s d e t e r m i n e d (in a n o r m a l e n v i r o n m e n t a n d i n the a b s e n c e o f i n g e n i o u s p l a s t i c s u r g e r y o r h o r m o n e t h e r a p y ) b y sex c h r o m o s o m e s . O b v i o u s l y , o n this v i e w , i f w e e x p e r i m e n t a l l y b r o u g h t u p a s a m p l e o f b o y s to p l a y w i t h dolls a n d a s a m p l e of girls to p l a y w i t h guns, we w o u l d expect easily
to
reverse
the
normal
preferences.
This
might
be
an
interesting
e x p e r i m e n t t o d o , for t h e r e s u l t j u s t m i g h t t u r n o u t t o b e t h a t g i r l s still prefer d o l l s a n d b o y s still p r e f e r g u n s . I f so, this m i g h t tell u s s o m e t h i n g a b o u t the t e n a c i t y , in t h e f a c e of a particular e n v i r o n m e n t a l m a n i p u l a t i o n , of a g e n e t i c difference.
But
all
genetic
causes
have
to
work
in
the
context
of an
e n v i r o n m e n t o f s o m e k i n d . I f a g e n e t i c sex d i f f e r e n c e m a k e s i t s e l f felt t h r o u g h t h e m e d i u m o f a s e x - b i a s e d e d u c a t i o n s y s t e m , i t i s still a g e n e t i c d i f f e r e n c e . I f i t m a k e s i t s e l f felt t h r o u g h s o m e o t h e r m e d i u m , s u c h t h a t m a n i p u l a t i o n s o f t h e e d u c a t i o n s y s t e m d o n o t p e r t u r b it, i t is, i n p r i n c i p l e , n o m o r e a n d n o less a genetic difference than in the former, education-sensitive case: no doubt s o m e o t h e r e n v i r o n m e n t a l m a n i p u l a t i o n c o u l d b e f o u n d w h i c h did p e r t u r b it.
Genetic D e t e r m i n i s m and G e n e S e l e c t i o n i s m
13
H u m a n psychological attributes vary along almost as m a n y dimensions as p s y c h o l o g i s t s c a n m e a s u r e . I t i s difficult i n p r a c t i c e ( K e m p t h o r n e 1 9 7 8 ) , b u t i n p r i n c i p l e w e c o u l d p a r t i t i o n this v a r i a t i o n a m o n g s u c h p u t a t i v e c a u s a l factors a s a g e , h e i g h t , y e a r s o f e d u c a t i o n , t y p e o f e d u c a t i o n c l a s s i f i e d i n m a n y different w a y s , n u m b e r o f s i b l i n g s , b i r t h o r d e r , c o l o u r o f m o t h e r ' s e y e s , father's skill i n s h o e i n g h o r s e s , a n d , o f c o u r s e , s e x c h r o m o s o m e s . W e c o u l d also e x a m i n e t w o - w a y a n d m u l t i - w a y i n t e r a c t i o n s b e t w e e n s u c h f a c t o r s . F o r present purposes the i m p o r t a n t point is that the v a r i a n c e we seek to e x p l a i n will h a v e m a n y causes, w h i c h interact i n c o m p l e x w a y s . genetic
variance
is
a significant cause of m u c h
Undoubtedly
p h e n o t y p i c v a r i a n c e in
o b s e r v e d p o p u l a t i o n s , b u t its effects m a y b e o v e r r i d d e n , m o d i f i e d , e n h a n c e d o r r e v e r s e d b y o t h e r c a u s e s . G e n e s m a y m o d i f y t h e effects o f o t h e r g e n e s , a n d m a y modify
t h e effects o f t h e e n v i r o n m e n t .
Environmental
events,
both
i n t e r n a l a n d e x t e r n a l , m a y m o d i f y t h e effects o f g e n e s , a n d m a y m o d i f y t h e effects o f o t h e r e n v i r o n m e n t a l e v e n t s . P e o p l e s e e m t o h a v e little d i f f i c u l t y i n a c c e p t i n g t h e m o d i f i a b i l i t y o f 'environmental'
effects o n
human
development.
If a
child
has
had
bad
teaching in m a t h e m a t i c s , it is a c c e p t e d that the resulting d e f i c i e n c y c a n be r e m e d i e d b y e x t r a g o o d t e a c h i n g the f o l l o w i n g y e a r . B u t a n y s u g g e s t i o n t h a t the c h i l d ' s m a t h e m a t i c a l d e f i c i e n c y m i g h t h a v e a g e n e t i c o r i g i n i s l i k e l y t o b e greeted with something a p p r o a c h i n g despair:
i f i t i s i n t h e g e n e s 'it i s
written', it is 'determined' and nothing can be done a b o u t it; y o u m i g h t as well g i v e up a t t e m p t i n g to teach the child m a t h e m a t i c s . T h i s is p e r n i c i o u s rubbish on an almost astrological scale. G e n e t i c causes and e n v i r o n m e n t a l causes are in principle no different from e a c h other. S o m e influences of b o t h types m a y be hard to reverse; others m a y be easy to reverse. S o m e m a y be usually hard to reverse but easy if the right a g e n t is a p p l i e d . T h e i m p o r t a n t p o i n t i s t h a t t h e r e i s n o g e n e r a l r e a s o n for e x p e c t i n g g e n e t i c i n f l u e n c e s t o b e any more irreversible than environmental ones. W h a t d i d g e n e s d o t o d e s e r v e t h e i r sinister, j u g g e r n a u t - l i k e r e p u t a t i o n ? W h y d o w e n o t m a k e a s i m i l a r b o g e y o u t of, s a y , n u r s e r y e d u c a t i o n o r confirmation classes? W h y are genes t h o u g h t to be so m u c h m o r e fixed a n d i n e s c a p a b l e i n t h e i r effects t h a n t e l e v i s i o n , n u n s , o r b o o k s ? D o n ' t b l a m e y o u r m a t e s for s l e e p i n g a r o u n d , l a d i e s , it's n o t t h e i r f a u l t t h e y h a v e b e e n i n f l a m e d b y p o r n o g r a p h i c l i t e r a t u r e ! T h e a l l e g e d J e s u i t b o a s t , ' G i v e m e t h e c h i l d for his f i r s t s e v e n y e a r s , a n d I ' l l g i v e y o u t h e m a n ' , m a y h a v e s o m e t r u t h i n it. Educational, or other cultural influences m a y , in some circumstances, be just as unmodifiable a n d irreversible as genes a n d 'stars' are p o p u l a r l y t h o u g h t to be. I suppose part of the reason genes h a v e b e c o m e deterministic b o g e y s is a confusion
resulting
from
the
well-known
fact
of the
non-inheritance
of
a c q u i r e d c h a r a c t e r i s t i c s . B e f o r e this c e n t u r y i t w a s w i d e l y b e l i e v e d t h a t experience and other acquisitions of an individual's lifetime w e r e s o m e h o w
Genetic D e t e r m i n i s m and Gene Selectionism
>4
i m p r i n t e d on the h e r e d i t a r y substance and transmitted to the children. T h e a b a n d o n i n g o f this belief, a n d its r e p l a c e m e n t b y W e i s m a n n ' s d o c t r i n e o f the c o n t i n u i t y o f t h e g e r m p l a s m , a n d its m o l e c u l a r c o u n t e r p a r t the ' c e n t r a l d o g m a ' , is o n e of the g r e a t a c h i e v e m e n t s of m o d e r n biology. If we steep ourselves in the implications of W e i s m a n n i a n o r t h o d o x y , there really does seem to be something j u g g e r n a u t - l i k e and inexorable about genes. T h e y march
through
generations,
influencing
the
form
and
behaviour
of a
s u c c e s s i o n o f m o r t a l b o d i e s , b u t , e x c e p t for r a r e a n d n o n - s p e c i f i c m u t a g e n i c effects, t h e y a r e n e v e r i n f l u e n c e d b y t h e e x p e r i e n c e o r e n v i r o n m e n t o f those bodies. T h e g e n e s i n m e c a m e from m y four g r a n d p a r e n t s ;
they flowed
straight t h r o u g h my parents to m e , and n o t h i n g that my parents achieved, acquired,
learned or experienced
h a d a n y effect o n those g e n e s a s t h e y
f l o w e d t h r o u g h . P e r h a p s t h e r e i s s o m e t h i n g a little sinister a b o u t that. B u t , h o w e v e r i n e x o r a b l e a n d u n d e v i a t i n g the g e n e s m a y b e a s t h e y m a r c h d o w n t h e g e n e r a t i o n s , t h e n a t u r e o f t h e i r p h e n o t y p i c effects o n t h e b o d i e s t h e y f l o w t h r o u g h i s b y n o m e a n s i n e x o r a b l e a n d u n d e v i a t i n g . I f I a m h o m o z y g o u s for a g e n e G , n o t h i n g s a v e m u t a t i o n c a n p r e v e n t m y p a s s i n g G o n t o all m y children. So m u c h is inexorable. But whether or not I, or my children, show t h e p h e n o t y p i c effect n o r m a l l y a s s o c i a t e d w i t h possession o f G m a y d e p e n d v e r y m u c h on h o w we are brought up, w h a t diet or education we experience, a n d w h a t o t h e r g e n e s w e h a p p e n t o possess. S o , o f t h e t w o effects t h a t g e n e s have on
the w o r l d — m a n u f a c t u r i n g copies of themselves, and influencing
p h e n o t y p e s — t h e first i s i n f l e x i b l e a p a r t f r o m t h e r a r e p o s s i b i l i t y o f m u t a t i o n ; the
second
evolution
may and
be
exceedingly
d e v e l o p m e n t is,
flexible.
then,
I
think
a
confusion
between
p a r t l y r e s p o n s i b l e for t h e m y t h o f
genetic determinism. But
there is another m y t h c o m p l i c a t i n g matters,
and
I
have already
m e n t i o n e d i t a t t h e b e g i n n i n g o f this c h a p t e r . T h e c o m p u t e r m y t h i s a l m o s t as d e e p - s e a t e d in the m o d e r n m i n d as the g e n e m y t h .
N o t i c e that both
passages I q u o t e d c o n t a i n the w o r d ' p r o g r a m m e d ' . T h u s R o s e sarcastically absolved
promiscuous
men
from
blame
because
they
are
genetically
programmed. G o u l d s a y s t h a t i f w e a r e programmed t o b e w h a t w e a r e t h e n these traits
are
ineluctable.
programmed of action.
And
to indicate
it
is
true
that
we
unthinking inflexibility,
Computers and
'robots'
are,
ordinarily
use
the
word
the antithesis o f f r e e d o m
by repute,
notoriously
inflexible,
c a r r y i n g out instructions to the letter, e v e n if the c o n s e q u e n c e s are obviously a b s u r d . W h y else w o u l d t h e y s e n d o u t t h o s e f a m o u s m i l l i o n p o u n d bills t h a t e v e r y b o d y ' s friend's friend's cousin's a c q u a i n t a n c e keeps r e c e i v i n g ? I had forgotten the great c o m p u t e r m y t h , as well as the great gene m y t h , or I w o u l d h a v e b e e n m o r e careful w h e n I m y s e l f w r o t e o f genes s w a r m i n g 'inside gigantic l u m b e r i n g robots . . . ' , and of ourselves as 'survival machines—robot v e h i c l e s b l i n d l y p r o g r a m m e d t o p r e s e r v e t h e selfish m o l e c u l e s k n o w n a s genes'
(Dawkins
1 9 7 6 a ) . T h e s e passages h a v e been triumphantly quoted,
G e n e t i c D e t e r m i n i s m and G e n e S e l e c t i o n i s m
and
requoted
examples
apparently
of rabid
from
genetic
secondary
determinism
and
even
(e.g.
tertiary
'Nabi'
15
sources,
1981).
I
am
as not
a p o l o g i z i n g for u s i n g t h e l a n g u a g e o f r o b o t i c s . I w o u l d u s e i t a g a i n w i t h o u t hesitation. But I n o w realize that it is necessary to g i v e m o r e e x p l a n a t i o n . F r o m 1 3 y e a r s ' e x p e r i e n c e o f t e a c h i n g it, I k n o w t h a t a m a i n p r o b l e m w i t h the 'selfish-gene s u r v i v a l m a c h i n e ' w a y of l o o k i n g at n a t u r a l selection is a p a r t i c u l a r risk o f m i s u n d e r s t a n d i n g . T h e m e t a p h o r o f t h e i n t e l l i g e n t g e n e r e c k o n i n g u p h o w best t o e n s u r e its o w n s u r v i v a l
(Hamilton
1972)
is a
powerful and i l l u m i n a t i n g one. B u t it is all too easy to get carried a w a y , a n d allow hypothetical genes cognitive w i s d o m and foresight in p l a n n i n g their 'strategy'. A t least three out o f t w e l v e m i s u n d e r s t a n d i n g s o f kin selection (Dawkins
1979a)
a r e d i r e c t l y a t t r i b u t a b l e t o this b a s i c e r r o r . T i m e a n d
again, non-biologists h a v e tried to justify a form of g r o u p selection to me b y , i n effect, i m p u t i n g f o r e s i g h t t o g e n e s :
' T h e l o n g - t e r m interests of a g e n e
require the c o n t i n u e d existence of the species; therefore s h o u l d n ' t y o u e x p e c t adaptations to prevent species extinction, even at the expense of short-term individual r e p r o d u c t i v e success?' It w a s in an a t t e m p t to forestall errors like this t h a t I u s e d the l a n g u a g e o f a u t o m a t i o n a n d r o b o t i c s , a n d u s e d t h e w o r d ' b l i n d l y ' i n r e f e r r i n g t o g e n e t i c p r o g r a m m i n g . B u t i t is, o f c o u r s e , t h e g e n e s that are blind, not the a n i m a l s they p r o g r a m . N e r v o u s systems, like m a n made
computers,
can
be
sufficiently
complex
to
show
intelligence
and
foresight. S y m o n s (1979) m a k e s the c o m p u t e r m y t h e x p l i c i t : I wish to point out that D a w k i n s ' s i m p l i c a t i o n — t h r o u g h the use of words
like
'robot'
and
'blindly'—that
evolutionary
theory
favors
d e t e r m i n i s m is u t t e r l y w i t h o u t f o u n d a t i o n . . . A r o b o t is a m i n d l e s s automaton.
Perhaps some animals are robots
(we have no w a y of
k n o w i n g ) ; h o w e v e r , D a w k i n s i s n o t r e f e r r i n g t o some a n i m a l s , b u t t o a l l a n i m a l s a n d i n this c a s e s p e c i f i c a l l y t o h u m a n b e i n g s . N o w , t o paraphrase Stebbing, 'robot' can be opposed to 'thinking being' or it can
be
used
mechanically,
figuratively but
there
to indicate a person w h o seems is
no
common
usage
to act
of language
that
p r o v i d e s a m e a n i n g for t h e w o r d ' r o b o t ' i n w h i c h i t w o u l d m a k e sense to say that all l i v i n g things are robots [p. 4 1 ] .
T h e point o f the passage from S t e b b i n g w h i c h S y m o n s p a r a p h r a s e d i s the r e a s o n a b l e o n e t h a t X is a useless w o r d u n l e s s t h e r e a r e s o m e t h i n g s t h a t a r e n o t X . I f e v e r y t h i n g i s a r o b o t , t h e n the w o r d r o b o t d o e s n ' t m e a n a n y t h i n g useful. B u t the w o r d r o b o t h a s o t h e r a s s o c i a t i o n s , a n d r i g i d i n f l e x i b i l i t y w a s n o t t h e a s s o c i a t i o n I w a s t h i n k i n g of. A r o b o t is a p r o g r a m m e d m a c h i n e , a n d an important thing a b o u t p r o g r a m m i n g is that it is distinct from, and done in
advance
of,
performance
of the
behaviour
itself.
A
computer
is
6
Genetic D e t e r m i n i s m and Gene Selectionism
p r o g r a m m e d to p e r f o r m the b e h a v i o u r of c a l c u l a t i n g s q u a r e roots, or p l a y i n g c h e s s . T h e r e l a t i o n s h i p b e t w e e n a c h e s s - p l a y i n g c o m p u t e r a n d the person w h o p r o g r a m m e d it is not obvious, and is open to misunderstanding. It m i g h t be t h o u g h t that the p r o g r a m m e r w a t c h e s the progress of the g a m e and gives instructions to the c o m p u t e r m o v e by m o v e .
I n fact, h o w e v e r , the
p r o g r a m m i n g i s finished b e f o r e t h e g a m e b e g i n s . T h e p r o g r a m m e r tries t o anticipate
contingencies,
and
builds
in
conditional
instructions
of great
c o m p l e x i t y , b u t o n c e t h e g a m e b e g i n s h e h a s t o k e e p his h a n d s off. H e i s n o t a l l o w e d t o g i v e the c o m p u t e r a n y n e w hints d u r i n g the course o f the g a m e . I f h e d i d h e w o u l d n o t b e p r o g r a m m i n g b u t p e r f o r m i n g , a n d his e n t r y w o u l d be disqualified from the t o u r n a m e n t . In the w o r k criticized by S y m o n s , I m a d e e x t e n s i v e use o f t h e a n a l o g y o f c o m p u t e r chess i n o r d e r t o e x p l a i n the p o i n t t h a t g e n e s d o n o t c o n t r o l b e h a v i o u r d i r e c t l y i n t h e sense o f i n t e r f e r i n g i n its p e r f o r m a n c e . T h e y o n l y c o n t r o l b e h a v i o u r i n t h e sense o f p r o g r a m m i n g t h e m a c h i n e i n advance o f p e r f o r m a n c e . I t w a s this a s s o c i a t i o n w i t h the w o r d robot that I w a n t e d to i n v o k e , not the association w i t h mindless inflexibility. A s for t h e m i n d l e s s i n f l e x i b i l i t y a s s o c i a t i o n itself,
it could
have been
justified in the d a y s w h e n the a c m e of a u t o m a t i o n w a s the rod and c a m control system of a marine engine, and K i p l i n g wrote ' M c A n d r e w ' s H y m n ' :
F r o m c o u p l e r - f l a n g e t o s p i n d l e - g u i d e I see T h y H a n d , O G o d Predestination in the stride o' y o n c o n n e c t i n ' - r o d . J o h n C a l v i n m i g h t h a ' forged the s a m e —
But that w a s 1893 a n d the h e y d a y o f steam. W e are n o w w e l l e m b a r k e d o n t h e g o l d e n a g e o f e l e c t r o n i c s . I f m a c h i n e s e v e r h a d a s s o c i a t i o n s w i t h rigid inflexibility— and I a c c e p t that they h a d — i t is high time they lived them down.
Computer
International
programs
have
Master standard
now
(Levy
been
written
that
play
chess
to
1978), that converse and reason in
correct and indefinitely c o m p l e x grammatical
English
(Winograd
1972),
that c r e a t e e l e g a n t a n d aesthetically satisfying n e w proofs o f m a t h e m a t i c a l theorems (Hofstadter 1 9 7 9 ) , that c o m p o s e music and diagnose illness; and t h e p a c e o f p r o g r e s s i n t h e f i e l d s h o w s n o sign o f s l o w i n g d o w n ( E v a n s 1 9 7 9 ) . T h e a d v a n c e d p r o g r a m m i n g field k n o w n as artificial intelligence is in a b u o y a n t , confident state ( B o d e n 1 9 7 7 ) . F e w w h o h a v e studied i t w o u l d n o w b e t a g a i n s t c o m p u t e r p r o g r a m s b e a t i n g t h e s t r o n g e s t G r a n d M a s t e r s a t chess w i t h i n the n e x t 10 years. F r o m b e i n g s y n o n y m o u s in the p o p u l a r mind with a
moronically
undeviating, jerky-limbed
zombie,
'robot'
will
one
day
b e c o m e a b y w o r d for f l e x i b i l i t y a n d r a p i d i n t e l l i g e n c e . U n f o r t u n a t e l y I j u m p e d t h e g u n a little i n t h e p a s s a g e q u o t e d . W h e n I wrote
it
I
had just
returned
from
an
eye-opening
and
mind-boggling
c o n f e r e n c e on the state of the art of artificial intelligence p r o g r a m m i n g , and
Genetic D e t e r m i n i s m and Gene Selectionism
I
genuinely
and
innocently
in
my
enthusiasm
forgot
that
17
robots
are
p o p u l a r l y s u p p o s e d t o b e i n f l e x i b l e i d i o t s . I a l s o h a v e t o a p o l o g i z e for t h e fact t h a t , w i t h o u t m y k n o w l e d g e , t h e c o v e r o f t h e G e r m a n e d i t i o n o f The Selfish Gene w a s g i v e n a p i c t u r e o f a h u m a n p u p p e t j e r k i n g o n t h e e n d o f strings d e s c e n d i n g f r o m t h e w o r d g e n e , a n d t h e F r e n c h e d i t i o n a p i c t u r e o f little b o w l e r - h a t t e d m e n w i t h c l o c k w o r k w i n d - u p k e y s s t i c k i n g o u t o f t h e i r b a c k s . I h a v e h a d slides o f b o t h c o v e r s m a d e u p a s i l l u s t r a t i o n s o f w h a t I w a s not t r y i n g to s a y . S o , the a n s w e r to S y m o n s is that of course he w a s right to criticize w h a t he thought I was saying, but of course I wasn't actually s a y i n g it ( R i d l e y 1 9 8 0 a ) . N o d o u b t I w a s p a r t l y t o b l a m e for t h e o r i g i n a l m i s u n d e r s t a n d i n g , but I c a n o n l y u r g e n o w that we put aside the p r e c o n c e p t i o n s d e r i v e d from common
usage
('...most
men
don't
understand
computers
to
even
the
slightest d e g r e e ' — W e i z e n b a u m 1 9 7 6 , p . 9 ) , a n d a c t u a l l y g o a n d r e a d s o m e of the fascinating m o d e r n literature on robotics a n d c o m p u t e r intelligence (e.g. B o d e n 1 9 7 7 ; E v a n s 1 9 7 9 ; Hofstadter 1 9 7 9 ) . O n c e again, of course, philosophers m a y debate the ultimate d e t e r m i n a c y of computers p r o g r a m m e d to b e h a v e in artificially intelligent w a y s , but if we are g o i n g t o g e t i n t o t h a t l e v e l o f p h i l o s o p h y m a n y w o u l d a p p l y t h e s a m e arguments to h u m a n intelligence ( T u r i n g 1950). W h a t is a brain, they w o u l d ask, b u t a c o m p u t e r , a n d w h a t i s e d u c a t i o n b u t a f o r m o f p r o g r a m m i n g ? I t i s very
hard
to
give
a non-supernatural
account
of the
human
brain
and
h u m a n e m o t i o n s , f e e l i n g s a n d a p p a r e n t free w i l l , without r e g a r d i n g t h e b r a i n as, i n s o m e sense, t h e e q u i v a l e n t o f a p r o g r a m m e d , c y b e r n e t i c m a c h i n e . T h e astronomer Sir F r e d H o y l e (1964) expresses v e r y v i v i d l y w h a t , it seems to me, any evolutionist must think a b o u t nervous systems:
L o o k i n g b a c k [at e v o l u t i o n ] I a m o v e r w h e l m i n g l y i m p r e s s e d b y t h e w a y in w h i c h chemistry has g r a d u a l l y g i v e n w a y to electronics. It is not unreasonable
to describe the first l i v i n g creatures as entirely
chemical
in
character.
important
in
plants,
Although
organized
electrochemical
electronics,
in
the
processes sense
are
of data
processing, does not enter or operate in the plant w o r l d . But primitive electronics begins to assume i m p o r t a n c e as soon as we h a v e a creature that m o v e s a r o u n d primitive
animals
. . . T h e first electronic systems possessed by were
essentially
guidance
systems,
analogous
l o g i c a l l y t o s o n a r o r r a d a r . A s w e pass t o m o r e d e v e l o p e d a n i m a l s w e f i n d e l e c t r o n i c s y s t e m s b e i n g u s e d n o t m e r e l y for g u i d a n c e b u t for directing the a n i m a l t o w a r d food . . . T h e situation is a n a l o g o u s to a g u i d e d missile, the j o b of w h i c h is to intercept a n d destroy a n o t h e r missile. Just as in o u r m o d e r n w o r l d attack and defense b e c o m e m o r e and m o r e subtle in their m e t h o d s , so it was the case w i t h a n i m a l s . A n d w i t h i n c r e a s i n g subtlety, better a n d
Genetic D e t e r m i n i s m and Gene Selectionism
18
better systems of electronics b e c o m e necessary. W h a t happened in n a t u r e has a close parallel w i t h the d e v e l o p m e n t of electronics in m o d e r n m i l i t a r y a p p l i c a t i o n s . . . I find it a s o b e r i n g t h o u g h t that but for t h e t o o t h - a n d - c l a w e x i s t e n c e o f t h e j u n g l e w e s h o u l d n o t possess o u r i n t e l l e c t u a l c a p a b i l i t i e s , w e s h o u l d n o t b e a b l e t o i n q u i r e into the structure of the U n i v e r s e , or be able to a p p r e c i a t e a s y m p h o n y of B e e t h o v e n . . . V i e w e d i n this l i g h t , t h e q u e s t i o n t h a t i s s o m e t i m e s a s k e d — c a n c o m p u t e r s think?—is s o m e w h a t ironic. H e r e of course I mean
the
computers
that
we
ourselves
make
out
of inorganic
m a t e r i a l s . W h a t o n e a r t h d o those w h o ask s u c h a q u e s t i o n t h i n k they t h e m s e l v e s a r e ? S i m p l y c o m p u t e r s , b u t v a s t l y m o r e c o m p l i c a t e d ones than anything we have yet learned to make.
R e m e m b e r that our
m a n - m a d e c o m p u t e r industry is a mere t w o or three decades old, whereas
we
ourselves
are
the
products
of an
evolution
t h a t has
operated over hundreds of millions of years [pp. 24-26].
O t h e r s m a y d i s a g r e e w i t h this c o n c l u s i o n , a l t h o u g h I s u s p e c t t h a t the o n l y alternatives to it are religious ones. W h a t e v e r the o u t c o m e of that debate, to r e t u r n t o g e n e s a n d t h e m a i n p o i n t o f this c h a p t e r , t h e issue o f d e t e r m i n i s m v e r s u s free w i l l i s j u s t n o t a f f e c t e d o n e w a y o r t h e o t h e r b y w h e t h e r o r not y o u h a p p e n t o b e c o n s i d e r i n g genes a s c a u s a l a g e n t s r a t h e r t h a n e n v i r o n mental
determinants.
But, it will p a r d o n a b l y be said, there is no smoke without fire. Functional e t h o l o g i s t s a n d ' s o c i o b i o l o g i s t s ' m u s t h a v e said s o m e t h i n g t o d e s e r v e b e i n g tarred w i t h the brush of g e n e t i c d e t e r m i n i s m . Or if it is all a misunderstandi n g there must b e s o m e g o o d e x p l a n a t i o n , b e c a u s e m i s u n d e r s t a n d i n g s that a r e s o w i d e s p r e a d d o n o t c o m e a b o u t for n o r e a s o n , e v e n i f a b e t t e d b y c u l t u r a l m y t h s as p o w e r f u l as the g e n e m y t h and the c o m p u t e r m y t h in u n h o l y a l l i a n c e . S p e a k i n g for m y s e l f , I t h i n k I k n o w t h e r e a s o n . It is an interesting one,
and
it
will
occupy
the
rest
o f this c h a p t e r .
The
mis-
u n d e r s t a n d i n g arises f r o m t h e w a y w e t a l k a b o u t a q u i t e different s u b j e c t , n a m e l y natural selection. G e n e selectionism, w h i c h is a w a y of talking about e v o l u t i o n , i s m i s t a k e n for g e n e t i c d e t e r m i n i s m , w h i c h i s a p o i n t o f v i e w a b o u t d e v e l o p m e n t . P e o p l e l i k e m e a r e c o n t i n u a l l y p o s t u l a t i n g g e n e s ' f o r ' this a n d g e n e s for t h a t . W e g i v e t h e i m p r e s s i o n o f b e i n g o b s e s s e d w i t h g e n e s a n d w i t h 'genetically programmed'
behaviour.
T a k e this i n
conjunction
with
the
p o p u l a r m y t h s o f the C a l v i n i s t i c d e t e r m i n a c y o f genes, a n d o f ' p r o g r a m m e d ' b e h a v i o u r as the h a l l m a r k of j a c t i t a t i n g D i s n e y l a n d puppets, and is it any w o n d e r that we are accused of being genetic determinists? W h y , then, do functional ethologists talk about genes so m u c h ? Because w e a r e i n t e r e s t e d i n n a t u r a l s e l e c t i o n , a n d n a t u r a l s e l e c t i o n i s differential s u r v i v a l o f g e n e s . I f w e a r e t o s o m u c h a s d i s c u s s t h e possibility o f a b e h a v i o u r pattern's
evolving
by
natural
selection,
we
have
to
postulate
genetic
Genetic D e t e r m i n i s m and Gene Selectionism
19
variation with respect to the t e n d e n c y or c a p a c i t y to p e r f o r m that b e h a v i o u r p a t t e r n . T h i s i s n o t t o s a y t h a t t h e r e n e c e s s a r i l y i s s u c h g e n e t i c v a r i a t i o n for any particular b e h a v i o u r pattern, only that there must h a v e been genetic variation in the past if we are to treat the b e h a v i o u r p a t t e r n as a D a r w i n i a n adaptation.
Of course
the
behaviour
pattern
may
not
be
a
Darwinian
adaptation, in w h i c h case the a r g u m e n t will not a p p l y . Incidentally,
I
should
defend
my usage of ' D a r w i n i a n
adaptation'
as
s y n o n y m o u s w i t h ' a d a p t a t i o n p r o d u c e d b y n a t u r a l s e l e c t i o n ' , for G o u l d a n d L e w o n t i n (1979) h a v e recently emphasized, with a p p r o v a l , the 'pluralistic' character of D a r w i n ' s o w n thought. It is indeed true that, especially towards the e n d o f his life, D a r w i n w a s d r i v e n b y c r i t i c i s m s , w h i c h w e c a n n o w see t o be erroneous, to m a k e some concessions to 'pluralism': he did not regard natural selection as the o n l y i m p o r t a n t d r i v i n g force in e v o l u t i o n . As the historian R .
M. Y o u n g (1971)
h a s s a r d o n i c a l l y p u t it,
' . . . b y the sixth
e d i t i o n the b o o k w a s m i s t i t l e d a n d s h o u l d h a v e r e a d On the Origin of Species by Means
of Natural
arguably
Selection
incorrect
to
and use
All
Sorts
'Darwinian
of Other
Things'.
evolution'
as
It
is,
therefore,
synonymous
with
' e v o l u t i o n b y n a t u r a l s e l e c t i o n ' . B u t D a r w i n i a n adaptation i s a n o t h e r m a t t e r . A d a p t a t i o n c a n n o t b e p r o d u c e d b y r a n d o m drift, o r b y a n y o t h e r r e a l i s t i c evolutionary force that we k n o w of save natural selection. It is true that D a r w i n ' s p l u r a l i s m d i d f l e e t i n g l y a l l o w for o n e o t h e r d r i v i n g f o r c e t h a t might, in principle, lead to a d a p t a t i o n , but that d r i v i n g force is i n s e p a r a b l y linked with the n a m e o f L a m a r c k , not o f D a r w i n . ' D a r w i n i a n a d a p t a t i o n ' could
not
sensibly
mean
anything
other
than
adaptation
produced
by
n a t u r a l s e l e c t i o n , a n d I s h a l l use i t i n this sense. I n s e v e r a l o t h e r p l a c e s i n this b o o k ( e . g . i n C h a p t e r s 3 a n d 6 ) , w e s h a l l r e s o l v e a p p a r e n t d i s p u t e s b y drawing a distinction b e t w e e n evolution in general, and a d a p t i v e evolution in
particular.
regarded
The
fixation
as evolution,
of neutral
mutations,
for
instance,
but it is not a d a p t i v e e v o l u t i o n .
can
be
If a m o l e c u l a r
geneticist interested in g e n e substitutions, or a p a l a e o n t o l o g i s t interested in major trends, argues w i t h an ecologist interested in a d a p t a t i o n ,
they are
likely to find themselves at cross-purposes s i m p l y b e c a u s e e a c h of t h e m e m p h a s i z e s a different a s p e c t o f w h a t e v o l u t i o n m e a n s . 'Genes
for
conformity,
xenophobia,
and
aggressiveness
are
simply
p o s t u l a t e d for h u m a n s b e c a u s e t h e y a r e n e e d e d for t h e t h e o r y , n o t b e c a u s e a n y e v i d e n c e for t h e m e x i s t s ' ( L e w o n t i n 1 9 7 9 ) . T h i s i s a fair c r i t i c i s m o f E. O. Wilson, but not a v e r y d a m n i n g one. A p a r t from possible political repercussions w h i c h cautiously
might
speculating
be
about
unfortunate, a
possible
there is Darwinian
nothing wrong with survival
value
of
x e n o p h o b i a o r a n y other trait. A n d y o u c a n n o t b e g i n t o s p e c u l a t e , h o w e v e r cautiously,
about
the s u r v i v a l v a l u e of a n y t h i n g unless y o u
postulate a
g e n e t i c basis for v a r i a t i o n i n t h a t t h i n g . O f c o u r s e x e n o p h o b i a m a y n o t v a r y genetically, and of course x e n o p h o b i a m a y not be a D a r w i n i a n adaptation,
20
G e n e t i c D e t e r m i n i s m and G e n e S e l e c t i o n i s m
b u t w e c a n ' t e v e n d i s c u s s t h e p o s s i b i l i t y o f its b e i n g a D a r w i n i a n a d a p t a t i o n u n l e s s w e p o s t u l a t e a g e n e t i c b a s i s for it. L e w o n t i n h i m s e l f h a s e x p r e s s e d the p o i n t a s w e l l a s a n y b o d y : ' I n o r d e r for a trait t o e v o l v e b y n a t u r a l s e l e c t i o n i t i s n e c e s s a r y t h a t t h e r e b e g e n e t i c v a r i a t i o n i n the p o p u l a t i o n for s u c h a trait' ( L e w o n t i n 1 9 7 9 ) . A n d ' g e n e t i c v a r i a t i o n i n t h e p o p u l a t i o n for' a trait X i s e x a c t l y w h a t w e m e a n w h e n w e t a l k , for b r e v i t y , o f ' a g e n e for' X . X e n o p h o b i a is controversial, so consider a b e h a v i o u r pattern that n o b o d y w o u l d fear to r e g a r d as a D a r w i n i a n a d a p t a t i o n . P i t - d i g g i n g in antlions is o b v i o u s l y an a d a p t a t i o n to c a t c h prey. A n t l i o n s are insects, neuropteran l a r v a e w i t h t h e g e n e r a l a p p e a r a n c e a n d d e m e a n o u r o f m o n s t e r s from o u t e r s p a c e . T h e y a r e 'sit a n d w a i t ' p r e d a t o r s w h o d i g pits i n soft s a n d w h i c h t r a p ants a n d other small w a l k i n g insects. T h e pit is a nearly perfect c o n e , whose sides s l o p e s o s t e e p l y t h a t p r e y c a n n o t c l i m b o u t o n c e t h e y h a v e fallen in. T h e a n t l i o n sits j u s t u n d e r t h e s a n d a t the b o t t o m o f t h e pit, w h e r e i t l u n g e s w i t h its h o r r o r - f i l m j a w s a t a n y t h i n g t h a t falls in. P i t - d i g g i n g i s a c o m p l e x b e h a v i o u r p a t t e r n . I t costs t i m e a n d e n e r g y , a n d satisfies t h e m o s t e x a c t i n g c r i t e r i a for r e c o g n i t i o n a s a n a d a p t a t i o n ( W i l l i a m s 1966; C u r i o 1 9 7 3 ) . It must, then, h a v e evolved by natural selection. H o w m i g h t this h a v e h a p p e n e d ? T h e d e t a i l s d o n ' t m a t t e r for the m o r a l I w a n t t o d r a w . P r o b a b l y a n a n c e s t r a l a n t l i o n e x i s t e d w h i c h d i d not d i g a pit b u t s i m p l y l u r k e d j u s t b e n e a t h t h e s a n d s u r f a c e w a i t i n g for p r e y t o b l u n d e r o v e r it. I n d e e d s o m e s p e c i e s still d o this. L a t e r , b e h a v i o u r l e a d i n g t o t h e c r e a t i o n of a shallow depression in because
the
depression
the sand p r o b a b l y w a s favoured by selection
marginally
impeded
escaping
prey.
By
gradual
degrees o v e r m a n y generations the b e h a v i o u r c h a n g e d so that w h a t was a shallow
depression
became
deeper
and
wider.
This
not
only
hindered
e s c a p i n g p r e y but also increased the c a t c h m e n t area o v e r w h i c h prey might s t u m b l e i n t h e f i r s t p l a c e . L a t e r still t h e d i g g i n g b e h a v i o u r c h a n g e d a g a i n s o t h a t t h e r e s u l t i n g pit b e c a m e a s t e e p - s i d e d c o n e , l i n e d w i t h f i n e , s l i d i n g s a n d so that prey w e r e u n a b l e to c l i m b out. N o t h i n g in the previous p a r a g r a p h is contentious or controversial. It will be r e g a r d e d as l e g i t i m a t e s p e c u l a t i o n a b o u t historical events that we cannot see d i r e c t l y , a n d i t w i l l p r o b a b l y b e t h o u g h t p l a u s i b l e . O n e r e a s o n w h y i t will be a c c e p t e d as uncontroversial historical speculation is that it makes no mention
of genes.
But
my
point
is
that
none of that
history,
nor any
c o m p a r a b l e h i s t o r y , c o u l d p o s s i b l y h a v e b e e n t r u e unless t h e r e w a s g e n e t i c v a r i a t i o n in the b e h a v i o u r at e v e r y step of the e v o l u t i o n a r y w a y . P i t - d i g g i n g in antlions is o n l y o n e of the thousands of e x a m p l e s that I c o u l d h a v e chosen. U n l e s s n a t u r a l s e l e c t i o n h a s g e n e t i c v a r i a t i o n t o a c t u p o n , i t c a n n o t g i v e rise t o e v o l u t i o n a r y c h a n g e . I t f o l l o w s t h a t w h e r e y o u find D a r w i n i a n a d a p t a t i o n t h e r e m u s t h a v e b e e n g e n e t i c v a r i a t i o n i n the c h a r a c t e r c o n c e r n e d . N o b o d y has ever d o n e a genetic study of pit-digging b e h a v i o u r in antlions (J. L u c a s , p e r s o n a l c o m m u n i c a t i o n ) . T h e r e i s n o n e e d t o d o o n e , i f a l l w e
Genetic D e t e r m i n i s m and Gene Selectionism
21
w a n t t o d o i s satisfy o u r s e l v e s o f t h e s o m e t i m e e x i s t e n c e o f g e n e t i c v a r i a t i o n in the b e h a v i o u r p a t t e r n . It is sufficient t h a t we a r e c o n v i n c e d t h a t it is a D a r w i n i a n a d a p t a t i o n (if y o u a r e n o t c o n v i n c e d t h a t p i t - d i g g i n g i s s u c h a n adaptation, simply substitute a n y e x a m p l e o f w h i c h y o u are c o n v i n c e d ) . I s p o k e o f t h e sometime e x i s t e n c e o f g e n e t i c v a r i a t i o n . T h i s w a s b e c a u s e i t i s quite likely that, w e r e a genetic study to be m o u n t e d of antlions today, no genetic variation w o u l d be found. It is in general to be e x p e c t e d that, w h e r e t h e r e i s s t r o n g s e l e c t i o n i n f a v o u r o f s o m e trait, t h e o r i g i n a l v a r i a t i o n o n w h i c h selection a c t e d to g u i d e the e v o l u t i o n of the trait w i l l h a v e b e c o m e u s e d u p . T h i s i s t h e f a m i l i a r ' p a r a d o x ' (it i s n o t r e a l l y v e r y p a r a d o x i c a l w h e n w e t h i n k a b o u t i t c a r e f u l l y ) t h a t traits u n d e r s t r o n g s e l e c t i o n t e n d t o h a v e low heritability (Falconer 1960); ' . . .evolution by natural selection destroys the
genetic
variance
hypotheses
frequently
which
all
are
but
on
which
it
feeds'
concern phenotypic universal
in
the
(Lewontin traits,
1979).
Functional
like possession of eyes,
population,
and
therefore
without
contemporary genetic variation. W h e n we speculate about, or m a k e models of, the e v o l u t i o n a r y p r o d u c t i o n o f a n a d a p t a t i o n , w e a r e n e c e s s a r i l y t a l k i n g about a time w h e n there was appropriate genetic variation. We are b o u n d , in such discussions, to postulate, implicitly or explicitly, genes 'for' p r o p o s e d adaptations. Some m a y balk at treating 'a genetic contribution to variation in X' as e q u i v a l e n t t o ' a g e n e o r g e n e s for X ' . B u t this i s a r o u t i n e g e n e t i c p r a c t i c e , and one w h i c h close e x a m i n a t i o n shows to be almost i n e v i t a b l e . O t h e r than a t the m o l e c u l a r l e v e l , w h e r e o n e g e n e i s s e e n d i r e c t l y t o p r o d u c e o n e p r o t e i n chain, geneticists never deal w i t h units of p h e n o t y p e as such. R a t h e r , they a l w a y s d e a l w i t h differences. W h e n a g e n e t i c i s t s p e a k s o f a g e n e ' f o r ' r e d e y e s in
Drosophila,
h e i s n o t s p e a k i n g o f t h e c i s t r o n w h i c h a c t s a s t e m p l a t e for t h e
synthesis o f t h e r e d p i g m e n t m o l e c u l e .
He is implicitly s a y i n g :
there is
variation in e y e c o l o u r in the p o p u l a t i o n ; other things b e i n g e q u a l , a fly w i t h this g e n e i s m o r e l i k e l y t o h a v e r e d e y e s t h a n a f l y w i t h o u t t h e g e n e . T h a t i s all that we e v e r m e a n by a g e n e 'for' red eyes. T h i s h a p p e n s to be a morphological rather than a behavioural example,
but exactly the same
a p p l i e s to b e h a v i o u r . A g e n e ' f o r ' b e h a v i o u r X is a g e n e ' f o r ' w h a t e v e r m o r p h o l o g i c a l a n d p h y s i o l o g i c a l states t e n d t o p r o d u c e t h a t b e h a v i o u r . A r e l a t e d p o i n t is t h a t t h e use of s i n g l e - l o c u s m o d e l s is j u s t a c o n c e p t u a l c o n v e n i e n c e , a n d this i s t r u e o f a d a p t i v e h y p o t h e s e s i n e x a c t l y t h e s a m e w a y a s i t i s t r u e o f o r d i n a r y p o p u l a t i o n g e n e t i c m o d e l s . W h e n w e use s i n g l e - g e n e l a n g u a g e in our adaptive hypotheses, we do not intend to m a k e a point about single-gene models as against multi-gene models.
We are usually
m a k i n g a p o i n t a b o u t gene m o d e l s a s a g a i n s t n o n - g e n e m o d e l s , for e x a m p l e a s against ' g o o d of the species' m o d e l s . S i n c e it is difficult e n o u g h c o n v i n c i n g p e o p l e t h a t t h e y o u g h t to t h i n k in g e n e t i c t e r m s at all r a t h e r t h a n in t e r m s of, s a y , the g o o d o f t h e s p e c i e s , t h e r e i s n o sense i n m a k i n g t h i n g s e v e n m o r e
22
G e n e t i c D e t e r m i n i s m and G e n e S e l e c t i o n i s m
difficult b y t r y i n g t o h a n d l e t h e c o m p l e x i t i e s o f m a n y l o c i a t t h e o u t s e t . W h a t L l o y d ( 1 9 7 9 ) c a l l s t h e O G A M ( o n e g e n e a n a l y s i s m o d e l ) is, o f c o u r s e , not t h e last w o r d i n g e n e t i c a c c u r a c y . O f course w e s h a l l e v e n t u a l l y h a v e t o face u p t o multi-locus c o m p l e x i t y . But the O G A M i s vastly preferable t o modes o f a d a p t i v e r e a s o n i n g t h a t f o r g e t a b o u t g e n e s a l t o g e t h e r , a n d this i s the o n l y point I am trying to m a k e at present. S i m i l a r l y we m a y find ourselves aggressively challenged to substantiate o u r ' c l a i m s ' o f t h e e x i s t e n c e o f ' g e n e s for' s o m e a d a p t a t i o n i n w h i c h w e are i n t e r e s t e d . B u t this c h a l l e n g e , if it is a r e a l c h a l l e n g e at a l l , s h o u l d be d i r e c t e d a t t h e w h o l e o f t h e n e o - D a r w i n i a n ' m o d e r n s y n t h e s i s ' a n d the w h o l e of population genetics. To phrase a functional hypothesis in terms of genes is to m a k e no strong claims about genes at all: it is simply to m a k e explicit an a s s u m p t i o n w h i c h is i n s e p a r a b l y built into the m o d e r n synthesis, albeit it is sometimes implicit rather than explicit. A few w o r k e r s h a v e , indeed, flung just such a c h a l l e n g e at the w h o l e neoD a r w i n i a n m o d e r n synthesis, a n d h a v e c l a i m e d not to be n e o - D a r w i n i a n s . Goodwin
(1979)
in a published debate with D e b o r a h Charlesworth and
o t h e r s , s a i d , '. . . n e o - D a r w i n i s m h a s an i n c o h e r e n c e in it . . . we are not g i v e n a n y w a y o f g e n e r a t i n g p h e n o t y p e s from g e n o t y p e s i n n e o - D a r w i n i s m . T h e r e f o r e t h e t h e o r y i s i n this r e s p e c t d e f e c t i v e . ' G o o d w i n is, o f c o u r s e , q u i t e right that d e v e l o p m e n t is terribly complicated, and we don't yet understand m u c h a b o u t h o w p h e n o t y p e s a r e g e n e r a t e d . B u t that t h e y a r e g e n e r a t e d , a n d that g e n e s
contribute
facts, a n d
t h o s e facts a r e a l l w e n e e d i n o r d e r t o m a k e n e o - D a r w i n i s m
significantly
to
their variation
are
incontrovertible
c o h e r e n t . G o o d w i n m i g h t just a s w e l l s a y t h a t , b e f o r e H o d g k i n a n d H u x l e y w o r k e d out h o w the n e r v e impulse fired, we w e r e not entitled to believe t h a t n e r v e i m p u l s e s c o n t r o l l e d b e h a v i o u r . O f course i t w o u l d b e n i c e t o k n o w h o w p h e n o t y p e s a r e m a d e b u t , w h i l e e m b r y o l o g i s t s a r e b u s y f i n d i n g o u t , the rest o f u s a r e e n t i t l e d b y t h e k n o w n facts o f g e n e t i c s t o c a r r y o n b e i n g n e o D a r w i n i a n s , treating e m b r y o n i c d e v e l o p m e n t as a black box. T h e r e is no c o m p e t i n g theory that has even a remote claim to be called coherent. It
follows
from
the
fact
that
geneticists
are
always
concerned
with
p h e n o t y p i c differences t h a t w e n e e d n o t b e a f r a i d o f p o s t u l a t i n g g e n e s w i t h i n d e f i n i t e l y c o m p l e x p h e n o t y p i c effects, a n d w i t h p h e n o t y p i c effects t h a t show themselves only in highly complex developmental conditions. Together w i t h Professor J o h n M a y n a r d S m i t h , I recently took part in a public debate w i t h t w o radical critics of 'sociobiology', before an a u d i e n c e of students. At one time in the discussion we w e r e trying to establish that to talk of a gene 'for X ' i s t o m a k e n o o u t l a n d i s h c l a i m , e v e n w h e r e X i s a c o m p l e x , l e a r n e d b e h a v i o u r p a t t e r n . M a y n a r d S m i t h r e a c h e d for a h y p o t h e t i c a l e x a m p l e a n d c a m e u p w i t h a ' g e n e for skill i n t y i n g s h o e l a c e s ' . P a n d e m o n i u m b r o k e loose at
this
rampant
genetic
determinism!
The
air was
thick
with
the
un-
mistakable sound of worst suspicions being gleefully confirmed. Delightedly
G e n e t i c D e t e r m i n i s m and G e n e S e l e c t i o n i s m
23
s c e p t i c a l cries d r o w n e d t h e q u i e t a n d p a t i e n t e x p l a n a t i o n o f j u s t w h a t a modest c l a i m i s b e i n g m a d e w h e n e v e r o n e p o s t u l a t e s a g e n e for, s a y , skill in tying shoelaces.
Let me
explain
the point w i t h
the
aid
of an
more radical-sounding yet truly innocuous thought experiment
even
(Dawkins
1981). R e a d i n g i s a l e a r n e d skill o f p r o d i g i o u s c o m p l e x i t y , b u t this p r o v i d e s n o r e a s o n i n itself for s c e p t i c i s m a b o u t t h e p o s s i b l e e x i s t e n c e o f a g e n e for r e a d i n g . A l l w e w o u l d n e e d i n o r d e r t o e s t a b l i s h t h e e x i s t e n c e o f a g e n e for r e a d i n g is to d i s c o v e r a g e n e for n o t r e a d i n g , s a y a g e n e w h i c h i n d u c e d a brain lesion c a u s i n g specific d y s l e x i a .
S u c h a dyslexic person
might be
n o r m a l a n d intelligent i n all respects e x c e p t that h e c o u l d not r e a d . N o g e n e t i c i s t w o u l d b e p a r t i c u l a r l y s u r p r i s e d i f this t y p e o f d y s l e x i a t u r n e d o u t t o b r e e d t r u e i n s o m e M e n d e l i a n f a s h i o n . O b v i o u s l y , i n this e v e n t , t h e g e n e w o u l d o n l y e x h i b i t its effect i n a n e n v i r o n m e n t w h i c h i n c l u d e d n o r m a l education.
In a prehistoric environment it m i g h t h a v e h a d no detectable
effect, o r i t m i g h t h a v e h a d s o m e different effect a n d h a v e b e e n k n o w n t o cave-dwelling
geneticists
as,
say,
a
gene
for
inability
to
read
animal
footprints. In our e d u c a t e d e n v i r o n m e n t it w o u l d p r o p e r l y be c a l l e d a g e n e 'for' d y s l e x i a , s i n c e d y s l e x i a w o u l d b e its m o s t s a l i e n t c o n s e q u e n c e . S i m i l a r l y , a gene w h i c h caused total blindness w o u l d also p r e v e n t r e a d i n g , b u t it w o u l d n o t usefully b e r e g a r d e d a s a g e n e for n o t r e a d i n g . T h i s i s s i m p l y b e c a u s e p r e v e n t i n g r e a d i n g w o u l d n o t b e its m o s t o b v i o u s o r d e b i l i t a t i n g p h e n o t y p i c effect. R e t u r n i n g t o o u r g e n e for s p e c i f i c d y s l e x i a , i t f o l l o w s f r o m t h e o r d i n a r y conventions of genetic t e r m i n o l o g y that the w i l d - t y p e g e n e at the s a m e locus, the g e n e t h a t t h e rest o f t h e p o p u l a t i o n h a s i n d o u b l e d o s e , w o u l d p r o p e r l y b e c a l l e d a g e n e 'for r e a d i n g ' . I f y o u o b j e c t t o t h a t , y o u m u s t a l s o o b j e c t t o o u r s p e a k i n g o f a g e n e for t a l l n e s s i n M e n d e l ' s p e a s , b e c a u s e t h e l o g i c o f t h e t e r m i n o l o g y is identical in the t w o cases.
In b o t h cases the c h a r a c t e r of
interest is a difference, a n d in b o t h c a s e s t h e d i f f e r e n c e o n l y s h o w s i t s e l f in some specified e n v i r o n m e n t . T h e reason w h y s o m e t h i n g so simple as a o n e g e n e d i f f e r e n c e c a n h a v e s u c h a c o m p l e x effect a s t o d e t e r m i n e w h e t h e r o r not a person c a n learn to read, or h o w g o o d he is at t y i n g shoelaces, is basically as follows. H o w e v e r c o m p l e x a g i v e n state of the w o r l d m a y be, the difference b e t w e e n t h a t s t a t e o f t h e w o r l d a n d s o m e a l t e r n a t i v e s t a t e o f t h e world may be caused by something extremely simple. T h e point I m a d e using antlions is a g e n e r a l one. I c o u l d h a v e used a n y real o r p u r p o r t e d D a r w i n i a n a d a p t a t i o n w h a t s o e v e r . F o r f u r t h e r e m p h a s i s I shall
use
one
more
example.
Tinbergen
et
al.
(1962)
investigated
the
adaptive significance of a particular behaviour pattern in b l a c k - h e a d e d gulls (Larus
ridibundus),
eggshell
removal.
Shortly
after
a
chick
hatches,
the
parent bird grasps the e m p t y eggshell in the bill a n d r e m o v e s it from the v i c i n i t y o f t h e nest. T i n b e r g e n a n d his c o l l e a g u e s c o n s i d e r e d a n u m b e r o f
24
Genetic D e t e r m i n i s m and Gene Selectionism
p o s s i b l e h y p o t h e s e s a b o u t t h e s u r v i v a l v a l u e o f this b e h a v i o u r p a t t e r n . F o r instance t h e y suggested that the e m p t y eggshells m i g h t serve as breeding g r o u n d s for h a r m f u l b a c t e r i a , o r t h e s h a r p e d g e s m i g h t c u t t h e c h i c k s . B u t t h e h y p o t h e s i s for w h i c h t h e y e n d e d u p f i n d i n g e v i d e n c e w a s t h a t t h e e m p t y eggshell serves as a c o n s p i c u o u s visual b e a c o n s u m m o n i n g crows and other p r e d a t o r s o f c h i c k s o r e g g s t o t h e nest. T h e y d i d i n g e n i o u s e x p e r i m e n t s , l a y i n g o u t a r t i f i c i a l nests w i t h a n d w i t h o u t e m p t y e g g s h e l l s , a n d s h o w e d t h a t eggs a c c o m p a n i e d
by e m p t y eggshells were,
indeed,
m o r e likely to be
a t t a c k e d b y c r o w s t h a n eggs w i t h o u t e m p t y eggshells b y their side. T h e y c o n c l u d e d that natural selection had favoured eggshell r e m o v a l behaviour of adult gulls, b e c a u s e past adults w h o did not do it reared fewer children. As in the case of antlion d i g g i n g , n o b o d y has ever d o n e a genetic study of eggshell
removal
behaviour
in
black-headed
gulls.
There
is
no
direct
e v i d e n c e t h a t v a r i a t i o n i n t e n d e n c y t o r e m o v e e m p t y eggshells breeds true. Y e t c l e a r l y t h e a s s u m p t i o n t h a t i t d o e s , o r o n c e d i d , i s e s s e n t i a l for the T i n b e r g e n hypothesis. T h e T i n b e r g e n hypothesis, as normally phrased in g e n e - f r e e l a n g u a g e , i s n o t p a r t i c u l a r l y c o n t r o v e r s i a l . Y e t it, l i k e a l l t h e r i v a l f u n c t i o n a l h y p o t h e s e s t h a t T i n b e r g e n r e j e c t e d , rests f u n d a m e n t a l l y u p o n the assumption that o n c e u p o n a time there must h a v e been gulls with a genetic t e n d e n c y t o r e m o v e e g g s h e l l s , a n d o t h e r g u l l s w i t h a g e n e t i c t e n d e n c y not t o r e m o v e t h e m , o r t o b e less l i k e l y t o r e m o v e t h e m . T h e r e m u s t h a v e b e e n g e n e s for r e m o v i n g e g g s h e l l s . H e r e I m u s t e n t e r a n o t e o f c a u t i o n . S u p p o s e w e a c t u a l l y d i d a s t u d y o f the genetics of eggshell r e m o v a l b e h a v i o u r in modern gulls.
It w o u l d be a
behaviour-geneticist's d r e a m to find a simple M e n d e l i a n mutation which radically altered
the b e h a v i o u r pattern, p e r h a p s abolished the b e h a v i o u r
a l t o g e t h e r . B y t h e a r g u m e n t g i v e n a b o v e , this m u t a n t w o u l d t r u l y b e a g e n e ' f o r ' n o t r e m o v i n g e g g s h e l l s , a n d , b y d e f i n i t i o n , its w i l d - t y p e a l l e l e w o u l d h a v e t o b e c a l l e d a g e n e for e g g s h e l l r e m o v a l . B u t n o w c o m e s t h e n o t e o f caution.
I t m o s t d e f i n i t e l y d o e s n o t f o l l o w t h a t this p a r t i c u l a r l o c u s 'for'
eggshell r e m o v a l w a s one of the ones u p o n w h i c h natural selection worked d u r i n g the e v o l u t i o n o f the a d a p t a t i o n . O n the c o n t r a r y , i t seems m u c h more p r o b a b l e that a c o m p l e x b e h a v i o u r pattern like eggshell r e m o v a l must h a v e been built up by selection on a large n u m b e r of loci, e a c h h a v i n g a small effect i n i n t e r a c t i o n w i t h t h e o t h e r s . O n c e t h e b e h a v i o u r c o m p l e x h a d b e e n b u i l t u p , i t i s e a s y t o i m a g i n e a s i n g l e m a j o r m u t a t i o n a r i s i n g , w h o s e effect i s t o d e s t r o y it. G e n e t i c i s t s p e r f o r c e m u s t e x p l o i t t h e g e n e t i c v a r i a t i o n a v a i l a b l e for t h e m t o s t u d y . T h e y a l s o b e l i e v e t h a t n a t u r a l s e l e c t i o n m u s t h a v e w o r k e d on similar genetic variation in w r e a k i n g evolutionary c h a n g e . But there is no r e a s o n for t h e m t o b e l i e v e t h a t t h e l o c i c o n t r o l l i n g m o d e r n v a r i a t i o n i n a n a d a p t a t i o n w e r e the v e r y s a m e loci at w h i c h selection acted in b u i l d i n g up the a d a p t a t i o n in the first p l a c e . C o n s i d e r the most famous e x a m p l e of single gene control of c o m p l e x
Genetic D e t e r m i n i s m and Gene Selectionism
25
behaviour, the case of R o t h e n b u h l e r ' s (1964) h y g i e n i c bees. T h e point of u s i n g this e x a m p l e i s t h a t i t i l l u s t r a t e s w e l l h o w a h i g h l y c o m p l e x b e h a v i o u r difference c a n be d u e to a single g e n e difference. T h e h y g i e n i c b e h a v i o u r of the B r o w n strain o f h o n e y b e e s involves the w h o l e n e u r o m u s c u l a r system, but the fact t h a t t h e y p e r f o r m t h e b e h a v i o u r w h e r e a s V a n S c o y b e e s d o n o t is, a c c o r d i n g to R o t h e n b u h l e r ' s m o d e l , d u e to differences at t w o loci o n l y . O n e locus determines the u n c a p p i n g of cells c o n t a i n i n g diseased b r o o d , the o t h e r l o c u s d e t e r m i n e s t h e r e m o v i n g o f d i s e a s e d b r o o d after u n c a p p i n g . I t w o u l d be possible, therefore, to i m a g i n e a natural selection in f a v o u r of u n c a p p i n g behaviour and a natural selection in favour of r e m o v i n g behaviour, m e a n i n g selection of the t w o genes versus their respective alleles. B u t the p o i n t I am m a k i n g here is that, although that could h a p p e n , it is not likely to be very interesting evolutionarily.
The
modern uncapping gene
and
the modern
r e m o v i n g gene m a y very well not h a v e been i n v o l v e d in the original natural selection
process
that
steered
the
evolutionary
putting
together
of the
behaviour. Rothenbuhler observed
that
even
Van
Scoy
bees
sometimes
perform
h y g i e n i c b e h a v i o u r . T h e y a r e j u s t q u a n t i t a t i v e l y m u c h less l i k e l y t o d o s o than are B r o w n bees. It is likely, therefore, that b o t h B r o w n and V a n S c o y bees h a v e h y g i e n i c a n c e s t o r s , a n d b o t h h a v e i n t h e i r n e r v o u s s y s t e m s t h e machinery of u n c a p p i n g and removing b e h a v i o u r : it is just that V a n S c o y bees
have
genes
that
prevent
them
from
turning
the
machinery
on.
P r e s u m a b l y i f w e w e n t b a c k e v e n f u r t h e r i n t i m e w e s h o u l d find a n a n c e s t o r of all m o d e r n bees w h i c h not o n l y w a s not h y g i e n i c itself b u t h a d n e v e r h a d a hygienic
ancestor.
There
must
have
been
an
evolutionary
progression
b u i l d i n g u p t h e u n c a p p i n g a n d r e m o v i n g b e h a v i o u r f r o m n o t h i n g , a n d this evolutionary progression involved the selection of m a n y genes w h i c h are n o w fixed in
both
the
Brown
and
the
Van
Scoy
strains.
So,
although
the
u n c a p p i n g and the r e m o v i n g genes of the B r o w n strain really are rightly c a l l e d g e n e s for u n c a p p i n g a n d r e m o v i n g , t h e y a r e d e f i n e d a s s u c h o n l y b e c a u s e t h e y h a p p e n t o h a v e a l l e l e s w h o s e effect i s t o p r e v e n t t h e b e h a v i o u r from b e i n g p e r f o r m e d . T h e m o d e o f a c t i o n o f t h e s e a l l e l e s c o u l d b e b o r i n g l y destructive. T h e y m i g h t simply cut some vital link in the neural m a c h i n e r y . I am r e m i n d e d of G r e g o r y ' s ( 1 9 6 1 ) v i v i d illustration of the perils of m a k i n g inferences from a b l a t i o n e x p e r i m e n t s o n the b r a i n : ' . . . the r e m o v a l o f a n y o f s e v e r a l w i d e l y s p a c e d resistors m a y c a u s e a r a d i o set t o e m i t h o w l s , b u t i t d o e s n o t f o l l o w t h a t h o w l s a r e i m m e d i a t e l y a s s o c i a t e d w i t h t h e s e resistors, o r indeed that the causal relation is a n y t h i n g but the most indirect. In part i c u l a r , w e s h o u l d n o t s a y t h a t t h e f u n c t i o n o f t h e resistors i n t h e n o r m a l circuit is to inhibit h o w l i n g . Neurophysiologists, w h e n faced w i t h a c o m parable situation, have postulated "suppressor regions".' T h i s c o n s i d e r a t i o n s e e m s t o m e t o b e a r e a s o n for c a u t i o n , n o t a r e a s o n for rejecting the w h o l e genetic theory o f natural selection! N e v e r m i n d i f l i v i n g
Genetic D e t e r m i n i s m and Gene Selectionism
26
geneticists are d e b a r r e d from s t u d y i n g the p a r t i c u l a r loci at w h i c h selection i n t h e p a s t g a v e rise t o t h e o r i g i n a l e v o l u t i o n o f i n t e r e s t i n g a d a p t a t i o n s . I t i s t o o b a d i f g e n e t i c i s t s u s u a l l y a r e f o r c e d t o c o n c e n t r a t e o n loci t h a t a r e convenient rather than evolutionary
putting
evolutionarily important. together
of
complex
I t i s still t r u e t h a t the
and
interesting
adaptation
consisted in the r e p l a c e m e n t of genes by their alleles. This
argument
can
contribute
tangentially
to
the
resolution
of a
f a s h i o n a b l e c o n t e m p o r a r y d i s p u t e , b y h e l p i n g t o p u t t h e issue i n p e r s p e c t i v e . It
is
now
highly,
indeed
passionately,
controversial
whether
there
is
significant genetic variation in h u m a n mental abilities. A r e some of us g e n e t i c a l l y b r a i n i e r t h a n others? W h a t w e m e a n b y ' b r a i n y ' i s also highly c o n t e n t i o u s , a n d r i g h t l y so. B u t I suggest that, by a n y m e a n i n g of the term, the f o l l o w i n g propositions c a n n o t be d e n i e d , (1) T h e r e w a s a time w h e n our a n c e s t o r s w e r e less b r a i n y t h a n w e a r e .
(2) T h e r e f o r e t h e r e h a s b e e n a n
i n c r e a s e i n b r a i n i n e s s i n o u r a n c e s t r a l l i n e a g e . (3) T h a t i n c r e a s e c a m e a b o u t through evolution, p r o b a b l y propelled by natural selection.
(4)
Whether
p r o p e l l e d by selection or not, at least part of the e v o l u t i o n a r y c h a n g e in p h e n o t y p e r e f l e c t e d a n u n d e r l y i n g g e n e t i c c h a n g e : a l l e l e r e p l a c e m e n t took p l a c e a n d c o n s e q u e n t l y m e a n m e n t a l a b i l i t y i n c r e a s e d o v e r g e n e r a t i o n s . (5) By definition therefore, at least in the past, there must h a v e b e e n significant g e n e t i c v a r i a t i o n i n braininess w i t h i n the h u m a n p o p u l a t i o n . S o m e people w e r e g e n e t i c a l l y clever in c o m p a r i s o n w i t h their contemporaries, others were genetically relatively stupid. T h e last s e n t e n c e m a y e n g e n d e r a frisson o f i d e o l o g i c a l d i s q u i e t , y e t n o n e of my five propositions c o u l d be seriously d o u b t e d , nor could their logical s e q u e n c e . T h e a r g u m e n t w o r k s for b r a i n s i z e , b u t i t e q u a l l y w o r k s for a n y b e h a v i o u r a l measure of cleverness we care to d r e a m up. It does not depend on simplistic v i e w s of h u m a n intelligence as b e i n g a one-dimensional scalar quantity. T h e fact that intelligence is not a simple scalar quantity, important as
that
fact
intelligence
is, in
is
simply
practice.
inevitable,
provided
proposition
that
once
irrelevant.
The
only upon
that a
So
conclusion we time
are
is
the
difficulty
of measuring
of the
previous
paragraph
evolutionists
our ancestors
who
were
agree
less
is
to
the
clever
(by
w h a t e v e r c r i t e r i o n ) t h e n w e a r e . Y e t i n s p i t e o f a l l t h a t , i t still d o e s n o t f o l l o w t h a t t h e r e i s a n y g e n e t i c v a r i a t i o n i n m e n t a l a b i l i t i e s left i n t h e h u m a n p o p u l a t i o n t o d a y : the g e n e t i c v a r i a n c e m i g h t all h a v e b e e n used u p b y selection. O n the o t h e r h a n d i t m i g h t not, a n d m y t h o u g h t e x p e r i m e n t shows a t l e a s t t h e i n a d v i s a b i l i t y o f d o g m a t i c a n d h y s t e r i c a l o p p o s i t i o n t o the v e r y possibility o f genetic variation i n h u m a n mental abilities. M y o w n opinion, for w h a t i t i s w o r t h , i s t h a t e v e n i f t h e r e i s s u c h g e n e t i c v a r i a t i o n i n m o d e r n h u m a n populations, to base any policy on it w o u l d be illogical and wicked. T h e existence of a D a r w i n i a n adaptation,
then,
implies the sometime
e x i s t e n c e o f g e n e s for p r o d u c i n g t h e a d a p t a t i o n . T h i s i s n o t a l w a y s m a d e
Genetic D e t e r m i n i s m and G e n e S e l e c t i o n i s m
explicit.
It is a l w a y s
possible
to
talk a b o u t the natural
27
selection of a
behaviour pattern in t w o w a y s . We can either talk a b o u t individuals with a tendency to perform the b e h a v i o u r pattern b e i n g 'fitter' t h a n i n d i v i d u a l s with
a
less s t r o n g l y
developed
tendency.
This
is
the
now
fashionable
p h r a s e o l o g y , w i t h i n t h e p a r a d i g m o f t h e 'selfish o r g a n i s m ' a n d t h e ' c e n t r a l theorem of sociobiology'.
Alternatively,
and
equivalently,
we
can
talk
d i r e c t l y o f g e n e s for p e r f o r m i n g t h e b e h a v i o u r p a t t e r n s u r v i v i n g b e t t e r t h a n their alleles. It is a l w a y s legitimate to postulate genes in a n y discussion of D a r w i n i a n a d a p t a t i o n , a n d i t w i l l b e o n e o f m y c e n t r a l p o i n t s i n this b o o k t h a t i t i s often p o s i t i v e l y b e n e f i c i a l t o d o s o . O b j e c t i o n s , s u c h a s I h a v e h e a r d made,
to
the
'unnecessary
geneticizing'
of the
language
of functional
ethology, betray a fundamental failure to face up to the reality of w h a t D a r w i n i a n selection is all a b o u t . L e t m e i l l u s t r a t e this f a i l u r e b y a n o t h e r a n e c d o t e . I r e c e n t l y a t t e n d e d a research seminar g i v e n by an anthropologist. He w a s t r y i n g to interpret the incidence a m o n g various h u m a n tribes of a p a r t i c u l a r m a t i n g system h a p p e n e d to be p o l y a n d r y )
(it
in terms of a theory of kin selection. A kin
selection theorist c a n m a k e m o d e l s t o predict the c o n d i t i o n s u n d e r w h i c h w e would expect to find polyandry. Thus, on one model applied to T a s m a n i a n native hens ( M a y n a r d S m i t h & R i d p a t h
1972), the p o p u l a t i o n sex ratio
w o u l d need to be male-biased, and partners w o u l d need to be close kin, before a biologist w o u l d predict p o l y a n d r y . T h e a n t h r o p o l o g i s t s o u g h t to s h o w t h a t his p o l y a n d r o u s h u m a n t r i b e s l i v e d u n d e r s u c h c o n d i t i o n s , a n d , b y implication,
that
other
tribes
showing
the
more
normal
patterns
of
m o n o g a m y o r p o l y g y n y lived u n d e r different conditions. T h o u g h fascinated by the information he presented, I tried to w a r n h i m of s o m e difficulties i n his h y p o t h e s i s .
I
pointed out that the t h e o r y of kin
selection is f u n d a m e n t a l l y a genetic theory, a n d that kin-selected a d a p t a t i o n s to local conditions h a d to c o m e a b o u t t h r o u g h the r e p l a c e m e n t of alleles by o t h e r a l l e l e s , o v e r g e n e r a t i o n s . H a d his p o l y a n d r o u s t r i b e s b e e n l i v i n g , I asked,
u n d e r t h e i r c u r r e n t p e c u l i a r c o n d i t i o n s for l o n g e n o u g h — e n o u g h
generations—for the necessary genetic r e p l a c e m e n t to h a v e t a k e n p l a c e ? W a s there, indeed, a n y reason to believe that variations in h u m a n m a t i n g systems are u n d e r g e n e t i c control at a l l ? T h e s p e a k e r , s u p p o r t e d b y m a n y o f his a n t h r o p o l o g i c a l c o l l e a g u e s i n t h e seminar, objected to my d r a g g i n g genes into the discussion. He w a s not talking a b o u t genes, he said, b u t a b o u t a social b e h a v i o u r pattern. S o m e of his c o l l e a g u e s s e e m e d u n c o m f o r t a b l e w i t h t h e v e r y m e n t i o n o f t h e f o u r - l e t t e r w o r d ' g e n e ' . I tried t o p e r s u a d e h i m t h a t i t w a s h e w h o h a d ' d r a g g e d g e n e s in' to the discussion a l t h o u g h , to be sure, he h a d not m e n t i o n e d the w o r d g e n e i n his t a l k . T h a t i s e x a c t l y t h e p o i n t I a m t r y i n g t o m a k e . Y o u c a n n o t t a l k a b o u t k i n s e l e c t i o n , o r a n y o t h e r f o r m o f D a r w i n i a n s e l e c t i o n , without d r a g g i n g g e n e s in, w h e t h e r y o u d o s o e x p l i c i t l y o r n o t . B y e v e n s p e c u l a t i n g
28
G e n e t i c D e t e r m i n i s m and G e n e S e l e c t i o n i s m
a b o u t k i n s e l e c t i o n a s a n e x p l a n a t i o n o f d i f f e r e n c e s i n t r i b a l m a t i n g systems, m y a n t h r o p o l o g i s t f r i e n d w a s i m p l i c i t l y d r a g g i n g g e n e s i n t o the d i s c u s s i o n . I t i s a p i t y h e d i d n o t m a k e i t explicit, b e c a u s e h e w o u l d t h e n h a v e r e a l i z e d w h a t f o r m i d a b l e d i f f i c u l t i e s l a y i n t h e p a t h o f his k i n s e l e c t i o n h y p o t h e s i s : e i t h e r his p o l y a n d r o u s t r i b e s h a d t o h a v e b e e n l i v i n g , i n p a r t i a l g e n e t i c i s o l a t i o n , u n d e r t h e i r p e c u l i a r c o n d i t i o n s for a l a r g e n u m b e r o f c e n t u r i e s , o r n a t u r a l selection h a d to h a v e f a v o u r e d the universal o c c u r r e n c e of genes p r o g r a m ming some complex
' c o n d i t i o n a l s t r a t e g y ' , t h e i r o n y i s t h a t , o f all the
p a r t i c i p a n t s i n t h a t s e m i n a r o n p o l y a n d r y , i t w a s I w h o w a s a d v a n c i n g the least ' g e n e t i c a l l y d e t e r m i n i s t i c ' v i e w o f the b e h a v i o u r u n d e r discussion. Y e t because
I
insisted
on
making
the
genetic
nature
of the
kin
selection
h y p o t h e s i s e x p l i c i t , I e x p e c t I a p p e a r e d t o b e c h a r a c t e r i s t i c a l l y obsessed w i t h g e n e s , a ' t y p i c a l g e n e t i c d e t e r m i n i s t ' . T h e s t o r y i l l u s t r a t e s w e l l the m a i n m e s s a g e o f this c h a p t e r , t h a t f r a n k l y f a c i n g u p t o t h e f u n d a m e n t a l g e n e t i c n a t u r e o f D a r w i n i a n selection i s a l l t o o e a s i l y m i s t a k e n
for a n
unhealthy
p r e o c c u p a t i o n w i t h h e r e d i t a r i a n i n t e r p r e t a t i o n s o f o n t o g e n e t i c development. T h e same prejudice against explicit mention of genes w h e r e one can get a w a y w i t h a n i n d i v i d u a l - l e v e l c i r c u m l o c u t i o n i s c o m m o n a m o n g biologists. T h e s t a t e m e n t , ' g e n e s for p e r f o r m i n g b e h a v i o u r X a r e f a v o u r e d o v e r g e n e s for n o t p e r f o r m i n g X ' h a s a v a g u e l y n a i v e a n d u n p r o f e s s i o n a l r i n g t o it. W h a t e v i d e n c e i s t h e r e for s u c h g e n e s ? H o w d a r e y o u c o n j u r e u p a d hoc g e n e s s i m p l y t o satisfy y o u r h y p o t h e t i c a l c o n v e n i e n c e ! T o s a y ' i n d i v i d u a l s t h a t p e r f o r m X a r e fitter t h a n i n d i v i d u a l s t h a t d o n o t p e r f o r m X ' s o u n d s m u c h m o r e respectable. E v e n if it is not k n o w n to be true, it will probably be a c c e p t e d as a permissible s p e c u l a t i o n . B u t the t w o sentences are exactly e q u i v a l e n t i n m e a n i n g . T h e s e c o n d o n e s a y s n o t h i n g t h a t the f i r s t d o e s n o t s a y m o r e c l e a r l y . Y e t i f w e r e c o g n i z e this e q u i v a l e n c e a n d t a l k e x p l i c i t l y a b o u t g e n e s ' f o r ' a d a p t a t i o n s , w e r u n t h e risk o f b e i n g a c c u s e d o f ' g e n e t i c d e t e r m i n i s m ' . I h o p e I h a v e s u c c e e d e d in s h o w i n g t h a t this risk results from n o t h i n g m o r e than misunderstanding. A sensible a n d u n e x c e p t i o n a b l e w a y o f t h i n k i n g a b o u t n a t u r a l s e l e c t i o n — ' g e n e s e l e c t i o n i s m ' — i s m i s t a k e n for a s t r o n g b e l i e f a b o u t d e v e l o p m e n t — ' g e n e t i c d e t e r m i n i s m ' . A n y o n e w h o thinks clearly a b o u t the details of h o w adaptations c o m e into b e i n g is almost bound to
think,
implicitly
if not
explicitly,
about
genes,
albeit
they
may be
h y p o t h e t i c a l g e n e s . A s I s h a l l s h o w i n this b o o k , t h e r e i s m u c h t o b e said for m a k i n g t h e g e n e t i c basis o f D a r w i n i a n f u n c t i o n a l s p e c u l a t i o n s e x p l i c i t r a t h e r than
implicit.
It
is a good
w a y of avoiding certain
t e m p t i n g errors o f
r e a s o n i n g ( L l o y d 1 9 7 9 ) . I n d o i n g this w e m a y g i v e t h e i m p r e s s i o n , e n t i r e l y for t h e w r o n g r e a s o n ,
of b e i n g obsessed
with genes and
all the m y t h i c
b a g g a g e that genes c a r r y in the c o n t e m p o r a r y journalistic consciousness. But d e t e r m i n i s m , i n t h e sense o f a n i n f l e x i b l e , t r a m l i n e - f o l l o w i n g o n t o g e n y , is, o r should
be,
a
sociobiologists
thousand may
or
miles may
from not
be
our
thoughts.
genetic
Of course,
determinists.
individual
They may
be
Genetic D e t e r m i n i s m and G e n e S e l e c t i o n i s m
Rastafarians,
29
Shakers or Marxists. B u t their private opinions on genetic
determinism, like their p r i v a t e opinions on religion, h a v e n o t h i n g to do w i t h the fact t h a t t h e y use t h e l a n g u a g e o f ' g e n e s for b e h a v i o u r ' w h e n t a l k i n g about natural selection. A l a r g e p a r t o f this c h a p t e r h a s b e e n b a s e d o n t h e a s s u m p t i o n t h a t a biologist m i g h t wish to s p e c u l a t e on the D a r w i n i a n 'function' of b e h a v i o u r patterns. T h i s is not to say that all b e h a v i o u r patterns necessarily h a v e a D a r w i n i a n function.
It m a y be that there is a l a r g e class of b e h a v i o u r
patterns w h i c h are selectively neutral or deleterious to their performers, a n d c a n n o t u s e f u l l y b e r e g a r d e d a s t h e p r o d u c t s o f n a t u r a l s e l e c t i o n . I f so, t h e a r g u m e n t s o f this c h a p t e r d o n o t a p p l y t o t h e m . B u t i t i s l e g i t i m a t e t o s a y T am interested in a d a p t a t i o n . I d o n ' t necessarily think all b e h a v i o u r patterns are adaptations, adaptations.'
but
I
want
Similarly,
to
to study those
behaviour patterns
that are
e x p r e s s a p r e f e r e n c e for s t u d y i n g v e r t e b r a t e s
rather than invertebrates does not c o m m i t us to the belief that all animals a r e v e r t e b r a t e s . G i v e n t h a t o u r field o f i n t e r e s t i s a d a p t i v e b e h a v i o u r , w e c a n n o t talk a b o u t t h e D a r w i n i a n e v o l u t i o n o f t h e o b j e c t s o f i n t e r e s t w i t h o u t postulating a genetic
basis for t h e m .
And
to use
' a g e n e for X '
as
a
c o n v e n i e n t w a y o f t a l k i n g a b o u t ' t h e g e n e t i c basis o f X ' , h a s b e e n s t a n d a r d p r a c t i c e i n p o p u l a t i o n g e n e t i c s for o v e r h a l f a c e n t u r y . T h e q u e s t i o n o f h o w l a r g e i s t h e class o f b e h a v i o u r p a t t e r n s t h a t w e c a n consider to be adaptations is an entirely separate question. It is the subject of the n e x t c h a p t e r .
3 C o n s t r a i n t s on Perfection
I n o n e w a y o r a n o t h e r , this b o o k i s l a r g e l y p r e o c c u p i e d w i t h the l o g i c of D a r w i n i a n
explanations
of function.
Bitter
experience
warns
that
a
biologist w h o shows a strong interest in functional e x p l a n a t i o n is likely to be a c c u s e d , s o m e t i m e s w i t h a p a s s i o n t h a t startles t h o s e m o r e a c c u s t o m e d t o scientific than i d e o l o g i c a l d e b a t e animals
are
perfectly
(Lewontin
optimal—accused
1 9 7 7 ) , of believing that all of
being
an
'adaptationist'
( L e w o n t i n 1 9 7 8 a , b ; G o u l d & L e w o n t i n 1 9 7 9 ) . A d a p t a t i o n i s m is defined as ' t h a t a p p r o a c h t o e v o l u t i o n a r y s t u d i e s w h i c h a s s u m e s w i t h o u t further p r o o f that all aspects of the m o r p h o l o g y , p h y s i o l o g y and b e h a v i o r of organisms are a d a p t i v e o p t i m a l s o l u t i o n s t o p r o b l e m s ' ( L e w o n t i n 1 9 7 9 ) . I n the first d r a f t o f this c h a p t e r I e x p r e s s e d d o u b t s t h a t a n y o n e w a s t r u l y a n a d a p t a t i o n i s t in the e x t r e m e sense, b u t I h a v e r e c e n t l y found the f o l l o w i n g q u o t a t i o n from, i r o n i c a l l y e n o u g h , L e w o n t i n himself: ' T h a t is the one point w h i c h I think all evolutionists are a g r e e d u p o n , that it is virtually impossible to do a better j o b (Lewontin
1967).
than an organism Lewontin
i s d o i n g i n its o w n
has since,
it
seems,
environment'
travelled
his
road
to
D a m a s c u s , s o i t w o u l d b e u n f a i r t o use h i m a s m y a d a p t a t i o n i s t s p o k e s m a n . I n d e e d t o g e t h e r w i t h G o u l d h e h a s , i n r e c e n t y e a r s , b e e n o n e o f the m o s t articulate
and
forceful
critics
of adaptationism.
As
my
representative
adaptationist I take A. J. C a i n , w h o has r e m a i n e d ( C a i n 1979) consistently t r u e t o t h e v i e w s e x p r e s s e d i n his t r e n c h a n t a n d e l e g a n t p a p e r o n
'The
perfection of animals'. W r i t i n g as a t a x o n o m i s t , C a i n (1964) is c o n c e r n e d to attack the traditional d i c h o t o m y b e t w e e n 'functional' characters, w h i c h by implication are not reliable t a x o n o m i c indicators, a n d ' a n c e s t r a l ' c h a r a c t e r s w h i c h are. C a i n a r g u e s f o r c e f u l l y t h a t a n c i e n t ' g r o u n d p l a n ' c h a r a c t e r s , like t h e p e n t a d a c t y l l i m b of tetrapods a n d the a q u a t i c phase of a m p h i b i a n s , are there because they
are
functionally
useful,
rather
than
because
they
are
inescapable
h i s t o r i c a l l e g a c i e s a s i s often i m p l i e d . I f o n e o f t w o g r o u p s 'is i n a n y w a y m o r e p r i m i t i v e t h a n t h e o t h e r , t h e n its p r i m i t i v e n e s s m u s t i n itself b e a n 30
C o n s t r a i n t s on P e r f e c t i o n
adaptation
to
some
less
specialized
mode
o f life
which
it
can
31
pursue
successfully; it c a n n o t be m e r e l y a sign of inefficiency' (p. 5 7 ) . C a i n m a k e s a s i m i l a r p o i n t a b o u t s o - c a l l e d t r i v i a l c h a r a c t e r s , c r i t i c i z i n g D a r w i n for b e i n g t o o r e a d y , u n d e r t h e a t first s i g h t s u r p r i s i n g i n f l u e n c e o f R i c h a r d O w e n , t o c o n c e d e functionlessness: ' N o o n e will suppose that the stripes on the w h e l p o f a l i o n , o r the spots o n t h e y o u n g b l a c k b i r d , a r e o f a n y u s e t o t h e s e animals . . . ' D a r w i n ' s remark must sound foolhardy t o d a y e v e n to the most extreme critic of a d a p t a t i o n i s m . I n d e e d , history seems to be on the side of the
adaptationists,
in
the
sense
that
in
particular
instances
they
have
c o n f o u n d e d t h e scoffers a g a i n a n d a g a i n . C a i n ' s o w n c e l e b r a t e d w o r k , w i t h Sheppard
and
their
school,
on
the
selection
pressures
maintaining
the
b a n d i n g p o l y m o r p h i s m i n t h e s n a i l Cepaea nemoralis m a y h a v e b e e n p a r t l y p r o v o k e d b y t h e fact t h a t 'it h a d b e e n c o n f i d e n t l y a s s e r t e d t h a t i t c o u l d n o t m a t t e r t o a s n a i l w h e t h e r i t h a d o n e b a n d o n its s h e l l o r t w o ' ( C a i n , p . 4 8 ) . 'But perhaps the most r e m a r k a b l e functional interpretation of a " t r i v i a l " c h a r a c t e r i s g i v e n b y M a n t o n ' s w o r k o n t h e d i p l o p o d Polyxenus, i n w h i c h s h e has s h o w n that a c h a r a c t e r formerly d e s c r i b e d as an " o r n a m e n t " ( a n d w h a t c o u l d s o u n d m o r e useless?) i s a l m o s t l i t e r a l l y t h e p i v o t o f t h e a n i m a l ' s l i f e ' (Cain, p. 51). A d a p t a t i o n i s m as a w o r k i n g hypothesis, a l m o s t as a faith, has u n d o u b t e d l y b e e n t h e i n s p i r a t i o n for s o m e o u t s t a n d i n g d i s c o v e r i e s , v o n F r i s c h ( 1 9 6 7 ) , i n defiance of the prestigious o r t h o d o x y of v o n Hess, c o n c l u s i v e l y d e m o n s t r a t e d colour vision in fish and in honeybees by controlled experiments. He w a s d r i v e n t o u n d e r t a k e t h o s e e x p e r i m e n t s b y his refusal t o b e l i e v e t h a t , for e x a m p l e , t h e c o l o u r s o f f l o w e r s w e r e t h e r e for n o r e a s o n , o r s i m p l y t o d e l i g h t m e n ' s e y e s . T h i s is, o f c o u r s e , n o t e v i d e n c e for t h e v a l i d i t y o f a d a p t a t i o n i s t faith. E a c h q u e s t i o n m u s t b e t a c k l e d afresh, o n its m e r i t s . W e n n e r ( 1 9 7 1 ) performed a valuable service in questioning von Frisch's dance l a n g u a g e hypothesis, since he p r o v o k e d J. L. G o u l d ' s (1976) brilliant confirmation
of von
Frisch's
theory.
If Wenner
had
been
more
of an
adaptationist G o u l d ' s research might never h a v e been done, but W e n n e r would
also
not
have
allowed
himself to
be
so
blithely
wrong.
Any
adaptationist, while perhaps c o n c e d i n g that W e n n e r h a d usefully exposed lacunae in von Frisch's original experimental design, w o u l d instantly h a v e j u m p e d , with L i n d a u e r ( 1 9 7 1 ) , o n the f u n d a m e n t a l q u e s t i o n o f w h y bees dance at all. W e n n e r never denied
that they d a n c e , nor that the d a n c e
c o n t a i n e d all t h e i n f o r m a t i o n a b o u t t h e d i r e c t i o n a n d d i s t a n c e o f f o o d t h a t von Frisch c l a i m e d . A l l he denied w a s that other bees used
the d a n c e
information. A n adaptationist c o u l d not h a v e rested h a p p y w i t h the i d e a o f animals performing such a time-consuming, and a b o v e all c o m p l e x a n d s t a t i s t i c a l l y i m p r o b a b l e , a c t i v i t y for n o t h i n g . A d a p t a t i o n i s m c u t s b o t h w a y s , h o w e v e r . I a m n o w d e l i g h t e d t h a t G o u l d d i d his c l i n c h i n g e x p e r i m e n t s , a n d it is entirely to my discredit that, e v e n in the u n l i k e l y e v e n t of my h a v i n g
32
C o n s t r a i n t s on P e r f e c t i o n
been ingenious e n o u g h to think of them, I w o u l d have been too adaptationist t o h a v e b o t h e r e d . I j u s t knew W e n n e r w a s w r o n g ( D a w k i n s 1 9 6 9 ) ! Adaptationist
thinking,
if not
blind
conviction,
has
been
a
valuable
stimulator of testable hypotheses in physiology. Barlow's (1961) recognition of the
overwhelming
functional
need
in
sensory
systems
to
reduce
re-
d u n d a n c y in input led h i m to a u n i q u e l y coherent understanding of a variety o f facts a b o u t s e n s o r y p h y s i o l o g y . A n a l o g o u s f u n c t i o n a l r e a s o n i n g c a n b e applied to the m o t o r system, and to hierarchical systems of organization generally (Dawkins 1 9 7 6 b ; H a i l m a n 1977). Adaptationist conviction cannot tell u s a b o u t p h y s i o l o g i c a l m e c h a n i s m . O n l y p h y s i o l o g i c a l e x p e r i m e n t c a n do that. But cautious adaptationist reasoning can suggest w h i c h of m a n y p o s s i b l e p h y s i o l o g i c a l h y p o t h e s e s a r e m o s t p r o m i s i n g a n d s h o u l d b e tested first. I h a v e t r i e d t o s h o w t h a t a d a p t a t i o n i s m c a n h a v e v i r t u e s a s w e l l a s faults. But
this
chapter's
main
purpose
is
to
list
and
classify
constraints
on
p e r f e c t i o n , t o list t h e m a i n r e a s o n s w h y t h e s t u d e n t o f a d a p t a t i o n s h o u l d proceed
with
caution.
Before
coming
to
my
list
o f six
constraints
on
perfection, I should deal w i t h three others that h a v e been proposed, but w h i c h I f i n d less p e r s u a s i v e . T a k i n g , f i r s t , t h e m o d e r n c o n t r o v e r s y a m o n g biochemical critiques
geneticists
about
of adaptationism,
'neutral
it
is
simply
mutations', irrelevant.
repeatedly If there
cited
are
in
neutral
m u t a t i o n s i n t h e b i o c h e m i s t s ' sense, w h a t this m e a n s i s t h a t a n y c h a n g e i n p o l y p e p t i d e s t r u c t u r e w h i c h t h e y i n d u c e h a s n o effect o n t h e e n z y m a t i c a c t i v i t y of the protein. T h i s m e a n s that the neutral m u t a t i o n will not c h a n g e t h e c o u r s e o f e m b r y o n i c d e v e l o p m e n t , w i l l h a v e n o p h e n o t y p i c effect a t all, a s a
whole-organism
biologist
would
understand
phenotypic
effect.
The
b i o c h e m i c a l c o n t r o v e r s y o v e r n e u t r a l i s m i s c o n c e r n e d w i t h the i n t e r e s t i n g a n d i m p o r t a n t q u e s t i o n o f w h e t h e r all g e n e s u b s t i t u t i o n s h a v e p h e n o t y p i c effects. T h e a d a p t a t i o n i s m c o n t r o v e r s y i s q u i t e different. I t i s c o n c e r n e d w i t h w h e t h e r , given t h a t w e a r e d e a l i n g w i t h a p h e n o t y p i c effect b i g e n o u g h t o see a n d ask q u e s t i o n s a b o u t , w e s h o u l d a s s u m e t h a t i t i s t h e p r o d u c t o f n a t u r a l s e l e c t i o n . T h e b i o c h e m i s t ' s ' n e u t r a l m u t a t i o n s ' a r e m o r e t h a n n e u t r a l . A s far a s t h o s e o f u s w h o l o o k a t gross m o r p h o l o g y , p h y s i o l o g y a n d b e h a v i o u r a r e c o n c e r n e d , t h e y a r e n o t m u t a t i o n s a t a l l . I t w a s i n this spirit t h a t M a y n a r d S m i t h (1976b) w r o t e : 'I interpret "rate of e v o l u t i o n " as a rate of adaptive c h a n g e . I n this s e n s e , t h e s u b s t i t u t i o n o f a n e u t r a l a l l e l e w o u l d n o t c o n s t i t u t e e v o l u t i o n . . . ' I f a w h o l e - o r g a n i s m b i o l o g i s t sees a g e n e t i c a l l y d e t e r m i n e d difference a m o n g p h e n o t y p e s , he already knows he c a n n o t be dealing with neutrality
in
the
sense
of the
modern
controversy
among
biochemical
geneticists. H e m i g h t , n e v e r t h e l e s s , b e d e a l i n g w i t h a n e u t r a l c h a r a c t e r i n t h e sense o f an
earlier controversy
(Fisher &
Ford
1950;
Wright
1951).
A genetic
d i f f e r e n c e c o u l d s h o w i t s e l f a t t h e p h e n o t y p i c l e v e l , y e t still b e s e l e c t i v e l y
C o n s t r a i n t s on P e r f e c t i o n
33
neutral. But m a t h e m a t i c a l calculations such as those of Fisher (1930b) a n d Haldane (1932a) show how unreliable h u m a n subjective j u d g e m e n t can be o n the ' o b v i o u s l y t r i v i a l ' n a t u r e o f s o m e b i o l o g i c a l c h a r a c t e r s . H a l d a n e , for e x a m p l e , s h o w e d that, with plausible assumptions a b o u t a t y p i c a l p o p u l a t i o n , a s e l e c t i o n p r e s s u r e as w e a k as 1
in
1000 w o u l d t a k e o n l y a f e w
thousand generations to push an initially rare m u t a t i o n to fixation, a small time by g e o l o g i c a l standards. It a p p e a r s that, in the c o n t r o v e r s y referred to a b o v e , W r i g h t w a s m i s u n d e r s t o o d (see b e l o w ) . W r i g h t ( 1 9 8 0 ) w a s e m b a r rassed a t f i n d i n g t h e i d e a o f e v o l u t i o n o f n o n a d a p t i v e c h a r a c t e r s b y g e n e t i c drift
labelled
previously rejected
the
'Sewall
advanced
it
from
Wright
effect',
the s a m e idea,
the
first
(1929),
'not
only
but because stating
that
"inevitably to degeneration and extinction" '.
because
I
pure I
others
myself had random
drift
have attributed
had
strongly leads
apparent
n o n a d a p t i v e t a x o n o m i c differences to pleiotropy, w h e r e not m e r e l y ignorance of an a d a p t i v e significance.' W r i g h t was in fact s h o w i n g h o w a subtle mixture
o f drift
and
selection
can
produce
adaptations
superior
to
the
p r o d u c t s o f s e l e c t i o n a l o n e (see p p . 3 9 - 4 0 ) . A second suggested constraint on perfection concerns allometry ( H u x l e y 1 9 3 2 ) : 'In c e r v i n e deer, antler size increases m o r e t h a n p r o p o r t i o n a t e l y to body
s i z e . . . so
that
larger
deer
have
more
than
proportionately
large
a n t l e r s . It is t h e n u n n e c e s s a r y to g i v e a s p e c i f i c a l l y a d a p t i v e r e a s o n for t h e extremely large antlers of large deer' ( L e w o n t i n 1 9 7 9 ) . W e l l , L e w o n t i n has a p o i n t h e r e , b u t I w o u l d p r e f e r t o r e p h r a s e it. A s i t s t a n d s i t s u g g e s t s t h a t t h e allometric
constant
is
constant
in
a
God-given
immutable
sense.
But
constants on one time scale c a n be variables on another. T h e allometric c o n s t a n t i s a p a r a m e t e r o f e m b r y o n i c d e v e l o p m e n t . Like; a n y o t h e r s u c h parameter it m a y be subject to genetic variation a n d therefore it m a y c h a n g e over evolutionary time (Clutton-Brock & H a r v e y 1979). L e w o n t i n ' s remark turns o u t t o b e a n a l o g o u s t o t h e f o l l o w i n g : a l l p r i m a t e s h a v e t e e t h ; this i s j u s t a
plain
fact
about
primates,
and
it
is
therefore
unnecessary
to
give
a
s p e c i f i c a l l y a d a p t i v e r e a s o n for t h e p r e s e n c e o f t e e t h i n p r i m a t e s . W h a t h e p r o b a b l y m e a n t to say is s o m e t h i n g like the f o l l o w i n g . Deer have
evolved
antlers r e l a t i v e t o allometry.
Very
development nothing
to
probably
occurred do
a developmental
mechanism
b o d y size is a l l o m e t r i c w i t h
with
the
under the
the
social
evolution
of
such
this
allometric
influence of selection function
that
growth
of
a p a r t i c u l a r constant of
of antlers:
system
pressures probably
of
having it
was
conveniently c o m p a t i b l e w i t h pre-existing d e v e l o p m e n t a l processes in a w a y w h i c h w e shall not understand until w e k n o w m o r e a b o u t the b i o c h e m i c a l and cellular details of e m b r y o l o g y . M a y b e ethological consequences of the e x t r a l a r g e a n t l e r s o f l a r g e d e e r e x e r t a s e l e c t i v e effect, b u t this s e l e c t i o n pressure i s l i k e l y t o b e s w a m p e d i n i m p o r t a n c e b y o t h e r s e l e c t i o n p r e s s u r e s concerned with concealed internal e m b r y o l o g i c a l details.
34
C o n s t r a i n t s on P e r f e c t i o n
W i l l i a m s ( 1 9 6 6 , p . 16) i n v o k e d a l l o m e t r y i n t h e s e r v i c e o f a s p e c u l a t i o n a b o u t t h e s e l e c t i o n p r e s s u r e s l e a d i n g t o i n c r e a s e d b r a i n size i n m a n . H e suggested that the p r i m e focus of selection w a s on early teachability, at an e l e m e n t a r y l e v e l , o f c h i l d r e n . ' T h e r e s u l t i n g s e l e c t i o n for a c q u i r i n g v e r b a l f a c i l i t y a s e a r l y a s p o s s i b l e m i g h t h a v e p r o d u c e d , a s a n a l l o m e t r i c effect o n cerebral development, populations in which an occasional Leonardo might a r i s e . ' W i l l i a m s , h o w e v e r , d i d n o t see a l l o m e t r y a s a w e a p o n a g a i n s t the use o f a d a p t i v e e x p l a n a t i o n s . O n e feels t h a t h e w a s r i g h t l y less l o y a l t o his particular
theory
of cerebral
hypertrophy
than
to
the
general
principle
e n u n c i a t e d i n his c o n c l u d i n g r h e t o r i c a l q u e s t i o n :
'Is it not reasonable to
anticipate
mind
that
our
understanding
o f the
human
would
be
aided
g r e a t l y b y k n o w i n g t h e p u r p o s e for w h i c h i t w a s d e s i g n e d ? ' W h a t h a s b e e n s a i d o f a l l o m e t r y a p p l i e s a l s o t o p l e i o t r o p y , t h e possession b y o n e g e n e o f m o r e t h a n o n e p h e n o t y p i c effect. T h i s i s t h e t h i r d o f t h e suggested constraints on perfection that I w a n t to get out of the w a y before e m b a r k i n g o n m y m a i n list. I t h a s a l r e a d y b e e n m e n t i o n e d i n m y q u o t a t i o n from W r i g h t . A possible source of confusion here is that p l e i o t r o p y has b e e n u s e d a s a w e a p o n b y b o t h sides i n this d e b a t e , i f i n d e e d i t i s a r e a l d e b a t e . Fisher
(1930b)
reasoned
that it was unlikely
that a n y one of a gene's
p h e n o t y p i c effects w a s n e u t r a l , s o h o w m u c h m o r e u n l i k e l y w a s i t t h a t all o f a g e n e ' s p l e i o t r o p i c effects c o u l d b e n e u t r a l . L e w o n t i n ( 1 9 7 9 ) , o n the o t h e r hand,
remarked
that
'many
changes
in
characters
are
the
result
of
p l e i o t r o p i c g e n e a c t i o n , r a t h e r t h a n the direct result of selection on the c h a r a c t e r itself. T h e y e l l o w c o l o r o f t h e M a l p i g h i a n t u b u l e s o f a n i n s e c t c a n n o t itself be the subject of n a t u r a l selection since that color c a n never be s e e n b y a n y o r g a n i s m . R a t h e r i t i s t h e p l e i o t r o p i c c o n s e q u e n c e o f red e y e p i g m e n t m e t a b o l i s m , w h i c h m a y be a d a p t i v e . ' T h e r e is no real disagreem e n t h e r e . F i s h e r w a s t a l k i n g o f t h e s e l e c t i v e effects o n a g e n e t i c m u t a t i o n , L e w o n t i n o f s e l e c t i v e effects o n a p h e n o t y p i c c h a r a c t e r ; distinction,
indeed,
as
I
was
making
in
discussing
i t i s the s a m e
neutrality
in
the
b i o c h e m i c a l geneticists' sense. L e w o n t i n ' s point a b o u t p l e i o t r o p y is related to a n o t h e r one w h i c h I shall c o m e o n t o b e l o w , a b o u t t h e p r o b l e m o f d e f i n i n g w h a t h e c a l l s the n a t u r a l ' s u t u r e l i n e s ' , t h e ' p h e n o t y p i c u n i t s ' o f e v o l u t i o n . S o m e t i m e s t h e d u a l effects o f a g e n e a r e i n p r i n c i p l e i n s e p a r a b l e ; t h e y a r e d i f f e r e n t v i e w s o f the s a m e t h i n g , j u s t a s E v e r e s t u s e d t o h a v e t w o n a m e s d e p e n d i n g o n w h i c h side i t w a s s e e n f r o m . W h a t a b i o c h e m i s t sees a s a n o x y g e n - c a r r y i n g m o l e c u l e m a y b e seen by an ethologist as red c o l o r a t i o n . B u t there is a m o r e interesting kind of p l e i o t r o p y i n w h i c h t h e t w o p h e n o t y p i c effects o f a m u t a t i o n a r e s e p a r a b l e . T h e p h e n o t y p i c effect o f a n y g e n e ( v e r s u s its a l l e l e s ) i s n o t a p r o p e r t y o f t h e g e n e alone, b u t also of the e m b r y o l o g i c a l context in w h i c h it acts. T h i s a l l o w s a b u n d a n t o p p o r t u n i t i e s for t h e p h e n o t y p i c effects o f o n e m u t a t i o n t o be modified by others, a n d is the basis of such respected ideas as Fisher's
C o n s t r a i n t s on P e r f e c t i o n
(1930a)
theory o f the e v o l u t i o n o f d o m i n a n c e ,
35
the M e d a w a r ( 1 9 5 2 )
and
Williams (1957) theories o f senescence, and H a m i l t o n ' s (1967) theory o f Y c h r o m o s o m e inertness.
In the present connection,
if a m u t a t i o n has one
b e n e f i c i a l effect a n d o n e h a r m f u l o n e , t h e r e i s n o r e a s o n w h y s e l e c t i o n s h o u l d not f a v o u r m o d i f i e r g e n e s t h a t d e t a c h t h e t w o p h e n o t y p i c effects, o r t h a t r e d u c e t h e h a r m f u l effect w h i l e e n h a n c i n g t h e b e n e f i c i a l o n e . A s i n t h e c a s e of allometry,
Lewontin
took
too static
a v i e w of gene
action,
treating
pleiotropy as if it w a s a p r o p e r t y of the g e n e rather than of the interaction b e t w e e n t h e g e n e a n d its ( m o d i f i a b l e ) e m b r y o l o g i c a l c o n t e x t . T h i s b r i n g s m e t o m y o w n c r i t i q u e o f n a i v e a d a p t a t i o n i s m , m y o w n list o f c o n s t r a i n t s o n p e r f e c t i o n , a list w h i c h h a s m u c h i n c o m m o n w i t h t h o s e o f L e w o n t i n a n d C a i n , a n d those o f M a y n a r d S m i t h ( 1 9 7 8 b ) , O s t e r a n d W i l s o n ( 1 9 7 8 ) , W i l l i a m s ( 1 9 6 6 ) , C u r i o ( 1 9 7 3 ) a n d o t h e r s . T h e r e is, i n d e e d , m u c h more a g r e e m e n t than the p o l e m i c a l tone of recent critiques w o u l d suggest. I shall n o t b e c o n c e r n e d w i t h p a r t i c u l a r c a s e s , e x c e p t a s e x a m p l e s . A s C a i n a n d L e w o n t i n b o t h stress,
it is not of general interest to c h a l l e n g e our
ingenuity in d r e a m i n g up possible a d v a n t a g e s of p a r t i c u l a r strange things that animals d o . H e r e w e are interested i n the m o r e g e n e r a l q u e s t i o n o f w h a t the t h e o r y o f n a t u r a l s e l e c t i o n e n t i t l e s u s t o e x p e c t . M y f i r s t c o n s t r a i n t o n perfection is an obvious one, mentioned by most writers on a d a p t a t i o n .
T i m e lags T h e animal we are looking at is v e r y p r o b a b l y out of date, built u n d e r the influence of genes that w e r e selected in some earlier era w h e n conditions w e r e different. M a y n a r d S m i t h ( 1 9 7 6 b ) g i v e s a q u a n t i t a t i v e m e a s u r e o f this effect, t h e ' l a g l o a d ' . H e ( M a y n a r d S m i t h
1978b)
cites N e l s o n ' s d e m o n -
stration that g a n n e t s , w h o n o r m a l l y lay o n l y o n e e g g , are q u i t e c a p a b l e o f successfully i n c u b a t i n g a n d r e a r i n g t w o i f a n e x t r a o n e i s e x p e r i m e n t a l l y a d d e d . O b v i o u s l y a n a w k w a r d c a s e for t h e L a c k h y p o t h e s i s o n o p t i m a l c l u t c h s i z e , a n d L a c k h i m s e l f ( 1 9 6 6 ) w a s n o t s l o w t o use t h e ' t i m e - l a g ' e s c a p e route. H e suggested, entirely plausibly, that the g a n n e t c l u t c h size o f o n e e g g e v o l v e d d u r i n g a t i m e w h e n food w a s less p l e n t i f u l , a n d t h a t t h e r e h a d n o t y e t b e e n t i m e for t h e m t o e v o l v e t o m e e t t h e c h a n g e d c o n d i t i o n s . S u c h post hoc
rescuing
of a
hypothesis
in
trouble
is
apt
to
provoke
a c c u s a t i o n s o f t h e sin o f u n f a l s i f i a b i l i t y , b u t I f i n d s u c h a c c u s a t i o n s r a t h e r unconstructive, almost nihilistic. We are not in P a r l i a m e n t or a c o u r t of l a w , with
advocates of D a r w i n i s m scoring d e b a t i n g points against
opponents,
and vice versa. W i t h the e x c e p t i o n of a few g e n u i n e o p p o n e n t s of D a r w i n i s m , who
are
unlikely
to
be
reading
this,
we
are
all
in
this
together,
all
D a r w i n i a n s w h o s u b s t a n t i a l l y a g r e e o n h o w w e i n t e r p r e t w h a t is, after a l l , the o n l y w o r k a b l e t h e o r y w e h a v e t o e x p l a i n t h e o r g a n i z e d c o m p l e x i t y o f life. W e s h o u l d a l l s i n c e r e l y w a n t t o know w h y g a n n e t s l a y o n l y o n e e g g w h e n t h e y c o u l d l a y t w o , r a t h e r t h a n t r e a t i n g t h e fact a s a d e b a t i n g p o i n t . L a c k ' s
36
C o n s t r a i n t s on Perfection
i n v o k i n g o f t h e ' t i m e - l a g ' h y p o t h e s i s m a y h a v e b e e n post hoc, b u t i t i s still t h o r o u g h l y p l a u s i b l e , a n d i t i s t e s t a b l e . N o d o u b t t h e r e a r e o t h e r possibilities w h i c h , w i t h luck, m a y also be testable. M a y n a r d S m i t h is surely right that we should
leave
aside
the
'defeatist'
(Tinbergen
1965)
and
untestable
' n a t u r a l s e l e c t i o n h a s b u n g l e d a g a i n ' e x p l a n a t i o n as a last resort, as a m a t t e r o f s i m p l e r e s e a r c h s t r a t e g y i f n o t h i n g else. L e w o n t i n ( 1 9 7 8 b ) says m u c h the s a m e : ' I n a sense, then, biologists are forced to the e x t r e m e adaptationist p r o g r a m b e c a u s e the alternatives, a l t h o u g h they are u n d o u b t e d l y operative in m a n y cases, are untestable in particular cases.' R e t u r n i n g t o t h e t i m e - l a g effect itself, s i n c e m o d e r n m a n h a s d r a s t i c a l l y c h a n g e d the e n v i r o n m e n t of m a n y a n i m a l s a n d plants o v e r a time-scale that i s n e g l i g i b l e b y o r d i n a r y e v o l u t i o n a r y s t a n d a r d s , w e c a n e x p e c t t o see a n a c h r o n i s t i c a d a p t a t i o n s rather often. T h e h e d g e h o g a n t i p r e d a t o r response of rolling up into a ball is sadly inadequate against motor cars. L a y critics frequently b r i n g u p some a p p a r e n t l y m a l a d a p t i v e feature o f modern down
human
behaviour—adoption,
a challenge to
'explain
say,
or
contraception—and fling
t h a t i f y o u c a n w i t h y o u r selfish g e n e s ' .
O b v i o u s l y , a s L e w o n t i n , G o u l d a n d o t h e r s h a v e r i g h t l y stressed, i t w o u l d b e possible, d e p e n d i n g on one's ingenuity, to pull a 'sociobiological' explan a t i o n o u t o f a h a t , a 'just-so s t o r y ' , b u t I a g r e e w i t h t h e m a n d C a i n t h a t t h e a n s w e r i n g of such c h a l l e n g e s is a trivial e x e r c i s e ; indeed it is likely to be p o s i t i v e l y h a r m f u l . A d o p t i o n a n d c o n t r a c e p t i o n , like r e a d i n g , m a t h e m a t i c s , a n d s t r e s s - i n d u c e d illness, a r e p r o d u c t s o f a n a n i m a l t h a t i s l i v i n g i n a n e n v i r o n m e n t r a d i c a l l y d i f f e r e n t f r o m t h e o n e i n w h i c h its g e n e s w e r e n a t u r a l l y selected. T h e question, about the a d a p t i v e significance of b e h a v i o u r in an a r t i f i c i a l w o r l d , s h o u l d n e v e r h a v e b e e n p u t ; a n d a l t h o u g h a silly q u e s t i o n m a y d e s e r v e a silly a n s w e r , it is wiser to g i v e no a n s w e r at all a n d to explain why. A useful a n a l o g y h e r e i s o n e t h a t I h e a r d f r o m R . D . A l e x a n d e r . M o t h s f l y i n t o c a n d l e f l a m e s , a n d this d o e s n o t h i n g t o h e l p t h e i r i n c l u s i v e f i t n e s s . I n the w o r l d before candles w e r e invented, small sources of bright light in darkness w o u l d either h a v e b e e n celestial b o d i e s at o p t i c a l infinity, or they m i g h t h a v e b e e n escape holes from c a v e s or other enclosed spaces. T h e latter case i m m e d i a t e l y s u g g e s t s a s u r v i v a l v a l u e for a p p r o a c h i n g l i g h t s o u r c e s . T h e f o r m e r c a s e a l s o s u g g e s t s o n e , b u t i n a m o r e i n d i r e c t sense ( F r a e n k e l & G u n n 1 9 4 0 ) . M a n y i n s e c t s use c e l e s t i a l b o d i e s a s c o m p a s s e s . S i n c e these a r e a t optical infinity, rays from them are parallel, and an insect that maintains a f i x e d o r i e n t a t i o n of, s a y , 3 0 ° t o t h e m w i l l g o i n a s t r a i g h t l i n e . B u t i f the r a y s d o n o t c o m e f r o m i n f i n i t y t h e y w i l l n o t b e p a r a l l e l , a n d a n insect t h a t b e h a v e s i n this w a y w i l l s p i r a l i n t o t h e l i g h t s o u r c e (if s t e e r i n g a n a c u t e a n g l e d c o u r s e ) o r s p i r a l a w a y (if s t e e r i n g a n o b t u s e - a n g l e d c o u r s e ) o r o r b i t t h e s o u r c e (if s t e e r i n g a c o u r s e o f e x a c t l y 9 0 ° t o t h e r a y s ) . S e l f - i m m o l a t i o n b y i n s e c t s i n c a n d l e f l a m e s , t h e n , h a s n o s u r v i v a l v a l u e i n itself: a c c o r d i n g t o
C o n s t r a i n t s on P e r f e c t i o n
37
this h y p o t h e s i s , i t i s a b y p r o d u c t o f t h e useful h a b i t o f s t e e r i n g b y m e a n s o f sources o f light w h i c h are ' a s s u m e d ' t o b e a t infinity. T h a t a s s u m p t i o n w a s o n c e safe. I t n o w i s safe n o l o n g e r , a n d i t m a y b e t h a t s e l e c t i o n i s e v e n n o w w o r k i n g t o modify the insects' b e h a v i o u r . ( N o t necessarily, h o w e v e r . T h e o v e r h e a d costs o f m a k i n g t h e n e c e s s a r y i m p r o v e m e n t s m a y o u t w e i g h t h e benefits t h e y m i g h t b r i n g : m o t h s t h a t p a y t h e costs o f d i s c r i m i n a t i n g c a n d l e s from stars m a y b e less s u c c e s s f u l , o n a v e r a g e , t h a n m o t h s t h a t d o n o t a t t e m p t the c o s t l y d i s c r i m i n a t i o n a n d a c c e p t t h e l o w risk o f s e l f - i m m o l a t i o n — s e e n e x t chapter.) But now we h a v e reached a problem w h i c h is more subtle than the simple t i m e - l a g h y p o t h e s i s itself. T h i s i s t h e p r o b l e m , a l r e a d y m e n t i o n e d , a b o u t w h a t characteristics of animals we choose to r e c o g n i z e as units w h i c h require e x p l a n a t i o n . A s L e w o n t i n ( 1 9 7 9 ) p u t s it, ' W h a t a r e t h e " n a t u r a l " s u t u r e lines for e v o l u t i o n a r y d y n a m i c s ? W h a t i s t h e t o p o l o g y o f p h e n o t y p e i n e v o l u t i o n ? W h a t a r e t h e p h e n o t y p i c units o f e v o l u t i o n ? ' T h e c a n d l e f l a m e p a r a d o x arose o n l y because of the w a y in w h i c h we chose to c h a r a c t e r i z e the moth's behaviour. W e asked ' W h y d o moths f l y into c a n d l e f l a m e s ? ' and were puzzled. If we had characterized the b e h a v i o u r differently and asked 'Why
do
moths
maintain
a
fixed
angle
to
light
rays
(a
habit
which
i n c i d e n t a l l y c a u s e s t h e m t o s p i r a l i n t o the l i g h t s o u r c e i f t h e r a y s h a p p e n n o t to be p a r a l l e l ) ? ' , we should not h a v e b e e n so p u z z l e d . Consider h u m a n m a l e h o m o s e x u a l i t y as a m o r e serious e x a m p l e . On the face o f it, t h e e x i s t e n c e o f a s u b s t a n t i a l m i n o r i t y o f m e n w h o p r e f e r s e x u a l r e l a t i o n s w i t h t h e i r o w n sex r a t h e r t h a n w i t h t h e o p p o s i t e s e x c o n s t i t u t e s a p r o b l e m for a n y s i m p l e D a r w i n i a n t h e o r y . T h e r a t h e r d i s c u r s i v e title o f a privately circulated homosexualist p a m p h l e t , w h i c h the author w a s kind e n o u g h t o send m e , s u m m a r i z e s the p r o b l e m : ' W h y are there " g a y s " a t a l l ? W h y hasn't evolution eliminated author,
incidentally,
thinks
the
" g a y n e s s " millions of years a g o ? ' T h e problem
so
important
that
it
seriously
u n d e r m i n e s t h e w h o l e D a r w i n i a n v i e w o f life. T r i v e r s ( 1 9 7 4 ) , W i l s o n ( 1 9 7 5 , 1978), and especially W e i n r i c h (1976) h a v e considered various versions of the p o s s i b i l i t y t h a t h o m o s e x u a l s m a y , a t s o m e t i m e i n h i s t o r y , h a v e b e e n f u n c t i o n a l l y e q u i v a l e n t t o sterile w o r k e r s , f o r e g o i n g p e r s o n a l r e p r o d u c t i o n the b e t t e r t o c a r e for o t h e r r e l a t i v e s . I d o n o t f i n d this i d e a p a r t i c u l a r l y plausible ( R i d l e y & D a w k i n s in press), certainly no m o r e so than a 'sneaky m a l e ' h y p o t h e s i s . A c c o r d i n g t o this l a t t e r i d e a , h o m o s e x u a l i t y r e p r e s e n t s a n ' a l t e r n a t i v e m a l e t a c t i c ' for o b t a i n i n g m a t i n g s w i t h f e m a l e s . I n a s o c i e t y w i t h harem defence by dominant males, a male w h o is k n o w n to be h o m o s e x u a l is more likely to be tolerated by a d o m i n a n t m a l e than a k n o w n heterosexual m a l e , a n d a n o t h e r w i s e s u b o r d i n a t e m a l e m a y b e a b l e , b y v i r t u e o f this, t o obtain clandestine copulations with females. B u t I raise t h e ' s n e a k y m a l e ' h y p o t h e s i s n o t as a p l a u s i b l e p o s s i b i l i t y so m u c h as a w a y of d r a m a t i z i n g h o w easy and inconclusive it is to d r e a m up
C o n s t r a i n t s on P e r f e c t i o n
e x p l a n a t i o n s o f this k i n d ( L e w o n t i n , 1 9 7 9 , u s e d t h e s a m e d i d a c t i c t r i c k i n d i s c u s s i n g a p p a r e n t h o m o s e x u a l i t y i n Drosophila). T h e m a i n p o i n t I w i s h t o m a k e is q u i t e different a n d m u c h m o r e i m p o r t a n t . It is a g a i n the point a b o u t h o w we c h a r a c t e r i z e the p h e n o t y p i c feature that we are trying to explain. H o m o s e x u a l i t y is, of c o u r s e , a p r o b l e m for D a r w i n i a n s o n l y if t h e r e is a genetic c o m p o n e n t to the difference b e t w e e n h o m o s e x u a l a n d heterosexual i n d i v i d u a l s . W h i l e the e v i d e n c e is controversial
(Weinrich
1 9 7 6 ) , let u s
a s s u m e for t h e s a k e o f a r g u m e n t t h a t this i s t h e c a s e . N o w the q u e s t i o n arises, w h a t d o e s it mean to s a y t h e r e is a g e n e t i c c o m p o n e n t to t h e d i f f e r e n c e , in c o m m o n p a r l a n c e t h a t t h e r e is a g e n e (or g e n e s ) ' f o r ' h o m o s e x u a l i t y ? It is a fundamental
truism,
of logic more than of genetics,
that the p h e n o t y p i c
'effect' of a g e n e is a c o n c e p t that has m e a n i n g o n l y if the context of environmental
influences
is
specified,
environment
being
understood
to
i n c l u d e a l l t h e o t h e r g e n e s in t h e g e n o m e . A g e n e ' f o r ' A in e n v i r o n m e n t X m a y w e l l t u r n o u t t o b e a g e n e for B i n e n v i r o n m e n t Y .
It is simply
m e a n i n g l e s s t o s p e a k o f a n a b s o l u t e , c o n t e x t - f r e e , p h e n o t y p i c effect o f a g i v e n gene. Even
if there
are
genes
which,
in
today's
environment,
produce
a
h o m o s e x u a l p h e n o t y p e , this d o e s n o t m e a n t h a t i n a n o t h e r e n v i r o n m e n t , s a y that of o u r Pleistocene ancestors, they w o u l d h a v e had the same p h e n o t y p i c effect. A g e n e for h o m o s e x u a l i t y i n o u r m o d e r n e n v i r o n m e n t m i g h t h a v e b e e n a g e n e for s o m e t h i n g u t t e r l y different i n t h e P l e i s t o c e n e . S o , w e h a v e the p o s s i b i l i t y o f a s p e c i a l k i n d o f ' t i m e - l a g effect' h e r e . I t m a y b e t h a t t h e p h e n o t y p e w h i c h w e a r e t r y i n g t o e x p l a i n d i d n o t e v e n exist i n s o m e e a r l i e r e n v i r o n m e n t , e v e n t h o u g h the g e n e did then exist. T h e o r d i n a r y time-lag effect w h i c h w e d i s c u s s e d a t t h e b e g i n n i n g o f this s e c t i o n w a s c o n c e r n e d w i t h c h a n g e s i n t h e e n v i r o n m e n t a s m a n i f e s t e d i n c h a n g e d s e l e c t i o n pressures. W e h a v e n o w a d d e d the more subtle point that changes in the environment m a y c h a n g e t h e v e r y n a t u r e o f t h e p h e n o t y p i c c h a r a c t e r w e set o u t t o e x p l a i n .
Historical constraints T h e j e t e n g i n e s u p e r s e d e d t h e p r o p e l l e r e n g i n e b e c a u s e , for m o s t p u r p o s e s , i t was superior.
T h e d e s i g n e r s o f t h e first j e t e n g i n e s t a r t e d
with a clean
d r a w i n g board. I m a g i n e w h a t they w o u l d h a v e produced if they had been constrained to ' e v o l v e ' the first j e t engine from an existing propeller engine, c h a n g i n g one c o m p o n e n t at a time, nut by nut, screw by screw, rivet by rivet. A j e t e n g i n e so assembled w o u l d be a w e i r d c o n t r a p t i o n indeed. It is hard to i m a g i n e that an a e r o p l a n e designed in that e v o l u t i o n a r y w a y w o u l d e v e r g e t off t h e g r o u n d . Y e t i n o r d e r t o c o m p l e t e t h e b i o l o g i c a l a n a l o g y w e h a v e t o a d d y e t a n o t h e r c o n s t r a i n t . N o t o n l y m u s t t h e e n d p r o d u c t g e t off the g r o u n d ; s o must e v e r y i n t e r m e d i a t e a l o n g the w a y , a n d e a c h intermediate m u s t b e s u p e r i o r t o its p r e d e c e s s o r . W h e n l o o k e d a t i n this l i g h t , far from
C o n s t r a i n t s on P e r f e c t i o n
39
expecting animals to be perfect we m a y w o n d e r that a n y t h i n g a b o u t them works at all. Examples character
o f the
Heath
of animals
are
Robinson harder
(or R u b e
to
be
Goldberg—Gould
confident
of than
the
1978)
previous
paragraph might lead us to expect. A favourite e x a m p l e , suggested to me by Professor J . D . C u r r e y , i s t h e r e c u r r e n t l a r y n g e a l n e r v e . T h e s h o r t e s t d i s t a n c e from
the
brain
to
the
larynx
in
a
mammal,
especially
a
giraffe,
is
e m p h a t i c a l l y not v i a the posterior side of the aorta, y e t that is the route t a k e n by the recurrent l a r y n g e a l . P r e s u m a b l y there o n c e w a s a t i m e in the r e m o t e ancestry of the m a m m a l s w h e n the straight line from origin to e n d o r g a n of the n e r v e did run posterior to the aorta. W h e n , in d u e course, the n e c k b e g a n t o l e n g t h e n , t h e n e r v e l e n g t h e n e d its d e t o u r p o s t e r i o r t o t h e a o r t a , b u t the m a r g i n a l cost o f e a c h s t e p i n t h e l e n g t h e n i n g o f t h e d e t o u r w a s n o t g r e a t . A major mutation might h a v e re-routed the nerve c o m p l e t e l y , but only at a cost o f g r e a t u p h e a v a l i n e a r l y e m b r y o n i c p r o c e s s e s . P e r h a p s a p r o p h e t i c , G o d - l i k e designer b a c k i n the D e v o n i a n c o u l d h a v e foreseen the giraffe a n d d e s i g n e d the o r i g i n a l e m b r y o n i c r o u t i n g o f t h e n e r v e d i f f e r e n t l y , b u t n a t u r a l selection
has
no
foresight.
As
Sydney
Brenner
has
remarked,
natural
s e l e c t i o n c o u l d n o t b e e x p e c t e d t o h a v e f a v o u r e d s o m e useless m u t a t i o n i n the C a m b r i a n s i m p l y b e c a u s e 'it m i g h t c o m e i n h a n d y i n t h e C r e t a c e o u s ' . T h e P i c a s s o - l i k e f a c e o f a flatfish s u c h a s a s o l e , g r o t e s q u e l y t w i s t e d t o b r i n g b o t h e y e s r o u n d t o t h e s a m e side o f t h e h e a d , i s a n o t h e r s t r i k i n g demonstration
of a
historical
constraint on
perfection.
The
evolutionary
h i s t o r y o f these fish i s s o c l e a r l y w r i t t e n i n t o t h e i r a n a t o m y , t h a t t h e e x a m p l e is a g o o d one to thrust d o w n the throats of religious fundamentalists. M u c h the s a m e c o u l d b e s a i d o f t h e c u r i o u s f a c t t h a t t h e r e t i n a o f t h e v e r t e b r a t e e y e appears to be installed b a c k w a r d s . T h e light-sensitive 'photocells' are at the b a c k o f the r e t i n a , a n d l i g h t h a s t o pass t h r o u g h t h e c o n n e c t i n g c i r c u i t r y , with some inevitable attenuation,
before it reaches them.
P r e s u m a b l y it
w o u l d be possible to write d o w n a v e r y l o n g s e q u e n c e of mutations w h i c h would eventually lead to the production of an eye whose retina w a s 'the right w a y r o u n d ' a s i t i s i n c e p h a l o p o d s , a n d this m i g h t b e , i n t h e e n d , s l i g h t l y m o r e efficient. B u t t h e c o s t i n e m b r y o l o g i c a l u p h e a v a l w o u l d b e s o g r e a t t h a t the i n t e r m e d i a t e s t a g e s w o u l d b e h e a v i l y d i s f a v o u r e d b y n a t u r a l s e l e c t i o n i n c o m p a r i s o n w i t h t h e r i v a l , p a t c h e d - u p j o b w h i c h d o e s , after a l l , w o r k p r e t t y well. P i t t e n d r i g h (1958) has well said of a d a p t i v e o r g a n i z a t i o n that it is 'a p a t c h w o r k of makeshifts pieced together, as it w e r e , from w h a t w a s a v a i l a b l e w h e n o p p o r t u n i t y k n o c k e d , a n d a c c e p t e d in the hindsight, not the foresight, o f n a t u r a l s e l e c t i o n ' (see a l s o J a c o b , 1 9 7 7 , o n ' t i n k e r i n g ' ) . S e w a l l W r i g h t ' s (1932) m e t a p h o r , w h i c h has b e c o m e k n o w n u n d e r the n a m e of the ' a d a p t i v e l a n d s c a p e ' , c o n v e y s the s a m e i d e a that selection in favour of local o p t i m a prevents evolution in
the direction of ultimately
40
C o n s t r a i n t s on P e r f e c t i o n
s u p e r i o r , m o r e g l o b a l o p t i m a . H i s s o m e w h a t m i s u n d e r s t o o d ( W r i g h t 1980) e m p h a s i s o n t h e r o l e o f g e n e t i c drift i n a l l o w i n g l i n e a g e s t o e s c a p e from the pull of local o p t i m a , and thereby attain a closer a p p r o x i m a t i o n to w h a t a h u m a n m i g h t r e c o g n i z e as 'the' o p t i m a l solution, contrasts interestingly with L e w o n t i n ' s ( 1 9 7 9 ) i n v o k i n g o f drift a s a n ' a l t e r n a t i v e t o a d a p t a t i o n ' . A s i n the case of pleiotropy, there is no p a r a d o x here. L e w o n t i n is right that 'the finiteness o f r e a l p o p u l a t i o n s results i n r a n d o m c h a n g e s i n g e n e f r e q u e n c y s o that, with a certain probability, genetic combinations with lower reproduct i v e fitness w i l l b e f i x e d i n a p o p u l a t i o n ' . B u t o n t h e o t h e r h a n d i t i s also t r u e that, to the extent that l o c a l o p t i m a constitute a limitation on the attainment o f d e s i g n p e r f e c t i o n , drift w i l l t e n d t o p r o v i d e a n e s c a p e
(Lande
1976).
I r o n i c a l l y , t h e n , a weakness in n a t u r a l s e l e c t i o n c a n t h e o r e t i c a l l y enhance t h e l i k e l i h o o d o f a l i n e a g e a t t a i n i n g o p t i m a l d e s i g n ! B e c a u s e i t h a s n o foresight, unalloyed
natural
selection
is
i n a sense a n
anti-perfection
mechanism,
h u g g i n g , a s i t w i l l , t h e tops o f t h e l o w f o o t - h i l l s o f W r i g h t ' s l a n d s c a p e . A m i x t u r e of strong selection interspersed w i t h periods of relaxation of selection a n d drift m a y b e t h e f o r m u l a for c r o s s i n g t h e v a l l e y s t o t h e h i g h u p l a n d s . C l e a r l y i f ' a d a p t a t i o n i s m ' i s t o b e c o m e a n issue w h e r e d e b a t i n g p o i n t s a r e s c o r e d , t h e r e i s s c o p e for b o t h sides t o h a v e i t b o t h w a y s ! M y o w n f e e l i n g i s t h a t s o m e w h e r e h e r e m a y lie t h e s o l u t i o n t o the r e a l p a r a d o x o f this s e c t i o n o n h i s t o r i c a l c o n s t r a i n t s . T h e j e t e n g i n e a n a l o g y suggested
that
animals
improvisation,
ought
to
be
risible
monstrosities
of lashed-up
t o p - h e a v y w i t h g r o t e s q u e relics o f p a t c h e d - o v e r a n t i q u i t y .
H o w c a n w e r e c o n c i l e this r e a s o n a b l e e x p e c t a t i o n w i t h t h e f o r m i d a b l e g r a c e o f t h e h u n t i n g c h e e t a h , t h e a e r o d y n a m i c b e a u t y o f t h e swift, t h e s c r u p u l o u s attention to d e c e p t i v e detail of the l e a f insect? E v e n m o r e impressive is the detailed
agreement
between
different
convergent
solutions
to
common
p r o b l e m s , for i n s t a n c e t h e m u l t i p l e p a r a l l e l s t h a t exist b e t w e e n t h e m a m m a l radiations o f A u s t r a l i a , S o u t h A m e r i c a and the O l d W o r l d . C a i n (1964) remarks that,
' U p to n o w it has usually been assumed, by D a r w i n and
others, that c o n v e r g e n c e will n e v e r be so g o o d as to mislead us' but he goes on to g i v e e x a m p l e s w h e r e c o m p e t e n t taxonomists h a v e been fooled. M o r e and more groups w h i c h had hitherto been regarded as decently monophyletic, are n o w b e i n g suspected of p o l y p h y l e t i c origin. T h e citation of e x a m p l e a n d c o u n t e r - e x a m p l e is m e r e idle fact-dropping. W h a t w e n e e d i s c o n s t r u c t i v e w o r k o n the relation b e t w e e n local a n d g l o b a l o p t i m a i n a n e v o l u t i o n a r y context. O u r understanding o f natural selection itself needs to be s u p p l e m e n t e d by a study of 'escapes from specialization' to use H a r d y ' s
(1954)
phrase. H a r d y himself was suggesting neoteny as an
e s c a p e f r o m s p e c i a l i z a t i o n , w h i l e i n this c h a p t e r , f o l l o w i n g W r i g h t , I h a v e e m p h a s i z e d drift i n this r o l e . M u l l e r i a n m i m i c r y i n b u t t e r f l i e s m a y p r o v e t o b e a useful c a s e - s t u d y h e r e . Turner
(1977)
remarks
that
'among
the
long-winged
butterflies
o f the
C o n s t r a i n t s on P e r f e c t i o n
tropical
American
pericopids)
rainforests
(ithomiids,
heliconids,
danaids,
41
pierids,
t h e r e a r e six d i s t i n c t w a r n i n g p a t t e r n s , a n d a l t h o u g h a l l t h e
w a r n i n g l y c o l o r e d s p e c i e s b e l o n g t o o n e o f these m i m i c r y " r i n g s " t h e r i n g s t h e m s e l v e s c o e x i s t i n the s a m e h a b i t a t s t h r o u g h m o s t o f t h e A m e r i c a n t r o p i c s and remain v e r y distinct. . . . O n c e the difference b e t w e e n t w o patterns is too great to be j u m p e d by a single mutation, c o n v e r g e n c e b e c o m e s virtually i m p o s s i b l e , a n d the m i m i c r y r i n g s w i l l c o e x i s t i n d e f i n i t e l y . ' T h i s i s o n e o f t h e o n l y cases w h e r e ' h i s t o r i c a l c o n s t r a i n t s ' m a y b e c l o s e t o b e i n g u n d e r s t o o d i n full g e n e t i c d e t a i l . I t m a y p r o v i d e a w o r t h w h i l e o p p o r t u n i t y a l s o for t h e s t u d y o f the g e n e t i c d e t a i l s o f ' v a l l e y - c r o s s i n g ' , w h i c h i n t h e p r e s e n t c a s e w o u l d consist i n t h e d e t a c h m e n t o f a t y p e o f b u t t e r f l y f r o m t h e o r b i t o f o n e m i m i c r y r i n g , a n d its e v e n t u a l ' c a p t u r e ' b y t h e ' p u l l ' o f a n o t h e r m i m i c r y r i n g . T h o u g h h e d o e s n o t i n v o k e drift a s a n e x p l a n a t i o n i n this c a s e , T u r n e r t a n t a l i z i n g l y i n d i c a t e s t h a t ' I n s o u t h e r n E u r o p e Amata phegea . . . h a s . . . captured
Zygenea
ephialtes f r o m t h e M u l l e r i a n m i m i c r y r i n g o f z y g a e n i d s ,
h o m o p t e r a n s , e t c . t o w h i c h i t still b e l o n g s o u t s i d e t h e r a n g e o f A . phegea i n n o r t h e r n E u r o p e . . .' At a more general theoretical level, L e w o n t i n (1978b) notes that 'there m a y often b e s e v e r a l a l t e r n a t i v e s t a b l e e q u i l i b r i u m s o f g e n e t i c c o m p o s i t i o n even w h e n the force of n a t u r a l selection r e m a i n s the s a m e . W h i c h of these a d a p t i v e peaks in the space of genetic c o m p o s i t i o n is e v e n t u a l l y r e a c h e d by a population
depends
entirely
on
chance
events
at
the
b e g i n n i n g of the
selective process . . . F o r e x a m p l e , the I n d i a n rhinoceros has one h o r n a n d the A f r i c a n r h i n o c e r o s h a s t w o .
H o r n s a r e a n a d a p t a t i o n for p r o t e c t i o n
against predators b u t it is not true that one h o r n is specifically a d a p t i v e under Indian conditions as opposed to two horns on the A f r i c a n plains. Beginning with
t w o s o m e w h a t different d e v e l o p m e n t a l systems,
the t w o
species r e s p o n d e d t o t h e s a m e s e l e c t i v e forces i n s l i g h t l y d i f f e r e n t w a y s . ' T h e point is basically a g o o d one, a l t h o u g h it is w o r t h a d d i n g that L e w o n t i n ' s uncharacteristically 'adaptationist' b l u n d e r a b o u t the functional significance o f r h i n o c e r o s h o r n s i s n o t t r i v i a l . I f h o r n s r e a l l y were a n a d a p t a t i o n a g a i n s t predators it w o u l d indeed be hard to i m a g i n e h o w a single horn c o u l d be m o r e useful a g a i n s t A s i a n p r e d a t o r s w h i l e t w o h o r n s w e r e o f m o r e h e l p a g a i n s t A f r i c a n p r e d a t o r s . H o w e v e r if, a s s e e m s m u c h m o r e l i k e l y , r h i n o c e r o s horns a r e a n a d a p t a t i o n for i n t r a s p e c i f i c c o m b a t a n d i n t i m i d a t i o n , i t c o u l d well be the case that a o n e - h o r n e d rhino w o u l d be at a d i s a d v a n t a g e in o n e c o n t i n e n t w h i l e a t w o - h o r n e d r h i n o w o u l d suffer i n t h e o t h e r . W h e n e v e r t h e n a m e o f the g a m e i s i n t i m i d a t i o n (or s e x u a l a t t r a c t i o n a s F i s h e r t a u g h t u s long a g o ) , m e r e c o n f o r m i t y to the m a j o r i t y style, w h a t e v e r that m a j o r i t y style m a y h a p p e n t o b e , c a n h a v e a d v a n t a g e s . T h e d e t a i l s o f a t h r e a t d i s p l a y and its a s s o c i a t e d o r g a n s m a y b e a r b i t r a r y ,
but woe betide any mutant
individual that departs from established custom ( M a y n a r d S m i t h & P a r k e r I976).
42
C o n s t r a i n t s on P e r f e c t i o n
Available genetic variation No m a t t e r h o w strong a potential selection pressure m a y be, no evolution w i l l r e s u l t u n l e s s t h e r e i s g e n e t i c v a r i a t i o n for i t t o w o r k o n . ' T h u s , a l t h o u g h I m i g h t a r g u e that the possession of w i n g s in a d d i t i o n to arms a n d legs m i g h t be a d v a n t a g e o u s to some vertebrates, none has ever e v o l v e d a third pair of appendages,
presumably
because
the
genetic
variation
has
never
been
a v a i l a b l e ' ( L e w o n t i n 1 9 7 9 ) . O n e c o u l d r e a s o n a b l y d i s s e n t f r o m this o p i n i o n . It m a y be that the o n l y reason pigs h a v e no w i n g s is that selection has never favoured their e v o l u t i o n . C e r t a i n l y we must be careful before we assume, on h u m a n - c e n t r e d c o m m o n - s e n s e g r o u n d s , t h a t i t w o u l d o b v i o u s l y b e h a n d y for a n y a n i m a l t o h a v e a p a i r o f w i n g s e v e n i f i t d i d n ' t use t h e m v e r y o f t e n , a n d that therefore the absence of wings in a g i v e n lineage must be due to lack of available mutations.
F e m a l e ants c a n sprout w i n g s if they h a p p e n to be
n u r t u r e d as q u e e n s , b u t if nurtured as workers they do not express their c a p a c i t y t o d o s o . M o r e s t r i k i n g l y , t h e q u e e n s i n m a n y s p e c i e s use t h e i r w i n g s o n l y o n c e , for t h e i r n u p t i a l f l i g h t , a n d t h e n t a k e t h e d r a s t i c s t e p o f b i t i n g o r breaking
them
off at
the
roots
in
p r e p a r a t i o n for
the
rest o f t h e i r life
u n d e r g r o u n d . E v i d e n t l y w i n g s h a v e costs a s w e l l a s b e n e f i t s . One
of the
most impressive demonstrations of the subtlety of Charles
D a r w i n ' s m i n d i s g i v e n b y his d i s c u s s i o n o f w i n g l e s s n e s s a n d t h e costs o f h a v i n g w i n g s in the insects of o c e a n i c islands. F o r present purposes, the r e l e v a n t p o i n t i s t h a t w i n g e d i n s e c t s m a y risk b e i n g b l o w n o u t t o s e a , a n d D a r w i n ( 1 8 5 9 , p . 1 7 7 ) s u g g e s t e d t h a t this i s w h y m a n y i s l a n d i n s e c t s h a v e r e d u c e d w i n g s . B u t h e a l s o n o t e d t h a t s o m e i s l a n d insects a r e far from wingless; they have extra large wings. T h i s is quite c o m p a t i b l e with the action of natural selection. For w h e n a n e w insect first arrived on the island, the t e n d e n c y of natural selection to e n l a r g e or to r e d u c e the w i n g s , w o u l d d e p e n d on w h e t h e r a g r e a t e r n u m b e r of i n d i v i d u a l s w e r e saved by successfully battling w i t h the w i n d s , or by g i v i n g up the a t t e m p t a n d rarely or never flying. As with mariners ship-wrecked near a coast, it w o u l d have b e e n b e t t e r for t h e g o o d s w i m m e r s i f t h e y h a d b e e n a b l e t o s w i m still f u r t h e r , w h e r e a s i t w o u l d h a v e b e e n b e t t e r for the b a d s w i m m e r s i f t h e y h a d not b e e n a b l e to s w i m at all a n d h a d stuck to the w r e c k .
A neater piece of evolutionary reasoning w o u l d be hard to find, although one c a n almost h e a r the b a y i n g chorus o f 'Unfalsifiable! T a u t o l o g i c a l ! Just-so story!' R e t u r n i n g to the question of w h e t h e r pigs ever could d e v e l o p wings, L e w o n t i n is u n d o u b t e d l y right that biologists interested in adaptation cannot afford t o i g n o r e t h e q u e s t i o n o f t h e a v a i l a b i l i t y o f m u t a t i o n a l v a r i a t i o n . I t i s c e r t a i n l y t r u e t h a t m a n y o f us, w i t h M a y n a r d S m i t h ( 1 9 7 8 a ) t h o u g h w i t h o u t
C o n s t r a i n t s on P e r f e c t i o n
43
his a n d L e w o n t i n ' s a u t h o r i t a t i v e k n o w l e d g e o f g e n e t i c s , t e n d t o a s s u m e ' t h a t genetic variance of an appropriate kind will usually exist'. M a y n a r d Smith's grounds are that 'with rare exceptions, artificial selection has a l w a y s p r o v e d effective, w h a t e v e r t h e o r g a n i s m o r t h e s e l e c t e d c h a r a c t e r ' . A n o t o r i o u s c a s e , fully c o n c e d e d b y M a y n a r d S m i t h
( 1 9 7 8 b ) , w h e r e the genetic variation
necessary to an o p t i m a l i t y theory often seems to be l a c k i n g , is that of Fisher's ( 1 9 3 0 a ) sex r a t i o t h e o r y . C a t t l e b r e e d e r s h a v e h a d n o t r o u b l e i n b r e e d i n g for high milk yield, high b e e f production, large size, small size, hornlessness, resistance t o v a r i o u s d i s e a s e s , a n d f i e r c e n e s s i n
fighting
bulls.
It w o u l d
obviously be of i m m e n s e benefit to the d a i r y industry if cattle c o u l d be b r e d with a bias t o w a r d s p r o d u c i n g heifer c a l v e s rather t h a n b u l l c a l v e s . A l l a t t e m p t s t o d o this h a v e s i n g u l a r l y f a i l e d , a p p a r e n t l y b e c a u s e t h e n e c e s s a r y genetic variation does not exist. It m a y be the m e a s u r e of h o w misled is my o w n biological intuition
that
I
find
this f a c t r a t h e r a s t o n i s h i n g ,
indeed
w o r r y i n g . I w o u l d like t o t h i n k t h a t i t i s a n e x c e p t i o n a l c a s e , b u t L e w o n t i n i s certainly right that we need to p a y m o r e attention to the p r o b l e m of the limitations
of available
genetic
variation.
From
this
point
of view,
a
compilation of the a m e n a b i l i t y or resistance to artificial selection of a w i d e variety of characters w o u l d be of g r e a t interest. Meanwhile,
there
are
certain
common-sense
things
that
can
be
said.
F i r s t l y , i t m a y m a k e sense t o i n v o k e l a c k o f a v a i l a b l e m u t a t i o n t o e x p l a i n w h y animals do not h a v e some adaptation w h i c h we think reasonable, but it is harder to a p p l y the a r g u m e n t the other w a y r o u n d . F o r instance, we m i g h t i n d e e d t h i n k t h a t p i g s w o u l d b e b e t t e r off w i t h w i n g s a n d s u g g e s t t h a t t h e y lack
them
only
because
their
ancestors
never
produced
the
necessary
m u t a t i o n s . B u t i f w e see a n a n i m a l w i t h a c o m p l e x o r g a n , o r a c o m p l e x a n d time-consuming behaviour pattern, we w o u l d seem to be on strong grounds in guessing that it must h a v e been put together by natural selection. H a b i t s such as d a n c i n g in bees as a l r e a d y discussed, ' a n t i n g ' in birds, ' r o c k i n g ' in stick insects, a n d e g g - s h e l l r e m o v a l i n g u l l s a r e p o s i t i v e l y t i m e - c o n s u m i n g , energy-consuming and
complex.
T h e working hypothesis that they must
h a v e a D a r w i n i a n survival v a l u e is o v e r w h e l m i n g l y strong. In a few cases it has p r o v e d p o s s i b l e t o f i n d o u t w h a t t h a t s u r v i v a l v a l u e i s ( T i n b e r g e n 1 9 6 3 ) . T h e second c o m m o n - s e n s e point is that the hypothesis of 'no a v a i l a b l e m u t a t i o n s ' loses s o m e o f its f o r c e i f a r e l a t e d s p e c i e s , o r t h e s a m e s p e c i e s i n o t h e r c o n t e x t s , h a s s h o w n itself c a p a b l e o f p r o d u c i n g t h e n e c e s s a r y v a r i a t i o n . I shall m e n t i o n b e l o w a c a s e w h e r e t h e k n o w n c a p a b i l i t i e s o f t h e d i g g e r w a s p Ammophila campestris w e r e u s e d t o i l l u m i n a t e t h e l a c k o f s i m i l a r c a p a b i l i t i e s i n t h e r e l a t e d s p e c i e s Sphex ichneumoneus.
A more subtle version
of t h e s a m e
argument c a n be applied within any one species. F o r instance, M a y n a r d Smith
(1977,
see a l s o D a l y
1979)
concludes
a paper with
an
up-beat
question: W h y d o m a l e m a m m a l s not l a c t a t e ? W e need n o t g o into the d e t a i l s o f w h y h e t h o u g h t t h e y o u g h t t o ; h e m a y h a v e b e e n w r o n g , his m o d e l
44
C o n s t r a i n t s on P e r f e c t i o n
m a y h a v e b e e n w r o n g l y set u p , a n d t h e r e a l a n s w e r t o his q u e s t i o n m a y b e t h a t i t w o u l d n o t p a y m a l e m a m m a l s t o l a c t a t e . T h e p o i n t h e r e i s t h a t this i s a slightly different kind o f question from ' W h y d o n ' t pigs h a v e w i n g s ? ' . W e k n o w t h a t m a l e m a m m a l s c o n t a i n t h e g e n e s n e c e s s a r y for l a c t a t i o n , b e c a u s e all the g e n e s in a f e m a l e m a m m a l h a v e passed t h r o u g h m a l e ancestors and m a y be h a n d e d on to m a l e descendants. G e n e t i c m a l e m a m m a l s treated with h o r m o n e s , i n d e e d , c a n d e v e l o p a s l a c t a t i n g f e m a l e s . T h i s a l l m a k e s i t less plausible that the reason m a l e m a m m a l s d o n ' t lactate is simply that they h a v e n ' t ' t h o u g h t of it' m u t a t i o n a l l y speaking. (Indeed, I bet I c o u l d breed a r a c e o f s p o n t a n e o u s l y l a c t a t i n g m a l e s b y s e l e c t i n g for i n c r e a s e d s e n s i t i v i t y t o progressively reduced dosages of injected hormone, an interesting practical a p p l i c a t i o n o f the B a l d w i n / W a d d i n g t o n Effect.) The
third
common-sense
point
is
that if the v a r i a t i o n
that
is
being
p o s t u l a t e d consists in a s i m p l e q u a n t i t a t i v e extension of a l r e a d y existing variation it is m o r e plausible than a radical qualitative innovation. It m a y be i m p l a u s i b l e to postulate a m u t a n t pig w i t h w i n g rudiments, but it is not i m p l a u s i b l e t o p o s t u l a t e a m u t a n t p i g w i t h a c u r l i e r tail t h a n e x i s t i n g p i g s . I h a v e e l a b o r a t e d this p o i n t e l s e w h e r e ( D a w k i n s 1 9 8 0 ) . I n a n y c a s e , w e n e e d a m o r e s u b t l e a p p r o a c h t o t h e q u e s t i o n o f w h a t i s the e v o l u t i o n a r y i m p a c t of differing degrees of m u t a b i l i t y . It is not g o o d e n o u g h to ask, in an all or n o n e w a y , w h e t h e r there is or is not genetic variation a v a i l a b l e to respond to a g i v e n selection pressure. As L e w o n t i n
(1979)
rightly says, ' N o t only is the qualitative possibility of adaptive evolution c o n s t r a i n e d b y a v a i l a b l e g e n e t i c v a r i a t i o n , b u t the relative rates o f evolution o f d i f f e r e n t c h a r a c t e r s a r e p r o p o r t i o n a l t o t h e a m o u n t o f g e n e t i c v a r i a n c e for e a c h . ' I t h i n k this o p e n s u p a n i m p o r t a n t l i n e o f t h o u g h t w h e n c o m b i n e d w i t h the n o t i o n of historical constraints treated in the previous section. T h e point c a n be illustrated w i t h a fanciful e x a m p l e . Birds fly w i t h w i n g s m a d e of feathers, bats w i t h w i n g s consisting of flaps of skin. W h y d o they not b o t h h a v e w i n g s m a d e i n the s a m e w a y , w h i c h e v e r w a y is ' s u p e r i o r ' ? A c o n f i r m e d adaptationist m i g h t reply that birds must be better off w i t h feathers a n d bats better off w i t h skin f l a p s . A n e x t r e m e antiadaptationist m i g h t say that v e r y p r o b a b l y feathers w o u l d a c t u a l l y be better t h a n s k i n - f l a p s for b o t h b i r d s a n d b a t s , b u t b a t s n e v e r h a d t h e g o o d f o r t u n e to p r o d u c e the right m u t a t i o n s . B u t there is an intermediate position, one w h i c h I find m o r e p e r s u a s i v e t h a n e i t h e r e x t r e m e . L e t u s c o n c e d e t o t h e a d a p t a t i o n i s t that, g i v e n e n o u g h time, the ancestors of bats p r o b a b l y could have produced
t h e s e q u e n c e o f m u t a t i o n s n e c e s s a r y for t h e m
to sprout
feathers. T h e o p e r a t i v e phrase i s ' g i v e n e n o u g h t i m e ' . W e are not m a k i n g a n all-or-none distinction ation,
but
simply
between impossible and
stating
the
undeniable
fact
possible mutational that
some
mutations
variare
q u a n t i t a t i v e l y m o r e p r o b a b l e t h a n o t h e r s . I n this c a s e , a n c e s t r a l m a m m a l s
C o n s t r a i n t s on P e r f e c t i o n
45
might have p r o d u c e d both mutants with r u d i m e n t a r y feathers and mutants w i t h r u d i m e n t a r y skin f l a p s . B u t t h e p r o t o - f e a t h e r m u t a n t s ( t h e y m i g h t h a v e had to go through an intermediate stage of small scales) w e r e so slow in m a k i n g their a p p e a r a n c e in c o m p a r i s o n w i t h the skin-flap m u t a n t s ,
that
skin-flap w i n g s h a d l o n g a g o a p p e a r e d a n d l e d t o t h e e v o l u t i o n o f p a s s a b l y efficient w i n g s . The
general
point
is
akin
to
the
one
already
made
about
adaptive
landscapes. T h e r e we were concerned with selection preventing lineages from e s c a p i n g t h e c l u t c h e s o f l o c a l o p t i m a . H e r e w e h a v e a l i n e a g e f a c e d w i t h t w o a l t e r n a t i v e r o u t e s o f e v o l u t i o n , o n e l e a d i n g to, s a y , f e a t h e r e d w i n g s , the o t h e r t o s k i n - f l a p w i n g s . T h e f e a t h e r e d d e s i g n m a y b e n o t o n l y a g l o b a l o p t i m u m b u t the p r e s e n t l o c a l o p t i m u m a s w e l l . T h e l i n e a g e , i n o t h e r w o r d s , m a y b e s i t t i n g e x a c t l y a t t h e foot o f t h e s l o p e l e a d i n g t o t h e f e a t h e r e d p e a k o f the S e w a l l W r i g h t l a n d s c a p e . I f o n l y t h e n e c e s s a r y m u t a t i o n s w e r e a v a i l a b l e it w o u l d c l i m b easily up the hill.
E v e n t u a l l y , a c c o r d i n g t o this f a n c i f u l
p a r a b l e , those m u t a t i o n s m i g h t h a v e c o m e , b u t — a n d this i s t h e i m p o r t a n t point—they w e r e too late. Skin-flap mutations h a d c o m e before t h e m , a n d the l i n e a g e h a d
already
a d a p t i v e hill
turn back.
to
climbed
t o o far u p
the slopes of the
skin-flap
As a river takes the line of least resistance
d o w n h i l l , t h e r e b y m e a n d e r i n g i n a r o u t e t h a t i s far f r o m t h e m o s t d i r e c t o n e t o the sea, s o a l i n e a g e w i l l e v o l v e a c c o r d i n g t o t h e effects o f s e l e c t i o n o n t h e variation available at a n y g i v e n m o m e n t . O n c e a lineage has b e g u n to e v o l v e in a given direction,
this m a y i n i t s e l f c l o s e o p t i o n s t h a t w e r e f o r m e r l y
a v a i l a b l e , s e a l i n g off a c c e s s t o a g l o b a l o p t i m u m . M y p o i n t i s t h a t l a c k o f available variation does not h a v e to
be absolute in order to b e c o m e a
significant constraint on perfection. It need o n l y be a q u a n t i t a t i v e b r a k e to h a v e d r a m a t i c q u a l i t a t i v e effects. I n spirit, t h e n , I a g r e e w i t h G o u l d a n d C a l l o w a y (1980) w h e n t h e y s a y , c i t i n g V e r m e i j ' s ( 1 9 7 3 ) s t i m u l a t i n g p a p e r o n the m a t h e m a t i c s o f m o r p h o l o g i c a l v e r s a t i l i t y t h a t , ' S o m e m o r p h o l o g i e s can be twisted, bent and altered in a variety of w a y s , a n d others c a n n o t . ' B u t I w o u l d p r e f e r to soften ' c a n n o t ' , to m a k e it a q u a n t i t a t i v e c o n s t r a i n t , n o t an absolute
barrier.
M c C l e e r y ( 1 9 7 8 ) , in an a g r e e a b l y c o m p r e h e n s i b l e i n t r o d u c t i o n to the M c F a r l a n d school of ethological optimality theory, mentions H. A. Simon's concept of 'satisficing' as an alternative to o p t i m i z i n g . If o p t i m i z i n g systems are c o n c e r n e d w i t h m a x i m i z i n g s o m e t h i n g , s a t i s f i c i n g s y s t e m s g e t a w a y w i t h d o i n g j u s t e n o u g h . I n this c a s e , d o i n g e n o u g h m e a n s d o i n g e n o u g h t o s t a y alive. M c C l e e r y contents himself with c o m p l a i n i n g that such ' a d e q u a c y ' concepts h a v e not g e n e r a t e d m u c h e x p e r i m e n t a l w o r k . I think e v o l u t i o n a r y t h e o r y e n t i t l e s us to be a b i t m o r e n e g a t i v e a priori. L i v i n g t h i n g s a r e n o t s e l e c t e d for t h e i r c a p a c i t y s i m p l y t o s t a y a l i v e ; t h e y a r e s t a y i n g a l i v e i n competition with other such living things. T h e trouble w i t h satisficing as a
46
C o n s t r a i n t s on P e r f e c t i o n
c o n c e p t is that it c o m p l e t e l y leaves out the c o m p e t i t i v e element w h i c h is f u n d a m e n t a l t o a l l life. I n G o r e V i d a l ' s w o r d s : ' I t i s n o t e n o u g h t o s u c c e e d . O t h e r s must fail.' On the other h a n d ' o p t i m i z i n g ' is also an unfortunate w o r d because it s u g g e s t s t h e a t t a i n m e n t o f w h a t a n e n g i n e e r w o u l d r e c o g n i z e a s t h e best design in a g l o b a l sense. It tends to o v e r l o o k the constraints on perfection w h i c h a r e t h e s u b j e c t o f this c h a p t e r . I n m a n y w a y s t h e w o r d ' m e l i o r i z i n g ' expresses a sensible m i d d l e w a y b e t w e e n o p t i m i z i n g a n d satisficing. W h e r e optimus m e a n s b e s t , melior m e a n s b e t t e r . T h e p o i n t s w e h a v e b e e n c o n s i d e r i n g a b o u t historical constraints, about Wright's adaptive landscapes and about r i v e r s f o l l o w i n g t h e l i n e o f i m m e d i a t e least r e s i s t a n c e , a r e all r e l a t e d t o the fact that n a t u r a l selection chooses the better of present a v a i l a b l e alternatives. N a t u r e does not h a v e the foresight to put together a sequence of mutations w h i c h , for a l l t h a t t h e y m a y e n t a i l t e m p o r a r y d i s a d v a n t a g e , set a l i n e a g e o n the r o a d to u l t i m a t e g l o b a l superiority. slightly
It c a n n o t refrain from favouring
advantageous
available
mutations
a d v a n t a g e of superior
mutations
which
natural
selection
blindly
meliorizes
its
now,
may way
so
arrive down
as later.
to
take
Like
successive
better
a river, lines
of
i m m e d i a t e l y a v a i l a b l e l e a s t r e s i s t a n c e . T h e a n i m a l t h a t results i s n o t the most perfect design c o n c e i v a b l e , nor is it merely good e n o u g h to scrape by. It is
the
product of a historical sequence of changes,
each
one of which
r e p r e s e n t e d , a t b e s t , t h e better o f t h e a l t e r n a t i v e s t h a t h a p p e n e d t o b e a r o u n d at the time.
Constraints of costs and materials ' I f t h e r e w e r e n o c o n s t r a i n t s o n w h a t i s p o s s i b l e , t h e best p h e n o t y p e w o u l d l i v e for e v e r , w o u l d b e i m p r e g n a b l e t o p r e d a t o r s , w o u l d l a y e g g s a t a n infinite r a t e , a n d s o o n ' ( M a y n a r d S m i t h 1 9 7 8 b ) . ' A n e n g i n e e r , g i v e n c a r t e b l a n c h e o n his d r a w i n g b o a r d c o u l d d e s i g n a n " i d e a l " w i n g for a b i r d , b u t he w o u l d d e m a n d to k n o w the constraints under w h i c h he must work. Is he constrained to use feathers a n d bones, or m a y he design the skeleton in titanium a l l o y ? H o w m u c h is he a l l o w e d to spend on the w i n g s , a n d h o w m u c h of the a v a i l a b l e e c o n o m i c investment must be diverted into, say, e g g p r o d u c t i o n ? ' ( D a w k i n s & B r o c k m a n n 1980). In practice, an engineer will normally be g i v e n a specification of m i n i m u m performance such as ' T h e b r i d g e m u s t b e a r a l o a d o f t e n tons . . . T h e a e r o p l a n e w i n g m u s t n o t b r e a k u n t i l i t r e c e i v e s a stress t h r e e t i m e s w h a t w o u l d b e e x p e c t e d i n w o r s t - c a s e turbulent conditions; n o w go ahead and build it as cheaply as you can.' T h e b e s t d e s i g n i s t h e o n e t h a t satisfies ('satisfices') t h e c r i t e r i o n s p e c i f i c a t i o n a t the least cost. A n y design that a c h i e v e s 'better' than the specified criterion performance is likely to be rejected, because p r e s u m a b l y the criterion could be achieved more cheaply. T h e particular criterion specification is an arbitrary w o r k i n g rule. T h e r e is
C o n s t r a i n t s on P e r f e c t i o n
47
n o t h i n g m a g i c a b o u t a safety m a r g i n o f t h r e e t i m e s t h e e x p e c t e d w o r s t - c a s e conditions. M i l i t a r y aircraft m a y be designed w i t h m o r e risky safety m a r g i n s t h a n c i v i l i a n o n e s . I n effect, t h e e n g i n e e r ' s o p t i m i z a t i o n i n s t r u c t i o n s a m o u n t to a m o n e t a r y e v a l u a t i o n of h u m a n safety, speed, c o n v e n i e n c e , p o l l u t i o n of the a t m o s p h e r e , e t c . T h e p r i c e p u t o n e a c h o f t h e s e i s a m a t t e r o f j u d g e m e n t , a n d is often a m a t t e r of c o n t r o v e r s y . I n the e v o l u t i o n a r y d e s i g n o f a n i m a l s a n d p l a n t s , j u d g e m e n t d o e s n o t e n t e r i n t o it, n o r d o e s c o n t r o v e r s y e x c e p t a m o n g t h e h u m a n s p e c t a t o r s o f t h e show. In some w a y , h o w e v e r , natural selection must p r o v i d e the e q u i v a l e n t of such j u d g e m e n t :
risks o f p r e d a t i o n m u s t b e e v a l u a t e d a g a i n s t risks o f
starving and benefits of m a t i n g w i t h an e x t r a f e m a l e . F o r a b i r d , resources s p e n t o n m a k i n g b r e a s t m u s c l e s for p o w e r i n g w i n g s a r e r e s o u r c e s t h a t c o u l d h a v e b e e n s p e n t o n m a k i n g e g g s . A n e n l a r g e d b r a i n w o u l d p e r m i t a finer tuning of b e h a v i o u r to e n v i r o n m e n t a l details, past a n d present, b u t at a cost of an enlarged h e a d , w h i c h m e a n s extra w e i g h t at the front e n d of the b o d y , w h i c h i n t u r n n e c e s s i t a t e s a l a r g e r tail for a e r o d y n a m i c s t a b i l i t y , w h i c h i n t u r n . . . W i n g e d a p h i d s a r e less f e c u n d t h a n w i n g l e s s o n e s o f t h e s a m e s p e c i e s (J.
S.
Kennedy,
personal
communication).
That
every
evolutionary
a d a p t a t i o n m u s t c o s t s o m e t h i n g , costs b e i n g m e a s u r e d i n lost o p p o r t u n i t i e s to do other things, is as true as that g e m of traditional e c o n o m i c w i s d o m , ' T h e r e is no s u c h t h i n g as a free l u n c h ' . Of
course
the
mathematics
of
biological
currency-conversion,
of
e v a l u a t i n g t h e costs o f w i n g m u s c l e , s i n g i n g t i m e , p r e d a t o r - v i g i l a n c e t i m e , etc., i n s o m e c o m m o n c u r r e n c y s u c h a s ' g o n a d e q u i v a l e n t s ' , a r e l i k e l y t o b e v e r y c o m p l e x . W h e r e a s t h e e n g i n e e r i s a l l o w e d t o s i m p l i f y his m a t h e m a t i c s by working to an arbitrarily chosen m i n i m u m threshold of performance, the biologist is granted no such l u x u r y . O u r s y m p a t h y and a d m i r a t i o n must go out to
t h o s e few
biologists
who
have attempted
to
grapple
with
these
problems in detail (e.g. Oster & Wilson 1 9 7 8 ; M c F a r l a n d & H o u s t o n 1 9 8 1 ) . O n the o t h e r h a n d , a l t h o u g h t h e m a t h e m a t i c s m a y b e f o r m i d a b l e , w e d o n ' t need m a t h e m a t i c s to d e d u c e the most i m p o r t a n t point, w h i c h is that a n y v i e w o f b i o l o g i c a l o p t i m i z a t i o n that denies the existence o f costs a n d trade-offs i s d o o m e d . A n a d a p t a t i o n i s t w h o l o o k s a t o n e a s p e c t o f a n a n i m a l ' s b o d y o r b e h a v i o u r , s a y t h e a e r o d y n a m i c p e r f o r m a n c e o f its w i n g s , w h i l e forgetting that efficiency in the w i n g s c a n o n l y be b o u g h t at a cost w h i c h w i l l b e felt s o m e w h e r e else i n t h e a n i m a l ' s e c o n o m y , w o u l d d e s e r v e a l l t h e c r i t i c i s m h e g e t s . I t h a s t o b e a d m i t t e d t h a t t o o m a n y o f us, w h i l e n e v e r a c t u a l l y d e n y i n g t h e i m p o r t a n c e o f costs, f o r g e t t o m e n t i o n t h e m , p e r h a p s even forget to think a b o u t them, w h e n we discuss b i o l o g i c a l function. T h i s has p r o b a b l y p r o v o k e d s o m e o f t h e c r i t i c i s m t h a t h a s c o m e o u r w a y . I n a n earlier section I q u o t e d Pittendrigh's remark that a d a p t i v e o r g a n i z a t i o n w a s a ' p a t c h w o r k of makeshifts'. We must also not forget that it is a t a n g l e of compromises (Tinbergen 1965).
48
C o n s t r a i n t s on P e r f e c t i o n
I n p r i n c i p l e , i t w o u l d s e e m a v a l u a b l e h e u r i s t i c p r o c e d u r e t o assume t h a t a n a n i m a l i s o p t i m i z i n g s o m e t h i n g u n d e r a g i v e n set o f c o n s t r a i n t s , a n d t o try to w o r k out w h a t those constraints are. T h i s is a restricted version of w h a t M c F a r l a n d a n d his c o l l e a g u e s c a l l t h e ' r e v e r s e o p t i m a l i t y ' a p p r o a c h ( e . g . M c C l e e r y 1 9 7 8 ) . As a case study I shall take some w o r k with w h i c h I happen to be familiar. Dawkins
and
Brockmann
(1980)
found
that
the
digger
wasps
(Sphex
ichneumoneus) s t u d i e d b y B r o c k m a n n b e h a v e d i n a w a y t h a t a n a i v e h u m a n economist might have criticized as maladaptive. Individual wasps appeared to c o m m i t the ' C o n c o r d e F a l l a c y ' of v a l u i n g a resource a c c o r d i n g to how m u c h t h e y h a d a l r e a d y s p e n t o n it, r a t h e r t h a n a c c o r d i n g t o h o w m u c h t h e y c o u l d get out of it in the future. V e r y briefly, the e v i d e n c e is as follows. Solitary females provision burrows with stung and paralysed katydids which a r e t o s e r v e a s f o o d for t h e i r l a r v a e (see C h a p t e r 7 ) . O c c a s i o n a l l y t w o f e m a l e s find
themselves provisioning the same burrow,
and
they usually end
up
f i g h t i n g o v e r it. E a c h f i g h t g o e s o n u n t i l o n e w a s p , t h e r e b y d e f i n e d a s t h e loser, flees f r o m t h e a r e a , l e a v i n g t h e w i n n e r i n c o n t r o l o f t h e b u r r o w a n d a l l the k a t y d i d s c a u g h t by b o t h w a s p s . We m e a s u r e d the 'real v a l u e ' of a b u r r o w as the n u m b e r of katydids w h i c h it contained. T h e 'prior investment' by each w a s p i n t h e b u r r o w w a s m e a s u r e d a s t h e n u m b e r o f k a t y d i d s w h i c h she, a s a n i n d i v i d u a l , h a d p u t i n t o it. T h e e v i d e n c e s u g g e s t e d t h a t e a c h w a s p f o u g h t for a t i m e p r o p o r t i o n a l t o h e r o w n i n v e s t m e n t , r a t h e r t h a n p r o p o r t i o n a l t o the 'true v a l u e ' of the burrow. S u c h a p o l i c y has great h u m a n p s y c h o l o g i c a l a p p e a l . We too tend to fight t e n a c i o u s l y for p r o p e r t y w h i c h w e h a v e p u t g r e a t effort i n t o a c q u i r i n g . T h e f a l l a c y g e t s its n a m e f r o m t h e fact t h a t , a t a t i m e w h e n s o b e r e c o n o m i c j u d g e m e n t o f future prospects counselled a b a n d o n i n g the d e v e l o p i n g o f the C o n c o r d e a i r l i n e r , o n e o f t h e a r g u m e n t s i n f a v o u r o f c o n t i n u i n g w i t h the h a l f c o m p l e t e d project w a s retrospective: ' W e h a v e already spent so m u c h on it t h a t w e c a n n o t b a c k o u t n o w . ' A p o p u l a r a r g u m e n t for p r o l o n g i n g w a r s g a v e rise t o t h e o t h e r n a m e for t h e f a l l a c y , t h e ' O u r b o y s shall n o t h a v e d i e d i n vain' fallacy. W h e n D r B r o c k m a n n a n d I first r e a l i z e d t h a t d i g g e r w a s p s b e h a v e d i n like m a n n e r , I w a s , i t h a s t o b e c o n f e s s e d , a little d i s c o n c e r t e d , p o s s i b l y b e c a u s e o f m y o w n p a s t i n v e s t m e n t o f effort ( D a w k i n s & C a r l i s l e 1976a)
in
persuading
my
colleagues
that
1976; Dawkins
the p s y c h o l o g i c a l l y
appealing
C o n c o r d e F a l l a c y w a s , indeed, a fallacy! B u t then we started to think more seriously a b o u t cost constraints.
Could
it be
that w h a t appeared
to be
m a l a d a p t i v e w a s b e t t e r i n t e r p r e t e d as an o p t i m u m , given certain constraints? The
question
then
became:
Is
there
a
constraint
such
that
the
wasps'
C o n c o r d i a n b e h a v i o u r is the best they c a n a c h i e v e u n d e r it? In fact the q u e s t i o n w a s m o r e c o m p l i c a t e d necessary to substitute
M a y n a r d Smith's
than
(1974)
that,
because it was
concept of evolutionary
C o n s t r a i n t s on P e r f e c t i o n
stability
('ESS'—see Chapter
7)
49
for t h a t o f s i m p l e o p t i m a l i t y ,
but the
principle remains that a reverse optimality a p p r o a c h m i g h t be heuristically valuable. If we c a n show that an animal's b e h a v i o u r is w h a t w o u l d be produced by an optimizing system w o r k i n g under constraint X, m a y b e we c a n use t h e a p p r o a c h t o l e a r n s o m e t h i n g o f t h e c o n s t r a i n t s u n d e r w h i c h animals actually do work. In the present case it s e e m e d that the r e l e v a n t constraint m i g h t be o n e of s e n s o r y c a p a c i t y . I f the w a s p s , for s o m e r e a s o n , c a n n o t c o u n t k a t y d i d s i n t h e b u r r o w , b u t c a n m e t r e s o m e a s p e c t o f t h e i r o w n h u n t i n g efforts, t h e r e i s a n asymmetry
of information
possessed
by
the
two
combatants.
Each
one
' k n o w s ' that the b u r r o w contains at least b k a t y d i d s , w h e r e b is the n u m b e r she h e r s e l f h a s c a u g h t .
She m a y 'estimate' that the true n u m b e r in the
b u r r o w is larger t h a n b, b u t she does not k n o w h o w m u c h l a r g e r . U n d e r s u c h conditions Grafen
(in p r e p a r a t i o n )
has shown that the expected
E S S is
a p p r o x i m a t e l y the one originally c a l c u l a t e d b y B i s h o p a n d C a n n i n g s (1978) for the s o - c a l l e d ' g e n e r a l i z e d w a r o f a t t r i t i o n ' . T h e m a t h e m a t i c a l d e t a i l s c a n be
left
aside;
for p r e s e n t
purposes w h a t
matters
is
that
the
behaviour
expected b y the e x t e n d e d w a r o f attrition m o d e l w o u l d look v e r y like the C o n c o r d i a n b e h a v i o u r actually s h o w n by the wasps. If we
were
interested
in
testing
the
general
hypothesis
that
animals
o p t i m i z e , this k i n d of post hoc r a t i o n a l i z a t i o n w o u l d be s u s p e c t . By post hoc m o d i f i c a t i o n o f t h e d e t a i l s o f t h e h y p o t h e s i s , o n e i s b o u n d t o find a v e r s i o n w h i c h fits t h e facts. M a y n a r d S m i t h ' s ( 1 9 7 8 b ) r e p l y t o this k i n d o f c r i t i c i s m i s very
relevant:
proposition
'...in
that
testing
nature
a
model
optimizes,
we
but
are
the
not
testing
specific
the
general
hypotheses
about
constraints, o p t i m i z a t i o n criteria, a n d heredity'. In the present case we are making a general assumption that nature does o p t i m i z e within constraints, and testing p a r t i c u l a r m o d e l s o f w h a t those constraints m i g h t b e . T h e particular constraint suggested—inability of the w a s p ' s sensory system t o assess t h e
contents of a
b u r r o w — i s in
accordance
with
independent
e v i d e n c e from the s a m e p o p u l a t i o n of w a s p s ( B r o c k m a n n , G r a f e n & D a w k i n s 1 9 7 9 ; B r o c k m a n n & D a w k i n s 1979). T h e r e is no reason to regard it as an i r r e v o c a b l y b i n d i n g l i m i t a t i o n for a l l t i m e . P r o b a b l y t h e w a s p s c o u l d e v o l v e the c a p a c i t y t o assess nest c o n t e n t s , b u t o n l y a t a c o s t . D i g g e r w a s p s o f t h e related
species
Ammophila
campestris
have
long
been
known
to
make
an
assessment o f t h e c o n t e n t s o f e a c h o f t h e i r nests e v e r y d a y ( B a e r e n d s 1 9 4 1 ) . U n l i k e Sphex, w h i c h p r o v i s i o n s o n e b u r r o w a t a t i m e , l a y s a n e g g , t h e n fills the b u r r o w i n w i t h soil a n d l e a v e s t h e l a r v a t o e a t t h e p r o v i s i o n o n its o w n , Ammophila
campestris
is
a
progressive
provisioner
of
several
burrows
concurrently. A female tends t w o or three g r o w i n g larvae, e a c h in a separate burrow, at the same time. T h e ages of her various l a r v a e are s t a g g e r e d , a n d t h e i r food
needs
are
different.
Every
m o r n i n g she
assesses
the
current
contents of each b u r r o w on a special early m o r n i n g 'inspection r o u n d ' . By
50
C o n s t r a i n t s on P e r f e c t i o n
e x p e r i m e n t a l l y c h a n g i n g t h e c o n t e n t s o f b u r r o w s , B a e r e n d s s h o w e d t h a t the female adjusts her w h o l e d a y ' s p r o v i s i o n i n g o f e a c h b u r r o w a c c o r d i n g t o w h a t i t c o n t a i n e d a t t h e t i m e o f h e r m o r n i n g i n s p e c t i o n . T h e c o n t e n t s o f the b u r r o w a t a n y o t h e r t i m e o f d a y h a v e n o effect o n h e r b e h a v i o u r , e v e n t h o u g h s h e i s p r o v i s i o n i n g i t a l l d a y . S h e a p p e a r s , t h e r e f o r e , t o use h e r a s s e s s m e n t f a c u l t y s p a r i n g l y , s w i t c h i n g i t off for t h e rest o f t h e d a y after the morning inspection, instrument.
almost as t h o u g h it w a s a costly,
power-consuming
F a n c i f u l a s t h a t a n a l o g y m a y b e , i t s u r e l y s u g g e s t s t h a t the
a s s e s s m e n t f a c u l t y , w h a t e v e r i t is, m a y h a v e o v e r h e a d r u n n i n g costs, e v e n i f ( G . P. B a e r e n d s , personal c o m m u n i c a t i o n ) these consist o n l y in the time consumed. Sphex ichneumoneus, n o t b e i n g a p r o g r e s s i v e p r o v i s i o n e r , a n d t e n d i n g o n l y o n e b u r r o w at a t i m e , p r e s u m a b l y h a s less n e e d t h a n Ammophila for a b u r r o w assessment faculty. By not a t t e m p t i n g to count prey in the b u r r o w , it c a n s a v e i t s e l f n o t o n l y t h e r u n n i n g e x p e n d i t u r e t h a t Ammophila s e e m s s o c a r e f u l to ration;
it
can
also
save
itself the
initial
m a n u f a c t u r i n g costs o f the
necessary neural a n d sensory a p p a r a t u s . P r o b a b l y it c o u l d benefit slightly from
having
an
ability
to
assess
burrow
contents,
but
only
on
the
c o m p a r a t i v e l y r a r e o c c a s i o n s w h e n i t f i n d s i t s e l f c o m p e t i n g for a b u r r o w w i t h a n o t h e r w a s p . I t i s e a s y t o b e l i e v e t h a t t h e costs o u t w e i g h t h e b e n e f i t s , a n d that
selection
has
therefore
never
favoured
the
evolution
o f assessment
a p p a r a t u s . I t h i n k this is a m o r e c o n s t r u c t i v e a n d i n t e r e s t i n g h y p o t h e s i s t h a n t h e a l t e r n a t i v e h y p o t h e s i s t h a t t h e n e c e s s a r y m u t a t i o n a l v a r i a t i o n has n e v e r a r i s e n . O f c o u r s e w e h a v e t o a d m i t t h a t the l a t t e r m i g h t b e r i g h t , b u t I w o u l d p r e f e r t o k e e p i t a s a h y p o t h e s i s o f last resort.
Imperfections at one level due to selection at another level O n e o f t h e m a i n t o p i c s t o b e t a c k l e d i n this b o o k i s t h a t o f t h e l e v e l a t w h i c h n a t u r a l s e l e c t i o n a c t s . T h e k i n d o f a d a p t a t i o n s w e s h o u l d see i f s e l e c t i o n a c t e d a t t h e l e v e l o f t h e g r o u p w o u l d b e q u i t e different f r o m t h e a d a p t a t i o n s w e s h o u l d e x p e c t i f s e l e c t i o n a c t s a t t h e l e v e l o f the i n d i v i d u a l . I t f o l l o w s t h a t a g r o u p s e l e c t i o n i s t m i g h t w e l l see a s i m p e r f e c t i o n s ,
features w h i c h
an
i n d i v i d u a l s e l e c t i o n i s t w o u l d see a s a d a p t a t i o n s . T h i s i s the m a i n r e a s o n w h y I
regard
as
adaptationism
unfair with
Gould the
and
naive
Lewontin's perfectionism
(1979) that
equating Haldane
of modern
named
after
V o l t a i r e ' s D r Pangloss. W i t h reservations d u e t o the various constraints o n p e r f e c t i o n , a n a d a p t a t i o n i s t m a y b e l i e v e t h a t all a s p e c t s o f o r g a n i s m s a r e ' a d a p t i v e o p t i m a l s o l u t i o n s t o p r o b l e m s ' , o r t h a t 'it i s v i r t u a l l y i m p o s s i b l e t o d o a b e t t e r j o b t h a n a n o r g a n i s m i s d o i n g i n its g i v e n e n v i r o n m e n t ' . Y e t the s a m e a d a p t a t i o n i s t m a y b e e x t r e m e l y fussy a b o u t t h e k i n d o f m e a n i n g h e allows
to
adaptive,
words indeed
like
'optimal'
Panglossian,
and
'better'.
explanations,
There for
are
many
example
most
kinds
of
group-
C o n s t r a i n t s on P e r f e c t i o n
selectionist
ones,
which
would
be
utterly
ruled
out
by
the
51
modern
adaptationist. F o r the Panglossian the d e m o n s t r a t i o n that s o m e t h i n g is ' b e n e f i c i a l '
(to
w h o m or to w h a t is often n o t s p e c i f i e d ) is a sufficient e x p l a n a t i o n for its e x i s t e n c e . T h e n e o - D a r w i n i a n a d a p t a t i o n i s t , o n t h e o t h e r h a n d , insists u p o n k n o w i n g the e x a c t nature of the selective process that has led to the e v o l u t i o n of the p u t a t i v e a d a p t a t i o n .
In particular,
h e insists o n p r e c i s e l a n g u a g e
a b o u t the l e v e l a t w h i c h n a t u r a l s e l e c t i o n i s s u p p o s e d t o h a v e a c t e d . T h e P a n g l o s s i a n l o o k s a t a o n e - t o - o n e s e x r a t i o a n d sees t h a t i t i s g o o d : d o e s i t n o t m i n i m i z e the w a s t a g e o f the p o p u l a t i o n ' s resources? T h e n e o - D a r w i n i a n a d a p t a t i o n i s t c o n s i d e r s i n d e t a i l t h e fates o f g e n e s a c t i n g o n p a r e n t s t o b i a s the sex r a t i o o f t h e i r o f f s p r i n g , a n d c a l c u l a t e s t h e e v o l u t i o n a r i l y s t a b l e s t a t e of the p o p u l a t i o n (Fisher 1 9 3 0 a ) . T h e Panglossian is d i s c o n c e r t e d by 1:1 sex ratios i n p o l y g y n o u s s p e c i e s , i n w h i c h a m i n o r i t y o f m a l e s h o l d h a r e m s a n d the rest sit a b o u t i n b a c h e l o r h e r d s c o n s u m i n g a l m o s t h a l f t h e p o p u l a t i o n ' s food r e s o u r c e s y e t c o n t r i b u t i n g n o t a t a l l t o t h e p o p u l a t i o n ' s r e p r o d u c t i o n . T h e n e o - D a r w i n i a n a d a p t a t i o n i s t t a k e s this i n his s t r i d e . T h e s y s t e m m a y b e hideously u n e c o n o m i c a l from the p o p u l a t i o n ' s point of v i e w , but, from the point of v i e w of the genes influencing the trait c o n c e r n e d , there is no m u t a n t that c o u l d do better. My point is that n e o - D a r w i n i a n a d a p t a t i o n i s m is not a c a t c h - a l l , b l a n k e t f a i t h i n a l l b e i n g for t h e b e s t . I t r u l e s o u t o f c o u r t m o s t o f the a d a p t i v e e x p l a n a t i o n s t h a t r e a d i l y o c c u r t o t h e P a n g l o s s i a n . S o m e years a g o , a c o l l e a g u e received an a p p l i c a t i o n from a p r o s p e c t i v e graduate student wishing to w o r k on adaptation, w h o was b r o u g h t up a religious fundamentalist a n d did not believe in e v o l u t i o n . He b e l i e v e d in adaptations,
but
thought
they were designed
by G o d ,
designed
for t h e
benefit o f . . . a h , b u t t h a t i s j u s t t h e p r o b l e m ! I t m i g h t b e t h o u g h t t h a t i t d i d not matter w h e t h e r the student
believed
adaptations
were
produced
by
natural selection or by G o d . A d a p t a t i o n s are 'beneficial' w h e t h e r because of natural
selection
or
because
of
beneficient
design,
and
could
not
a
fundamentalist student be usefully e m p l o y e d in u n c o v e r i n g the detailed w a y s i n w h i c h t h e y w e r e b e n e f i c i a l ? M y p o i n t i s t h a t this a r g u m e n t w i l l n o t d o , b e c a u s e w h a t i s b e n e f i c i a l t o o n e e n t i t y i n t h e h i e r a r c h y o f life i s h a r m f u l t o a n o t h e r , a n d c r e a t i o n i s m g i v e s u s n o g r o u n d s for s u p p o s i n g t h a t o n e e n t i t y ' s welfare will be preferred to another's. In passing, the fundamentalist student might pause to w o n d e r at a G o d w h o goes to great trouble to provide predators with beautiful adaptations to c a t c h prey, w h i l e w i t h the other hand g i v i n g prey beautiful adaptations to thwart them. P e r h a p s He enjoys the
spectator
sport.
Returning
to
the
main
point,
if adaptations
were
designed by G o d , He might h a v e designed them to benefit the i n d i v i d u a l a n i m a l (its s u r v i v a l o r — n o t t h e s a m e t h i n g — i t s i n c l u s i v e f i t n e s s ) , t h e s p e c i e s , some
other
species
such
as
mankind
(the
usual
view
of
religious
fundamentalists), the ' b a l a n c e of nature', or s o m e o t h e r i n s c r u t a b l e purpose
52
C o n s t r a i n t s on Perfection
k n o w n only to H i m . T h e s e are frequently incompatible alternatives. It really matters for w h o s e b e n e f i t a d a p t a t i o n s a r e d e s i g n e d . F a c t s s u c h a s t h e sex r a t i o in
harem-forming
mammals
are
inexplicable
on
certain
hypotheses
and
easily e x p l i c a b l e o n others. T h e adaptationist w o r k i n g w i t h i n the f r a m e w o r k of a
proper
understanding
of the
genetical
theory
of natural
selection
c o u n t e n a n c e s o n l y a v e r y r e s t r i c t e d set o f t h e p o s s i b l e f u n c t i o n a l h y p o t h e s e s w h i c h the Panglossian m i g h t admit. O n e o f t h e m a i n m e s s a g e s o f this b o o k i s t h a t , for m a n y p u r p o s e s , i t i s better to r e g a r d the level at w h i c h selection acts as neither the organism, nor the g r o u p or a n y larger unit, but the gene or small genetic fragment. T h i s difficult t o p i c w i l l b e d e b a t e d i n l a t e r c h a p t e r s . F o r the p r e s e n t , i t i s sufficient t o n o t e t h a t s e l e c t i o n a t t h e l e v e l o f t h e g e n e c a n g i v e rise t o a p p a r e n t i m p e r f e c t i o n s a t t h e l e v e l o f t h e i n d i v i d u a l . I s h a l l discuss ' m e i o t i c d r i v e ' a n d r e l a t e d p h e n o m e n a i n C h a p t e r 8 , b u t t h e classic e x a m p l e i s t h e c a s e o f h e t e r o z y g o u s a d v a n t a g e . A g e n e m a y b e p o s i t i v e l y s e l e c t e d b e c a u s e o f its b e n e f i c i a l effects w h e n h e t e r o z y g o u s , e v e n t h o u g h i t has h a r m f u l effects w h e n homozygous.
As
a
c o n s e q u e n c e o f this,
a predictable
p r o p o r t i o n o f the
individual organisms in the p o p u l a t i o n will h a v e defects. T h e general point i s this. T h e g e n o m e o f a n i n d i v i d u a l o r g a n i s m i n a s e x u a l p o p u l a t i o n i s t h e p r o d u c t o f a m o r e o r less r a n d o m s h u f f l i n g o f t h e g e n e s i n t h e p o p u l a t i o n . G e n e s a r e s e l e c t e d o v e r t h e i r a l l e l e s b e c a u s e o f t h e i r p h e n o t y p i c effects, a v e r a g e d o v e r all the i n d i v i d u a l bodies in w h i c h they are distributed, over the w h o l e population,
a n d t h r o u g h m a n y g e n e r a t i o n s . T h e effects t h a t a
g i v e n g e n e h a s w i l l u s u a l l y d e p e n d u p o n t h e o t h e r g e n e s w i t h w h i c h i t shares a body:
h e t e r o z y g o u s a d v a n t a g e is j u s t a s p e c i a l c a s e of this. A c e r t a i n
proportion of bad bodies seems an almost inevitable c o n s e q u e n c e of selection for g o o d g e n e s ,
w h e r e g o o d refers t o t h e a v e r a g e effects o f a g e n e o n a
s t a t i s t i c a l s a m p l e o f b o d i e s i n w h i c h i t f i n d s itself p e r m u t e d w i t h o t h e r g e n e s . I n e v i t a b l e , t h a t is, a s l o n g a s w e a c c e p t t h e M e n d e l i a n shuffle a s g i v e n a n d inescapable. adaptive
Williams
fine-adjustment
(1979),
disappointed
at
finding
no
evidence
for
of the sex ratio, m a k e s the p e r c e p t i v e point that
S e x is o n l y one of m a n y offspring characters that w o u l d seem a d a p t i v e for a p a r e n t t o c o n t r o l . F o r i n s t a n c e , i n h u m a n p o p u l a t i o n s affected b y s i c k l e - c e l l a n a e m i a , i t w o u l d b e a d v a n t a g e o u s for a h e t e r o z y g o u s w o m a n to h a v e her A eggs fertilized only by a-bearing sperm, and v i c e versa, or e v e n to a b o r t all h o m o z y g o u s e m b r y o s . Y e t if m a t e d to another
heterozygote
she
will
reliably
submit
to
the
Mendelian
l o t t e r y , e v e n t h o u g h this m e a n s m a r k e d l y l o w e r e d fitness for h a l f h e r children . .. T h e really fundamental questions in evolution m a y be a n s w e r a b l e only by r e g a r d i n g each gene as ultimately in conflict with e v e r y other g e n e , e v e n those at other loci in the s a m e cell. A really
C o n s t r a i n t s on P e r f e c t i o n
53
v a l i d t h e o r y o f n a t u r a l s e l e c t i o n m u s t b e b a s e d u l t i m a t e l y o n selfish replicators,
genes
and
all
other
entities
capable
of
the
biased
a c c u m u l a t i o n o f different v a r i a n t f o r m s . Amen!
Mistakes due to environmental unpredictability or 'malevolence' H o w e v e r well a d a p t e d a n a n i m a l m a y b e t o e n v i r o n m e n t a l c o n d i t i o n s , those conditions must be r e g a r d e d as a statistical a v e r a g e .
It will usually
be
i m p o s s i b l e t o c a t e r for e v e r y c o n c e i v a b l e c o n t i n g e n c y o f d e t a i l , a n d a n y given
animal
will therefore
frequently
be observed
to m a k e
'mistakes',
mistakes w h i c h c a n easily be fatal. T h i s is not the s a m e point as the t i m e - l a g p r o b l e m a l r e a d y m e n t i o n e d . T h e t i m e - l a g p r o b l e m arises b e c a u s e o f n o n stationarities
in
the
statistical
properties
of the
environment:
average
c o n d i t i o n s n o w a r e different f r o m t h e a v e r a g e c o n d i t i o n s e x p e r i e n c e d b y t h e animal's ancestors. T h e present point is m o r e inescapable. T h e m o d e r n a n i m a l m a y b e l i v i n g i n i d e n t i c a l average c o n d i t i o n s t o t h o s e o f a n a n c e s t o r , y e t the d e t a i l e d m o m e n t t o m o m e n t o c c u r r e n c e s f a c i n g e i t h e r o f t h e m a r e not the s a m e f r o m d a y t o d a y , a n d a r e t o o c o m p l e x for p r e c i s e p r e d i c t i o n t o be possible. It is particularly in b e h a v i o u r that such mistakes are seen. T h e m o r e static a t t r i b u t e s o f a n a n i m a l , its a n a t o m i c a l s t r u c t u r e for i n s t a n c e , a r e o b v i o u s l y adapted only to long-term average conditions. An individual is either big or s m a l l , i t c a n n o t c h a n g e s i z e f r o m m i n u t e t o m i n u t e a s t h e n e e d arises. Behaviour, rapid muscular m o v e m e n t , is that part of an animal's a d a p t i v e repertoire w h i c h is specifically concerned w i t h h i g h speed adjustment. T h e animal can be n o w here, n o w there, n o w up a tree, n o w u n d e r g r o u n d , rapidly a c c o m m o d a t i n g to environmental s u c h possible c o n t i n g e n c i e s ,
w h e n defined
contingencies. in
all
T h e number of
their detail,
is
like
the
n u m b e r of possible chess positions, v i r t u a l l y infinite. Just as c h e s s - p l a y i n g c o m p u t e r s ( a n d c h e s s - p l a y i n g p e o p l e ) l e a r n t o classify c h e s s p o s i t i o n s i n t o a m a n a g e a b l e n u m b e r o f g e n e r a l i z e d classes, s o t h e best t h a t a n a d a p t a t i o n i s t c a n h o p e for i s t h a t a n a n i m a l w i l l h a v e b e e n p r o g r a m m e d t o b e h a v e i n w a y s appropriate to a m a n a g e a b l e n u m b e r of g e n e r a l c o n t i n g e n c y classes. A c t u a l c o n t i n g e n c i e s w i l l f i t these g e n e r a l classes o n l y a p p r o x i m a t e l y , a n d a p p a r e n t mistakes are therefore b o u n d to be m a d e . T h e a n i m a l t h a t w e see u p a t r e e m a y c o m e f r o m a l o n g l i n e o f t r e e dwelling ancestors.
T h e trees i n w h i c h t h e a n c e s t o r s u n d e r w e n t n a t u r a l
s e l e c t i o n w e r e , i n g e n e r a l , m u c h t h e s a m e a s t h e trees o f t o d a y . G e n e r a l r u l e s of behaviour w h i c h w o r k e d then, such as ' N e v e r go out on a l i m b that is too t h i n ' , still w o r k . B u t t h e d e t a i l s o f a n y o n e t r e e a r e i n e v i t a b l y d i f f e r e n t from
54
C o n s t r a i n t s on P e r f e c t i o n
t h e d e t a i l s o f a n o t h e r . T h e l e a v e s a r e i n s l i g h t l y different p l a c e s , t h e b r e a k i n g strain of the b r a n c h e s is o n l y a p p r o x i m a t e l y p r e d i c t a b l e from their d i a m e t e r , a n d s o o n . H o w e v e r s t r o n g l y a d a p t a t i o n i s t o u r beliefs m a y b e , w e c a n o n l y e x p e c t animals to be a v e r a g e statistical optimizers, never perfect anticipators of every detail. S o far w e h a v e c o n s i d e r e d t h e e n v i r o n m e n t a s s t a t i s t i c a l l y c o m p l e x a n d therefore
hard
to
predict.
We
h a v e not
reckoned on
its
being actively
m a l e v o l e n t from o u r a n i m a l ' s point o f v i e w . T r e e b o u g h s surely d o not d e l i b e r a t e l y s n a p out of spite w h e n m o n k e y s v e n t u r e on to t h e m . B u t a 'tree b o u g h ' m a y t u r n o u t t o b e a c a m o u f l a g e d p y t h o n , a n d o u r m o n k e y ' s last m i s t a k e i s t h e n n o a c c i d e n t b u t is, i n a sense, d e l i b e r a t e l y e n g i n e e r e d . P a r t o f a m o n k e y ' s e n v i r o n m e n t i s n o n - l i v i n g o r a t least i n d i f f e r e n t t o t h e m o n k e y ' s existence,
and
the
unpredictability.
monkey's
mistakes
can
be
put
down
to
statistical
B u t o t h e r p a r t s o f t h e m o n k e y ' s e n v i r o n m e n t consist o f
l i v i n g t h i n g s t h a t a r e t h e m s e l v e s a d a p t e d t o profit a t the e x p e n s e o f m o n k e y s . T h i s portion o f the m o n k e y ' s e n v i r o n m e n t m a y b e called m a l e v o l e n t . M a l e v o l e n t e n v i r o n m e n t a l influences m a y themselves be hard to predict for t h e s a m e r e a s o n s a s i n d i f f e r e n t o n e s , b u t t h e y i n t r o d u c e a n a d d e d h a z a r d ; a n a d d e d o p p o r t u n i t y for t h e v i c t i m t o m a k e ' m i s t a k e s ' . T h e m i s t a k e m a d e by a r o b i n in f e e d i n g a c u c k o o in its nest is p r e s u m a b l y in s o m e sense a m a l a d a p t i v e blunder. T h i s is not an isolated, u n p r e d i c t a b l e o c c u r r e n c e such a s arises b e c a u s e o f t h e s t a t i s t i c a l u n p r e d i c t a b i l i t y o f t h e n o n - m a l e v o l e n t p a r t of the e n v i r o n m e n t .
It is a recurrent blunder,
a f f l i c t i n g g e n e r a t i o n after
g e n e r a t i o n o f r o b i n s , e v e n t h e s a m e r o b i n s e v e r a l t i m e s i n its life. E x a m p l e s o f this k i n d a l w a y s m a k e u s w o n d e r a t t h e c o m p l i a n c e , i n e v o l u t i o n a r y t i m e , of the organisms
that
are manipulated
against
t h e i r best
interests.
Why
doesn't selection s i m p l y e l i m i n a t e the susceptibility of robins to the deception of cuckoos? T h i s kind of problem is one of m a n y w h i c h I believe will one d a y b e c o m e the stock in trade of a n e w subdiscipline of b i o l o g y — t h e study of m a n i p u l a t i o n , arms races a n d the extended p h e n o t y p e . M a n i p u l a t i o n and a r m s races form the subject of the next c h a p t e r , w h i c h in some w a y s can be r e g a r d e d a s a n e x p a n s i o n o f t h e t h e m e o f the final s e c t i o n o f this c h a p t e r .
4 A r m s Races and Manipulation
O n e o f m y p u r p o s e s i n this b o o k i s t o q u e s t i o n t h e ' c e n t r a l t h e o r e m ' t h a t i t i s useful t o e x p e c t i n d i v i d u a l o r g a n i s m s t o b e h a v e i n s u c h a w a y a s t o m a x i m i z e t h e i r o w n i n c l u s i v e fitness, o r i n o t h e r w o r d s t o m a x i m i z e t h e survival of copies of the genes inside them. T h e end of the p r e v i o u s c h a p t e r suggests one w a y i n w h i c h the c e n t r a l t h e o r e m m i g h t b e v i o l a t e d . O r g a n i s m s might consistently w o r k in the interests of other o r g a n i s m s r a t h e r t h a n of t h e m s e l v e s . T h a t is, t h e y m i g h t b e ' m a n i p u l a t e d ' . T h e fact that a n i m a l s frequently cause other a n i m a l s to p e r f o r m s o m e a c t i o n t h a t i s a g a i n s t t h e i r o w n b e s t i n t e r e s t s is, o f c o u r s e , w e l l k n o w n . O b v i o u s l y i t h a p p e n s e v e r y t i m e a n a n g l e r fish c a t c h e s p r e y , e v e r y t i m e a c u c k o o i s fed b y its foster m o t h e r . I s h a l l m a k e use o f b o t h t h e s e e x a m p l e s i n this c h a p t e r , b u t I s h a l l a l s o e m p h a s i z e t w o p o i n t s t h a t h a v e n o t a l w a y s b e e n stressed. F i r s t l y , i t i s n a t u r a l t o a s s u m e t h a t e v e n i f a m a n i p u l a t o r g e t s a w a y with it temporarily, it is o n l y a m a t t e r of e v o l u t i o n a r y time before the l i n e a g e of manipulated organisms comes up with a counter-adaptation.
In other
words, we tend to assume that m a n i p u l a t i o n o n l y w o r k s b e c a u s e of the 'timel a g ' c o n s t r a i n t o n p e r f e c t i o n . I n this c h a p t e r I s h a l l p o i n t o u t t h a t , o n t h e contrary, there are conditions under w h i c h we should e x p e c t m a n i p u l a t o r s to s u c c e e d c o n s i s t e n t l y a n d for i n d e f i n i t e l e n g t h s o f e v o l u t i o n a r y t i m e . I s h a l l discuss this l a t e r u n d e r t h e c a t c h - p h r a s e o f ' a r m s r a c e s ' . S e c o n d l y , u n t i l t h e last d e c a d e o r so, m o s t o f u s h a v e p a i d i n s u f f i c i e n t attention to the likelihood of intraspecific m a n i p u l a t i o n , especially e x p l o i t a t i v e m a n i p u l a t i o n w i t h i n t h e f a m i l y . I a t t r i b u t e this d e f i c i e n c y t o a r e s i d u u m of group-selectionist
intuition
which
often
lurks
in
the
depths
of the
b i o l o g i s t ' s m i n d e v e n after g r o u p s e l e c t i o n h a s b e e n r e j e c t e d a t t h e s u r f a c e level of reason. I think that a m i n o r revolution has taken p l a c e in the w a y we think a b o u t social relationships. ' G e n t e e l ' benevolent
mutual
cooperation
(Lloyd
are replaced
1979) ideas of v a g u e l y
by an
expectation
o f stark,
ruthless, o p p o r t u n i s t i c m u t u a l e x p l o i t a t i o n ( e . g . H a m i l t o n 1 9 6 4 a , b , 1 9 7 0 , 1971a; Williams
1966; Trivers 1972, 55
1974; Ghiselin
1974a; Alexander
56
A r m s Races and Manipulation
1 9 7 4 ) . T h i s r e v o l u t i o n is p o p u l a r l y associated w i t h the n a m e 'sociobiology', a l t h o u g h the association is s o m e w h a t ironic since, as I h a v e suggested before, Wilson's
(1975)
great
book
of that
name
is
in
many
respects
pre-
r e v o l u t i o n a r y i n a t t i t u d e : n o t t h e n e w s y n t h e s i s , b u t t h e last a n d g r e a t e s t s y n t h e s i s o f t h e o l d , b e n e v o l e n t r e g i m e ( e . g . his C h a p t e r 5 ) . I c a n e x e m p l i f y t h e c h a n g e d v i e w b y q u o t i n g from o n e r e c e n t p a p e r , L l o y d ' s ( 1 9 7 9 ) e n t e r t a i n i n g r e v i e w o f s e x u a l d i r t y tricks i n i n s e c t s . S e l e c t i o n for h a s t e i n m a l e s , a n d c o y n e s s i n f e m a l e s , results i n w h a t a m o u n t s t o c o m p e t i t i o n between t h e s e x e s . M a l e s m a y b e s e l e c t e d t o b y p a s s a n y c h o i c e that the females a t t e m p t to exercise, and then females selected to m a i n t a i n their options, to not be misled or to h a v e t h e i r c h o i c e s s u b v e r t e d . I f m a l e s s u b d u e a n d s e d u c e f e m a l e s w i t h true a p h r o d i s i a c s [ L l o y d g i v e s e v i d e n c e e l s e w h e r e i n the p a p e r ] , f e m a l e s m a y be expected to escape sooner or later in evolutionary time. A n d after s p e r m h a s b e e n p l a c e d i n a f e m a l e , s h e s h o u l d m a n i p u l a t e i t : s t o r e , t r a n s f e r (from c h a m b e r t o c h a m b e r ) , use, e a t , o r d i s s o l v e it, a s she m a k e s a d d i t i o n a l observations o n males. F e m a l e s m a y a c c e p t and s t o r e s p e r m f r o m a m a l e for i n s u r a n c e t h a t t h e y w i l l g e t a m a t e , a n d t h e n b e c o m e c h o o s y . . . I t i s p o s s i b l e for s p e r m t o b e m a n i p u l a t e d i n the female (e.g. sex d e t e r m i n a t i o n in H y m e n o p t e r a ) . F e m a l e reprod u c t i v e m o r p h o l o g y o f t e n i n c l u d e s sacs, v a l v e s , a n d t u b e s t h a t c o u l d h a v e e v o l v e d i n this c o n t e x t . I n f a c t , i t i s p o s s i b l e t h a t s o m e r e p o r t e d examples
of
sperm
competition
m a n i p u l a t i o n . .. G i v e n
that
are
females,
actually to
one
cases
extent
of or
sperm another,
s u b v e r t m a l e interests by the internal m a n i p u l a t i o n of ejaculate, it is not
inconceivable
that
males
will
have
evolved
little
openers,
snippers, levers a n d syringes that put sperm in the places females h a v e evolved
( ' i n t e n d e d ' ) for s p e r m w i t h p r i o r i t y u s a g e — c o l l e c t i v e l y , a
veritable Swiss A r m y K n i f e of g a d g e t r y !
T h i s kind o f unsentimental, d o g eat d o g , l a n g u a g e w o u l d not h a v e c o m e e a s i l y t o b i o l o g i s t s a f e w y e a r s a g o , b u t n o w a d a y s I a m g l a d t o say i t dominates the textbooks (e.g. A l c o c k 1979). S u c h dirty tricks, as often as not, i n v o l v e direct a c t i o n , the muscles of one i n d i v i d u a l m o v i n g to molest the b o d y of another. T h e m a n i p u l a t i o n w h i c h is t h e s u b j e c t o f this c h a p t e r i s m o r e i n d i r e c t a n d m o r e s u b t l e . A n i n d i v i d u a l i n d u c e s t h e effectors o f a n o t h e r i n d i v i d u a l t o w o r k a g a i n s t its o w n best interests, a n d in f a v o u r of the interests of the m a n i p u l a t o r . A l e x a n d e r (1974) w a s o n e o f t h e first t o e m p h a s i z e t h e i m p o r t a n c e o f s u c h m a n i p u l a t i o n . H e g e n e r a l i z e d his c o n c e p t o f q u e e n d o m i n a t i o n i n t h e e v o l u t i o n o f s o c i a l insect worker behaviour, to produce a wide-ranging theory of 'parental manipul a t i o n ' (see a l s o G h i s e l i n
1 9 7 4 a ) . He suggested that parents are in such a
A r m s Races and Manipulation
57
c o m m a n d i n g position o v e r their offspring that offspring m a y be forced to w o r k i n t h e interests o f t h e i r p a r e n t s ' g e n e t i c f i t n e s s , e v e n w h e r e this c o n f l i c t s with their o w n .
West-Eberhard
(1975)
follows A l e x a n d e r in dignifying
parental manipulation as one of three general w a y s in w h i c h individual 'altruism' can e v o l v e , the others b e i n g kin selection a n d r e c i p r o c a l altruism. R i d l e y a n d I m a k e t h e s a m e p o i n t , b u t d o n o t r e s t r i c t o u r s e l v e s t o parental manipulation ( R i d l e y & D a w k i n s in press). T h e a r g u m e n t is as follows. Biologists define b e h a v i o u r as altruistic if it f a v o u r s o t h e r i n d i v i d u a l s a t the e x p e n s e o f t h e a l t r u i s t h i m s e l f . A p r o b l e m arises, i n c i d e n t a l l y , o v e r h o w b e n e f i t a n d e x p e n s e a r e t o b e d e f i n e d . I f t h e y are defined in terms of i n d i v i d u a l survival, acts of altruism are e x p e c t e d to be very c o m m o n , and will be taken to include parental care. If they are defined in terms of i n d i v i d u a l r e p r o d u c t i v e success, p a r e n t a l c a r e no l o n g e r c o u n t s as altruism, but altruistic acts towards other relatives are p r e d i c t e d by neoD a r w i n i a n theory. If benefit a n d expense are defined in terms of i n d i v i d u a l i n c l u s i v e f i t n e s s , n e i t h e r p a r e n t a l c a r e n o r c a r e for o t h e r g e n e t i c r e l a t i v e s counts as altruism, a n d indeed a n a i v e version of the t h e o r y e x p e c t s that altruism should not really exist. A n y of the three definitions c a n be justified, a l t h o u g h if we must talk of altruism at all I prefer the first definition, the o n e that allows parental care as altruistic. But my point here is that, w h i c h e v e r definition we favour, it is met if the 'altruist' is forced— m a n i p u l a t e d — b y the beneficiary into d o n a t i n g s o m e t h i n g to h i m . F o r instance, the definition (any o f the t h r e e ) a l l o w s u s n o c h o i c e b u t t o r e g a r d t h e f e e d i n g o f a c u c k o o n e s t l i n g b y its foster p a r e n t a s a l t r u i s t i c b e h a v i o u r . M a y b e this m e a n s w e n e e d a n e w k i n d o f d e f i n i t i o n , b u t t h a t i s a n o t h e r issue. K r e b s a n d I t a k e t h e a r g u m e n t t o its l o g i c a l c o n c l u s i o n , a n d i n t e r p r e t a l l o f a n i m a l c o m m u n i cation as manipulation of signal-receiver by signal-sender ( D a w k i n s & K r e b s 1978). M a n i p u l a t i o n is, i n d e e d , p i v o t a l t o t h e v i e w o f life e x p o u n d e d i n this b o o k , a n d i t i s a trifle i r o n i c t h a t I a m o n e o f those w h o h a s c r i t i c i z e d A l e x a n d e r ' s concept of parental manipulation (Dawkins 1976a, pp. 1 4 5 - 1 4 8 ; Blick 1 9 7 7 ; Parker & M a c n a i r 1 9 7 8 ; K r e b s & D a v i e s 1 9 7 8 ; S t a m p s & M e t c a l f 1980), a n d , i n t u r n , b e e n c r i t i c i z e d for d o i n g s o ( S h e r m a n 1 9 7 8 ; H a r p e n d i n g 1 9 7 9 ; D a l y 1 9 8 0 ) . N o t w i t h s t a n d i n g these d e f e n d e r s , A l e x a n d e r ( 1 9 8 0 , p p . 3 8 - 3 9 ) h i m s e l f h a s c o n c e d e d t h a t his c r i t i c s w e r e r i g h t . C l e a r l y some clarification is necessary. Neither I, nor a n y of the later critics
mentioned,
doubted
that
selection
would
favour
parents
who
s u c c e e d e d i n m a n i p u l a t i n g their offspring, o v e r parents w h o did not. N o r did we doubt that parents w o u l d indeed, in m a n y cases, ' w i n the a r m s r a c e ' a g a i n s t offspring. A l l w e w e r e o b j e c t i n g t o w a s t h e l o g i c o f s u g g e s t i n g t h a t parents enjoy a built-in a d v a n t a g e o v e r their children, simply b e c a u s e all children aspire to b e c o m e parents. T h a t is no m o r e true than that children enjoy a built-in a d v a n t a g e simply b e c a u s e all parents w e r e o n c e c h i l d r e n .
A r m s Races and Manipulation
58
A l e x a n d e r h a d s u g g e s t e d t h a t t e n d e n c i e s t o selfishness i n c h i l d r e n , t e n d e n c i e s to act a g a i n s t the interests of their parents, c o u l d not spread b e c a u s e , w h e n t h e c h i l d g r e w u p , its o w n c h i l d r e n ' s i n h e r i t e d selfishness a g a i n s t i t w o u l d d e t r a c t f r o m its o w n r e p r o d u c t i v e s u c c e s s . F o r A l e x a n d e r this s p r a n g from his c o n v i c t i o n that 'the entire parent-offspring interaction has evolved because it benefited one of the t w o individuals—the parent. No organism can evolve p a r e n t a l b e h a v i o u r , o r e x t e n d its p a r e n t a l c a r e , unless its o w n r e p r o d u c t i o n is t h e r e b y e n h a n c e d ' ( A l e x a n d e r 1 9 7 4 , p. 340). A l e x a n d e r was, therefore, t h i n k i n g f i r m l y w i t h i n t h e p a r a d i g m o f t h e selfish o r g a n i s m . H e u p h e l d the c e n t r a l t h e o r e m t h a t a n i m a l s a c t i n t h e interests o f t h e i r o w n i n c l u s i v e f i t n e s s , a n d h e u n d e r s t o o d this t o p r e c l u d e t h e p o s s i b i l i t y o f o f f s p r i n g a c t i n g a g a i n s t t h e i r p a r e n t ' s i n t e r e s t s . B u t t h e lesson I p r e f e r t o l e a r n f r o m A l e x a n d e r i s t h a t of t h e c e n t r a l i m p o r t a n c e of m a n i p u l a t i o n itself, w h i c h I r e g a r d as a violation of the central theorem. I
believe
animals
exert
strong
power
over
other
animals,
and
that
f r e q u e n t l y a n a n i m a l ' s a c t i o n s a r e m o s t u s e f u l l y i n t e r p r e t e d a s w o r k i n g i n the i n t e r e s t s of another i n d i v i d u a l ' s i n c l u s i v e fitness, r a t h e r t h a n its o w n . L a t e r in this b o o k w e s h a l l d i s p e n s e w i t h t h e use o f the c o n c e p t o f i n c l u s i v e f i t n e s s a l t o g e t h e r , a n d t h e p r i n c i p l e s o f m a n i p u l a t i o n w i l l b e s u b s u m e d u n d e r the u m b r e l l a o f the e x t e n d e d p h e n o t y p e . B u t for t h e rest o f this c h a p t e r i t w i l l b e c o n v e n i e n t t o d i s c u s s m a n i p u l a t i o n a t the l e v e l o f t h e i n d i v i d u a l o r g a n i s m . T h e r e is an inevitable o v e r l a p here with a paper w h i c h I wrote jointly with J.
R. K r e b s on a n i m a l signals as manipulation
(Dawkins & Krebs
1 9 7 8 ) . B e f o r e p r o c e e d i n g , I feel o b l i g e d t o a c k n o w l e d g e t h a t this p a p e r h a s b e e n s e v e r e l y c r i t i c i z e d b y H i n d e ( 1 9 8 1 ) . S o m e o f his c r i t i c i s m s , w h i c h d o n o t affect t h e p a r t s o f t h e p a p e r I w i s h t o use h e r e , a r e a n s w e r e d b y C a r y l (in p r e s s ) , w h o h a d a l s o b e e n c r i t i c i z e d b y H i n d e . H i n d e t o o k u s t o task for unfairness in q u o t i n g a p p a r e n t l y group-selectionist statements by T i n b e r g e n ( 1 9 6 4 ) a n d o t h e r s w h o m w e l a b e l l e d , for w a n t o f a b e t t e r title, c l a s s i c a l e t h o l o g i s t s . I h a v e s y m p a t h y w i t h this h i s t o r i c a l c r i t i c i s m . T h e ' g o o d o f the species' passage w h i c h we q u o t e d from T i n b e r g e n w a s a g e n u i n e quotation, b u t I a g r e e t h a t i t w a s n o t t y p i c a l o f T i n b e r g e n ' s ( e . g . 1 9 6 5 ) t h i n k i n g a t that t i m e . T h e f o l l o w i n g m u c h earlier q u o t a t i o n from T i n b e r g e n w o u l d , perhaps, h a v e b e e n a f a i r e r o n e for u s t o h a v e c h o s e n : ' . . . j u s t a s the f u n c t i o n i n g o f h o r m o n e s a n d the n e r v o u s system implies not o n l y the s e n d i n g out of signals b u t also a specific responsiveness in the r e a c t i n g o r g a n , so the releaser system i n v o l v e s a specific responsiveness to p a r t i c u l a r releasers in
the reacting
i n d i v i d u a l a s w e l l a s a s p e c i f i c t e n d e n c y t o s e n d o u t t h e s i g n a l s i n the i n i t i a t o r . T h e r e l e a s e r s y s t e m ties i n d i v i d u a l s i n t o u n i t s o f a s u p e r - i n d i v i d u a l order and renders t h e m h i g h e r units subject to natural selection' ( T i n b e r g e n 1954).
Even
if outright
group-selectionism
was
strongly
opposed
by
T i n b e r g e n a n d m o s t o f his p u p i l s i n t h e e a r l y 1960s, I still t h i n k t h a t n e a r l y all of us t h o u g h t of a n i m a l signals in terms of a v a g u e notion of 'mutual
A r m s Races and Manipulation
59
b e n e f i t ' : i f s i g n a l s w e r e n o t a c t u a l l y 'for t h e g o o d o f t h e s p e c i e s ' (as i n t h e unrepresentative
quotation
from
Tinbergen),
they
were
'for
the
mutual
benefit o f b o t h s i g n a l l e r a n d r e c e i v e r ' . T h e e v o l u t i o n o f r i t u a l i z e d s i g n a l s w a s regarded as m u t u a l e v o l u t i o n : e n h a n c e d signalling p o w e r on one side w a s a c c o m p a n i e d by increased sensitivity to the signals on the o t h e r side. T o d a y we w o u l d r e c o g n i z e that if receiver sensitivity increases, signal strength does not need to increase but, instead, is m o r e likely to d e c r e a s e o w i n g t o t h e a t t e n d a n t costs o f c o n s p i c u o u s o r l o u d s i g n a l s . T h i s m i g h t b e c a l l e d the S i r A d r i a n B o u l t p r i n c i p l e . O n c e , i n r e h e a r s a l , S i r A d r i a n t u r n e d t o the v i o l a s a n d told t h e m t o p l a y o u t m o r e . ' B u t S i r A d r i a n ' , p r o t e s t e d t h e p r i n c i p a l v i o l a , ' y o u w e r e i n d i c a t i n g less a n d less w i t h y o u r b a t o n . ' ' T h e i d e a ' , r e t o r t e d t h e m a e s t r o , 'is t h a t I s h o u l d d o less a n d less, a n d y o u s h o u l d d o m o r e a n d m o r e ! ' I n those cases w h e r e a n i m a l signals r e a l l y are o f m u t u a l b e n e f i t , t h e y w i l l t e n d t o sink t o the l e v e l o f a c o n s p i r a t o r i a l w h i s p e r : i n d e e d this m a y often h a v e h a p p e n e d , t h e r e s u l t i n g s i g n a l s b e i n g t o o i n c o n s p i c u o u s for u s t o h a v e n o t i c e d t h e m . I f s i g n a l s t r e n g t h i n c r e a s e s o v e r t h e g e n e r a t i o n s this
suggests,
on
the
other
hand,
that
there
has
been
increasing
sales
r e s i s t a n c e o n t h e side o f t h e r e c e i v e r ( W i l l i a m s 1 9 6 6 ) . As mentioned earlier, an a n i m a l will not necessarily submit passively to being manipulated, and an evolutionary 'arms race' is expected to develop. A r m s races w e r e the subject of a second j o i n t p a p e r ( D a w k i n s &
Krebs
1 9 7 9 ) . W e w e r e n o t , o f c o u r s e , t h e f i r s t t o m a k e t h e p o i n t s t h a t f o l l o w i n this chapter, but nevertheless it will be convenient to quote from our t w o joint papers. W i t h permission from Dr K r e b s , I shall do so w i t h o u t b r e a k i n g the flow with repeated bibliographic citations and quotation marks. A n a n i m a l often n e e d s t o m a n i p u l a t e o b j e c t s i n t h e w o r l d a r o u n d it. A p i g e o n c a r r i e s t w i g s t o its nest. A c u t t l e f i s h b l o w s s a n d f r o m t h e s e a b o t t o m t o e x p o s e p r e y . A b e a v e r fells trees a n d , b y m e a n s o f its d a m , m a n i p u l a t e s t h e e n t i r e l a n d s c a p e for m i l e s a r o u n d its l o d g e . W h e n t h e o b j e c t a n a n i m a l s e e k s t o m a n i p u l a t e i s n o n - l i v i n g , o r a t least w h e n i t i s n o t s e l f - m o b i l e , t h e a n i m a l has n o c h o i c e b u t t o shift i t b y b r u t e f o r c e . A d u n g b e e t l e c a n m o v e a b a l l o f d u n g o n l y b y f o r c i b l y p u s h i n g it. B u t s o m e t i m e s a n a n i m a l m a y b e n e f i t b y m o v i n g a n ' o b j e c t ' w h i c h h a p p e n s , itself, t o b e a n o t h e r l i v i n g a n i m a l . T h e o b j e c t has m u s c l e s a n d l i m b s o f its o w n , c o n t r o l l e d b y a n e r v o u s s y s t e m a n d sense o r g a n s . W h i l e i t m a y still b e p o s s i b l e t o shift s u c h a n ' o b j e c t ' b y b r u t e force, the g o a l m a y often b e m o r e e c o n o m i c a l l y e n g i n e e r e d b y s u b t l e r m e a n s . T h e object's muscles—may
internal be
chain
infiltrated
of command—sense organs, and
subverted.
A
male
nervous system, cricket
does
not
p h y s i c a l l y roll a f e m a l e a l o n g t h e g r o u n d a n d i n t o his b u r r o w . H e sits a n d sings, a n d the f e m a l e c o m e s t o h i m u n d e r h e r o w n p o w e r . F r o m his p o i n t o f v i e w this communication i s e n e r g e t i c a l l y m o r e efficient t h a n t r y i n g t o t a k e h e r by force. A q u e s t i o n i m m e d i a t e l y arises. W h y s h o u l d t h e f e m a l e s t a n d for i t ? S i n c e
A r m s R a c e s and M a n i p u l a t i o n
6o
s h e i s i n c o n t r o l o f h e r o w n m u s c l e s a n d l i m b s , w h y w o u l d she a p p r o a c h t h e male
unless
it
is
in
her
genetic
interests
to
do
so?
Surely
the
word
m a n i p u l a t i o n is a p p r o p r i a t e o n l y if the v i c t i m is u n w i l l i n g ? S u r e l y the m a l e c r i c k e t i s s i m p l y i n f o r m i n g t h e f e m a l e o f a f a c t t h a t i s useful t o h e r , t h a t o v e r h e r e i s a r e a d y a n d w i l l i n g m a l e o f h e r o w n s p e c i e s . H a v i n g g i v e n h e r this i n f o r m a t i o n , d o e s n ' t h e t h e n l e a v e i t u p t o h e r t o a p p r o a c h h i m o r n o t a s she pleases, or as natural selection has p r o g r a m m e d her? W e l l a n d g o o d w h e n m a l e s a n d f e m a l e s h a p p e n t o h a v e i d e n t i c a l interests, b u t e x a m i n e t h e p r e m i s e o f t h e last p a r a g r a p h . W h a t e n t i t l e s u s t o assert t h a t t h e f e m a l e i s ' i n c o n t r o l o f h e r o w n m u s c l e s a n d l i m b s ' ? D o e s n ' t this b e g the very question we are interested in? By a d v a n c i n g a manipulation hypothesis w e a r e , i n effect, s u g g e s t i n g t h a t t h e f e m a l e m a y not b e i n c o n t r o l o f h e r o w n muscles a n d limbs, a n d that the m a l e m a y be. T h i s e x a m p l e c o u l d , o f course, b e reversed, a n d the f e m a l e b e said t o m a n i p u l a t e the m a l e . T h e point b e i n g m a d e has no specific c o n n e c t i o n with sexuality.
I
could
h a v e u s e d the
e x a m p l e of plants, l a c k i n g muscles of their o w n , using insect muscles as e f f e c t o r o r g a n s t o t r a n s p o r t t h e i r p o l l e n , a n d f u e l l i n g those m u s c l e s w i t h nectar (Heinrich 1979). T h e general point is that an organism's limbs m a y be m a n i p u l a t e d
t o w o r k i n t h e i n t e r e s t s o f t h e g e n e t i c fitness o f a n o t h e r
o r g a n i s m . T h i s s t a t e m e n t c a n n o t be m a d e c o n v i n c i n g until later in the book when we have introduced
the i d e a o f the e x t e n d e d
phenotype.
F o r this
c h a p t e r w e a r e still w o r k i n g w i t h i n t h e p a r a d i g m o f the selfish o r g a n i s m , a l b e i t w e a r e s t a r t i n g t o s t r e t c h i t s o t h a t i t c r e a k s o m i n o u s l y a t the e d g e s . T h e e x a m p l e of male and female cricket m a y have been poorly chosen, b e c a u s e , a s I s a i d a b o v e , m a n y o f u s h a v e o n l y r e c e n t l y b e c o m e u s e d t o the i d e a of sexual relations as a battle. M a n y of us h a v e yet to absorb into our c o n s c i o u s n e s s t h e f a c t t h a t ' s e l e c t i o n c a n a c t i n o p p o s i t i o n o n t h e t w o sexes. C o m m o n l y , for a g i v e n t y p e o f e n c o u n t e r , m a l e s w i l l b e f a v o u r e d i f t h e y d o m a t e a n d f e m a l e s i f t h e y d o n ' t ' ( P a r k e r 1 9 7 9 ; see a l s o W e s t - E b e r h a r d 1 9 7 9 ) . I s h a l l r e t u r n t o this, b u t for t h e m o m e n t let u s use a s t a r k e r e x a m p l e o f m a n i p u l a t i o n . As starkly ruthless as a n y battle in n a t u r e is that b e t w e e n p r e d a t o r a n d p r e y . T h e r e a r e v a r i o u s t e c h n i q u e s a p r e d a t o r m a y use t o c a t c h his p r e y . H e m a y r u n after t h e m a n d a t t e m p t t o o u t p a c e , o u t s t a y , o r o u t f l a n k t h e m . H e m a y sit i n o n e p l a c e a n d a m b u s h o r t r a p t h e m . O r h e m a y d o a s angler fish and
'femmes
fatales' fireflies (Lloyd
1975,
1981)
do,
and
m a n i p u l a t e t h e p r e y ' s o w n n e r v o u s s y s t e m s o t h a t i t a c t i v e l y a p p r o a c h e s its o w n d o o m . A n a n g l e r f i s h sits o n t h e sea b o t t o m a n d i s h i g h l y c a m o u f l a g e d e x c e p t for a l o n g r o d p r o j e c t i n g f r o m t h e t o p o f t h e h e a d , o n t h e e n d o f w h i c h i s t h e ' l u r e ' , a f l e x i b l e p i e c e o f tissue w h i c h r e s e m b l e s s o m e a p p e t i z i n g m o r s e l s u c h as a w o r m . S m a l l fish, p r e y of the angler, are attracted by the lure w h i c h resembles their o w n prey. W h e n they a p p r o a c h it the a n g l e r ' p l a y s ' t h e m d o w n i n t o t h e v i c i n i t y o f his m o u t h , t h e n s u d d e n l y o p e n s his j a w s a n d
A r m s Races and Manipulation
61
the p r e y a r e e n g u l f e d i n t h e i n r u s h o f w a t e r . I n s t e a d o f u s i n g m a s s i v e b o d y and
tail
muscles
in
active
pursuit
of prey,
the
angler
uses
the
small
e c o n o m i c a l m u s c l e s c o n t r o l l i n g his r o d , t o t i t i l l a t e t h e p r e y ' s n e r v o u s s y s t e m v i a its e y e s . F i n a l l y i t i s t h e p r e y f i s h ' s o w n m u s c l e s t h a t t h e a n g l e r uses t o c l o s e the g a p b e t w e e n t h e m . K r e b s a n d I i n f o r m a l l y c h a r a c t e r i z e d a n i m a l ' c o m m u n i c a t i o n ' as a m e a n s by w h i c h one a n i m a l m a k e s use of a n o t h e r animal's muscle power. This is roughly synonymous with manipulation. T h e s a m e q u e s t i o n arises a s b e f o r e . W h y d o e s t h e v i c t i m o f m a n i p u l a t i o n s t a n d for i t ? W h y d o e s t h e p r e y f i s h r u s h l i t e r a l l y i n t o t h e j a w s o f d e a t h ? B e c a u s e i t ' t h i n k s ' i t i s r e a l l y r u s h i n g t o g e t a m e a l itself. M o r e f o r m a l l y , n a t u r a l s e l e c t i o n h a s a c t e d o n its a n c e s t o r s , f a v o u r i n g t e n d e n c i e s t o a p p r o a c h small w r i g g l i n g objects, because small w r i g g l i n g objects are usually w o r m s . Since they are not a l w a y s w o r m s but sometimes a n g l e r fish lures, there m a y well be some selection on prey fish to be cautious, or to sharpen up their powers of discrimination.
To
the
extent
that lures
are g o o d
mimics of
worms, we m a y surmise that selection has acted on the a n g l e r fishes' ancestors t o i m p r o v e t h e m , i n the f a c e o f i m p r o v e d d i s c r i m i n a t i o n b y t h e i r p r e y . S o m e prey are c a u g h t , and angler fish do m a k e a living, so some m a n i p u l a t i o n is g o i n g on successfully. I t i s c o n v e n i e n t t o use t h e m e t a p h o r o f a n a r m s r a c e w h e n e v e r w e h a v e progressive i m p r o v e m e n t s in adaptations in one lineage, as an e v o l u t i o n a r y response to progressive c o u n t e r - i m p r o v e m e n t s in an e n e m y l i n e a g e . important
to
realize
who
are
the
parties
that
are
'racing'
against
It is one
another. T h e y are not i n d i v i d u a l s but lineages. To be sure, it is i n d i v i d u a l s w h o a t t a c k a n d d e f e n d , i n d i v i d u a l s w h o k i l l o r resist b e i n g k i l l e d . B u t t h e arms race takes p l a c e on the e v o l u t i o n a r y time-scale, a n d i n d i v i d u a l s do not evolve. It is lineages that e v o l v e , and lineages that exhibit progressive trends i n r e s p o n s e t o t h e s e l e c t i o n p r e s s u r e s set u p b y t h e p r o g r e s s i v e i m p r o v e m e n t s in other lineages. O n e lineage will tend to e v o l v e a d a p t a t i o n s to m a n i p u l a t e the b e h a v i o u r o f a n o t h e r l i n e a g e , t h e n the s e c o n d l i n e a g e w i l l e v o l v e c o u n t e r - a d a p t a t i o n s . We must o b v i o u s l y be interested in a n y g e n e r a l rules g o v e r n i n g w h e t h e r o n e o r the o t h e r l i n e a g e c a n ' w i n ' , o r h a v e a b u i l t - i n a d v a n t a g e . I t w a s j u s t such a built-in a d v a n t a g e that A l e x a n d e r attributed to parents o v e r their c h i l d r e n . A p a r t f r o m his m a j o r t h e o r e t i c a l a r g u m e n t w h i c h , a s w e h a v e seen, is n o w not f a v o u r e d , he also p l a u s i b l y s u g g e s t e d v a r i o u s p r a c t i c a l a d v a n t a g e s of parents o v e r offspring: '. . . the p a r e n t is b i g g e r a n d stronger t h a n t h e o f f s p r i n g , h e n c e i n a b e t t e r p o s i t i o n t o i m p o s e its w i l l ' ( A l e x a n d e r 1974). T h i s is true, paragraph,
but we must not forget
t h e lesson o f t h e p r e v i o u s
that an arms race is run in e v o l u t i o n a r y
time.
In any one
g e n e r a t i o n the m u s c l e s o f a p a r e n t a r e s t r o n g e r t h a n t h o s e o f its o f f s p r i n g , and w h o e v e r controls those muscles must h a v e the u p p e r h a n d .
But the
62
A r m s R a c e s and M a n i p u l a t i o n
q u e s t i o n a t issue is, who c o n t r o l s t h e p a r e n t s ' m u s c l e s ? A s T r i v e r s ( 1 9 7 4 ) s a y s , A n o f f s p r i n g c a n n o t f l i n g its m o t h e r t o t h e g r o u n d a t w i l l a n d n u r s e . . . the offspring is e x p e c t e d to e m p l o y p s y c h o l o g i c a l rather than physical tactics.' Krebs
and
I
suggested
that
animal
signals
could
be
thought
of as
e m p l o y i n g p s y c h o l o g i c a l t a c t i c s i n r a t h e r the s a m e w a y a s h u m a n a d v e r t i s e m e n t s . A d v e r t i s e m e n t s a r e n o t t h e r e t o i n f o r m , o r t o m i s i n f o r m , t h e y are t h e r e t o persuade. T h e a d v e r t i s e r uses his k n o w l e d g e o f h u m a n p s y c h o l o g y , o f the
hopes,
fears
and
secret
motives
o f his
targets,
and
he
designs
an
a d v e r t i s e m e n t w h i c h is effective in m a n i p u l a t i n g their b e h a v i o u r . P a c k a r d ' s (1957) expose of the d e e p p s y c h o l o g i c a l techniques of c o m m e r c i a l advertisers m a k e s f a s c i n a t i n g r e a d i n g for t h e e t h o l o g i s t .
A s u p e r m a r k e t m a n a g e r is
q u o t e d a s s a y i n g ' P e o p l e like t o see a lot o f m e r c h a n d i s e . W h e n t h e r e a r e o n l y t h r e e o f f o u r c a n s o f a n i t e m o n a shelf, t h e y j u s t w o n ' t m o v e . ' T h e o b v i o u s a n a l o g y w i t h lek b i r d s d o e s n o t lose its v a l u e m e r e l y b e c a u s e the p h y s i o l o g i c a l m e c h a n i s m o f t h e effect w i l l p r o b a b l y p r o v e t o b e different i n the
t w o cases.
Hidden cine-cameras
r e c o r d i n g the e y e - b l i n k i n g rate of
h o u s e w i v e s i n a s u p e r m a r k e t i n d i c a t e d t h a t i n s o m e c a s e s t h e effect o f the multiplicity of bright-coloured packages was to induce a mild hypnoidal trance. K. N e l s o n o n c e g a v e a talk at a conference, entitled 'Is bird song music? W e l l , then, is it l a n g u a g e ? W e l l , then, w h a t is it?' Perhaps bird song is more akin to h y p n o t i c persuasion, or to a form of d r u g g i n g . T h e nightingale's song induced in J o h n K e a t s a drowsy numbness ' . . . drunk'.
as though of hemlock I had
M i g h t i t n o t h a v e a n e v e n m o r e p o w e r f u l effect o n t h e n e r v o u s
system of a n o t h e r n i g h t i n g a l e ? If nervous systems are susceptible to drug-like i n f l u e n c e s v i a t h e n o r m a l sense o r g a n s , s h o u l d w e n o t p o s i t i v e l y e x p e c t t h a t n a t u r a l s e l e c t i o n w o u l d h a v e f a v o u r e d t h e e x p l o i t a t i o n o f s u c h possibilities, would
have favoured
the d e v e l o p m e n t of visual,
olfactory,
or auditory
'drugs'? A neurophysiologist, presented w i t h an a n i m a l with a c o m p l e x nervous system
and
asked
to
manipulate
the
animal's
behaviour,
may
insert
electrodes in sensitive points of the brain a n d stimulate electrically, or m a k e p i n p o i n t l e s i o n s . A n a n i m a l n o r m a l l y d o e s n o t h a v e d i r e c t a c c e s s t o the b r a i n of a n o t h e r a n i m a l , a l t h o u g h I shall m e n t i o n o n e e x a m p l e , the so-called b r a i n w o r m , i n C h a p t e r 1 2 . B u t t h e e y e s a n d ears a r e a l s o e n t r y p o r t s t o the nervous system, a n d there m i g h t be patterns of light or sound w h i c h , if p r o p e r l y d e p l o y e d , c o u l d be as effective as direct electrical stimulation. G r e y W a l t e r ( 1 9 5 3 ) v i v i d l y i l l u s t r a t e s t h e p o w e r o f f l a s h i n g l i g h t s t u n e d t o the f r e q u e n c y o f h u m a n E E G r h y t h m s : i n o n e c a s e a m a n felt ' a n irresistible urge to strangle the person next to h i m ' . I f w e w e r e a s k e d t o i m a g i n e w h a t a n ' a u d i t o r y d r u g ' w o u l d s o u n d l i k e , say for m a k i n g t h e s o u n d t r a c k o f a s c i e n c e fiction f i l m , w h a t w o u l d w e s a y ? T h e i n c e s s a n t r h y t h m o f a n A f r i c a n d r u m ; t h e e e r i e t r i l l i n g o f t h e tree c r i c k e t
A r m s R a c e s and M a n i p u l a t i o n
63
Oecanthus, o f w h i c h i t h a s b e e n s a i d t h a t i f m o o n l i g h t c o u l d b e h e a r d t h a t i s how it would sound (quoted in Bennet-Clark
1 9 7 1 ) ; or the s o n g of the
n i g h t i n g a l e ? A l l three strike me as w o r t h y c a n d i d a t e s , a n d I b e l i e v e all three h a v e b e e n i n s o m e sense d e s i g n e d for t h e s a m e p u r p o s e : t h e m a n i p u l a t i o n o f one nervous system by another, in a w a y that is not in p r i n c i p l e different from manipulation of a nervous system by a neurophysiologist's electrodes. Of c o u r s e i f a n a n i m a l s o u n d p o w e r f u l l y affects a h u m a n n e r v o u s s y s t e m this i s probably incidental. T h e hypothesis being a d v a n c e d is that selection has shaped animal sounds to m a n i p u l a t e some nervous system, not necessarily a h u m a n o n e . T h e snort o f a p i g - f r o g Rana grylio m a y affect a n o t h e r p i g - f r o g a s the n i g h t i n g a l e a f f e c t e d K e a t s , o r t h e s k y l a r k S h e l l e y . T h e n i g h t i n g a l e h a p p e n e d t o b e a b e t t e r e x a m p l e for m e t o c h o o s e , b e c a u s e h u m a n n e r v o u s systems c a n b e m o v e d t o d e e p e m o t i o n b y n i g h t i n g a l e s o n g , w h e r e a s t h e y a r e u s u a l l y m o v e d t o l a u g h a t p i g - f r o g snorts. C o n s i d e r that other celebrated songster, the c a n a r y , since m u c h h a p p e n s t o b e k n o w n a b o u t t h e p h y s i o l o g y o f its r e p r o d u c t i v e b e h a v i o u r ( H i n d e & Steel
1978).
If a
physiologist
wants
to
bring
a
female
canary
into
r e p r o d u c t i v e c o n d i t i o n , i n c r e a s e t h e size o f h e r f u n c t i o n a l o v a r y a n d c a u s e h e r t o start n e s t - b u i l d i n g a n d o t h e r r e p r o d u c t i v e b e h a v i o u r p a t t e r n s , t h e r e are v a r i o u s t h i n g s h e c a n d o .
He c a n inject her w i t h g o n a d o t r o p i n s or
o e s t r o g e n s . H e c a n use e l e c t r i c l i g h t t o i n c r e a s e t h e d a y - l e n g t h
that she
experiences. O r , most interestingly from o u r point of v i e w , he c a n p l a y her a tape recording of m a l e c a n a r y song. It a p p a r e n t l y has to be c a n a r y s o n g ; b u d g e r i g a r s o n g w i l l n o t d o , a l t h o u g h b u d g e r i g a r s o n g h a s a s i m i l a r effect o n female budgerigars. N o w suppose a m a l e c a n a r y w a n t e d to bring a female into reproductive condition, w h a t could he d o ? He does not h a v e a syringe to inject h o r m o n e s . H e cannot switch o n artificial lights i n the female's e n v i r o n m e n t . O f course w h a t he does is sing. T h e particular pattern of sounds that he m a k e s enters the f e m a l e ' s h e a d t h r o u g h h e r e a r s , i s t r a n s l a t e d i n t o n e r v e i m p u l s e s , a n d bores i n s i d i o u s l y i n t o h e r p i t u i t a r y . T h e m a l e d o e s n o t h a v e t o s y n t h e s i z e a n d inject g o n a d o t r o p i n s ; h e m a k e s t h e f e m a l e ' s p i t u i t a r y w o r k t o s y n t h e s i z e t h e m for h i m . H e s t i m u l a t e s h e r p i t u i t a r y b y m e a n s o f n e r v e i m p u l s e s . T h e y a r e n o t ' h i s ' n e r v e i m p u l s e s , i n t h e sense t h a t t h e y a l l o c c u r w i t h i n t h e f e m a l e ' s o w n n e r v e c e l l s . B u t t h e y a r e his i n a n o t h e r s e n s e . I t i s his p a r t i c u l a r sounds w h i c h are subtly fashioned to m a k e the female's nerves w o r k on her pituitary. W h e r e a physiologist might p u m p g o n a d o t r o p i n s into the female's breast muscle, or electric c u r r e n t into her b r a i n , the m a l e c a n a r y p o u r s s o n g i n t o h e r e a r . A n d t h e effect i s t h e s a m e . S c h l e i d t ( 1 9 7 3 ) d i s c u s s e s o t h e r e x a m p l e s o f s u c h ' t o n i c ' effects o f s i g n a l s o n t h e p h y s i o l o g y o f t h e r e c e i v e r . ' B o r e s i n s i d i o u s l y i n t o h e r p i t u i t a r y ' m a y b e t o o m u c h for s o m e r e a d e r s . Certainly it begs important questions. T h e obvious point that will be m a d e is t h a t the f e m a l e m a y b e n e f i t f r o m t h e t r a n s a c t i o n a s m u c h a s t h e m a l e , i n
A r m s Races and Manipulation
64
which
case
'insidiously'
and
'manipulation'
are
inappropriate
words.
A l t e r n a t i v e l y , if there is a n y insidious m a n i p u l a t i o n it m a y be by the female o n t h e m a l e . M a y b e t h e f e m a l e 'insists' u p o n a n e x h a u s t i n g p e r f o r m a n c e o f s o n g b y h e r m a t e b e f o r e she w i l l c o m e i n t o r e p r o d u c t i v e c o n d i t i o n , t h e r e b y s e l e c t i n g o n l y t h e m o s t r o b u s t m a l e for a m a t e . I t h i n k s o m e t h i n g a l o n g those lines i s q u i t e p r o b a b l y t h e e x p l a n a t i o n o f t h e e x t r a o r d i n a r i l y h i g h r a t e o f c o p u l a t i o n o b s e r v e d in large cats ( E a t o n 1978). S c h a l l e r (1972) followed a s a m p l e m a l e l i o n for 5 5 h o u r s , d u r i n g w h i c h h e c o p u l a t e d 1 5 7 t i m e s , w i t h a n a v e r a g e inter-copulation interval of 21 minutes. O v u l a t i o n in cats is induced b y c o p u l a t i o n . I t s e e m s p l a u s i b l e t h a t t h e p r o d i g i o u s c o p u l a t i o n rates s h o w n by m a l e lions are the end p r o d u c t of a r u n a w a y arms race, in w h i c h females insisted o n p r o g r e s s i v e l y m o r e c o p u l a t i o n s b e f o r e o v u l a t i n g , a n d m a l e s w e r e s e l e c t e d for e v e r - i n c r e a s e d s e x u a l s t a m i n a . L i o n c o p u l a t i o n s t a m i n a m i g h t b e r e g a r d e d a s t h e b e h a v i o u r a l e q u i v a l e n t o f a p e a c o c k ' s t a i l . A v e r s i o n o f this hypothesis is c o m p a t i b l e with that of B e r t r a m
(1978), that females have
d e v a l u e d t h e c u r r e n c y o f c o p u l a t i o n a s a m e a n s o f r e d u c i n g the o c c u r r e n c e o f disruptive m a l e fights. T o c o n t i n u e the q u o t a t i o n from T r i v e r s o n p s y c h o l o g i c a l m a n i p u l a t i o n t a c t i c s t h a t c h i l d r e n m i g h t use a g a i n s t t h e i r p a r e n t s : S i n c e a n o f f s p r i n g w i l l often h a v e b e t t e r k n o w l e d g e o f its r e a l n e e d s t h a n w i l l its p a r e n t s , s e l e c t i o n s h o u l d f a v o u r p a r e n t a l a t t e n t i v e n e s s t o s i g n a l s f r o m its o f f s p r i n g t h a t a p p r i z e t h e p a r e n t o f t h e offspring's c o n d i t i o n . . . B u t o n c e s u c h a s y s t e m h a s e v o l v e d , t h e offspring c a n b e g i n t o e m p l o y i t o u t o f c o n t e x t . T h e o f f s p r i n g c a n c r y not o n l y w h e n i t i s f a m i s h e d b u t a l s o w h e n i t m e r e l y w a n t s m o r e f o o d t h a n the parent
is
selected
to
g i v e . .. Selection
will
then of course favor
p a r e n t a l a b i l i t y t o d i s c r i m i n a t e t h e t w o uses o f t h e s i g n a l s , b u t still subtler m i m i c r y a n d d e c e p t i o n by the offspring are a l w a y s possible [Trivers 1974]. W e h a v e a r r i v e d a g a i n a t the m a i n question raised b y arms races. A r e there a n y g e n e r a l i z a t i o n s w e c a n m a k e a b o u t w h i c h side i s l i k e l y t o ' w i n ' a n a r m s race? F i r s t , w h a t d o e s i t mean t o s p e a k o f o n e s i d e o r t h e o t h e r ' w i n n i n g ' ? D o e s the
'loser'
eventually go extinct? At
times
this m a y h a p p e n .
A bizarre
p o s s i b i l i t y i s s u g g e s t e d b y L l o y d a n d D y b a s ( 1 9 6 6 ) for p e r i o d i c a l c i c a d a s (Simon, 1979, gives an entertaining recent a c c o u n t ) . Periodical cicadas are t h r e e s p e c i e s o f t h e g e n u s Magicicada. A l l t h r e e s p e c i e s h a v e t w o v a r i e t i e s , a 17-year and a
1 3 - y e a r v a r i e t y . E a c h i n d i v i d u a l s p e n d s 1 7 (or 13) y e a r s
f e e d i n g a s a n u n d e r g r o u n d n y m p h , b e f o r e e m e r g i n g for a f e w w e e k s o f a d u l t r e p r o d u c t i v e life, after w h i c h i t d i e s . I n a n y p a r t i c u l a r a r e a a l l life c y c l e s a r e s y n c h r o n i z e d , w i t h the result that e a c h area experiences a c i c a d a p l a g u e
A r m s Races and Manipulation
65
e v e r y 1 7 (or 13) y e a r s . T h e f u n c t i o n a l s i g n i f i c a n c e o f this i s p r e s u m a b l y t h a t would-be predators or parasites are s w a m p e d in p l a g u e years and starved in i n t e r v e n i n g y e a r s . T h e risk t o a n i n d i v i d u a l w h o r e m a i n s s y n c h r o n i z e d i s t h e r e f o r e less t h a n t h e risk t o o n e w h o b r e a k s s y n c h r o n y a n d e m e r g e s , s a y , a y e a r early. But g i v e n the a d m i t t e d a d v a n t a g e o f s y n c h r o n y , w h y d i d n ' t the c i c a d a s settle o n a s h o r t e r life c y c l e t h a n 1 7 (or 13) y e a r s , t h e r e b y r e d u c i n g the u n f o r t u n a t e d e l a y b e f o r e r e p r o d u c t i o n ? L l o y d a n d D y b a s ' s s u g g e s t i o n i s t h a t the l o n g life c y c l e i s t h e e n d r e s u l t o f a n ' e v o l u t i o n a r y r a c e t h r o u g h time'
with
a
now
extinct
predator
(or
parasitoid).
'This
hypothetical
p a r a s i t o i d p r e s u m a b l y h a d a life c y c l e t h a t w a s a l m o s t s y n c h r o n i z e d w i t h , a n d n e a r l y e q u a l i n l e n g t h t o ( b u t a l w a y s s l i g h t l y less t h a n ) , t h e a n c e s t r a l protoperiodical c i c a d a . As the theory goes, the c i c a d a s finally o u t r a n their parasitoid
pursuer
and
the
poor specialized
beast
went extinct'
(Simon
1979). Ingeniously, L l o y d a n d D y b a s go further a n d suggest that the arms r a c e c u l m i n a t e d i n life c y c l e s l a s t i n g a p r i m e n u m b e r o f y e a r s ( 1 3 o r 1 7 ) b e c a u s e o t h e r w i s e a p r e d a t o r w i t h a s h o r t e r life c y c l e m i g h t s y n c h r o n i z e w i t h the c i c a d a s e v e r y s e c o n d o r e v e r y t h i r d t i m e a r o u n d ! T h e r e i s r e a l l y n o n e e d for t h e ' l o s e r ' l i n e a g e o f a n a r m s r a c e t o g o e x t i n c t , a s s u g g e s t e d for t h e c i c a d a p a r a s i t o i d . I t m a y b e t h a t t h e ' w i n n e r ' i s s u c h a r a r e s p e c i e s t h a t i t c o n s t i t u t e s a r e l a t i v e l y n e g l i g i b l e risk t o i n d i v i d u a l s o f t h e ' l o s e r ' s p e c i e s . T h e w i n n e r o n l y w i n s i n the sense t h a t its a d a p t a t i o n s a g a i n s t the loser a r e n o t e f f e c t i v e l y c o u n t e r e d . T h i s i s g o o d for i n d i v i d u a l s o f t h e w i n n e r l i n e a g e , b u t i t m a y n o t b e v e r y b a d for i n d i v i d u a l s o f t h e l o s e r l i n e a g e w h o , after a l l , a r e r u n n i n g o t h e r r a c e s s i m u l t a n e o u s l y a g a i n s t o t h e r l i n e a g e s , possibly v e r y successfully. This
' r a r e - e n e m y effect'
is an important e x a m p l e of an
asymmetry in
s e l e c t i o n p r e s s u r e s a c t i n g o n t h e t w o sides o f a n a r m s r a c e . A l t h o u g h w e g a v e no formal models, K r e b s and I considered one such a s y m m e t r y q u a l i t a t i v e l y u n d e r the c a t c h p h r a s e h e a d i n g o f t h e ' l i f e / d i n n e r p r i n c i p l e ' , n a m e d after a fable o f A e s o p w h i c h w a s c a l l e d t o o u r attention b y M . S l a t k i n : ' T h e r a b b i t runs faster t h a n t h e f o x , b e c a u s e t h e r a b b i t i s r u n n i n g for his life w h i l e t h e fox i s o n l y r u n n i n g for his d i n n e r . ' T h e g e n e r a l p o i n t h e r e i s t h a t for a n a n i m a l o n o n e side o f the a r m s r a c e t h e p e n a l t y o f f a i l u r e i s m o r e s e v e r e t h a n for a n a n i m a l o n the o t h e r side o f t h e a r m s r a c e . M u t a t i o n s t h a t m a k e f o x e s r u n m o r e s l o w l y t h a n r a b b i t s m i g h t t h e r e f o r e s u r v i v e i n t h e fox g e n e - p o o l l o n g e r than mutations that cause rabbits to run slowly c a n e x p e c t to survive in the r a b b i t g e n e - p o o l . A fox m a y r e p r o d u c e after b e i n g o u t r u n b y a r a b b i t . N o r a b b i t h a s e v e r r e p r o d u c e d after b e i n g o u t r u n b y a f o x . F o x e s m a y t h e r e f o r e b e b e t t e r a b l e t h a n r a b b i t s t o d i v e r t r e s o u r c e s a w a y f r o m a d a p t a t i o n s for r u n n i n g fast a n d i n t o o t h e r a d a p t a t i o n s ; r a b b i t s t h e r e f o r e a p p e a r t o ' w i n ' t h e a r m s r a c e a s far a s r u n n i n g s p e e d i s c o n c e r n e d . T h e p o i n t i s r e a l l y o n e a b o u t asymmetries in strengths of selection pressure. P r o b a b l y t h e s i m p l e s t a s y m m e t r y arises f r o m w h a t I h a v e j u s t c a l l e d t h e
66
A r m s Races and Manipulation
r a r e - e n e m y effect, w h e r e o n e side i n t h e a r m s r a c e i s r a r e e n o u g h t o e x e r t a r e l a t i v e l y n e g l i g i b l e influence on a n y g i v e n i n d i v i d u a l on the other side. T h i s c a n b e i l l u s t r a t e d b y t h e a n g l e r f i s h e x a m p l e a g a i n , a n d t h e e x a m p l e h a s the additional merit of s h o w i n g that there is no necessary reason w h y prey ('rabbits') should c o m e out ' a h e a d ' of predators ('foxes'). A s s u m e that angler f i s h a r e r a t h e r r a r e , s o h o w e v e r u n p l e a s a n t i t m a y b e for a n i n d i v i d u a l p r e y t o b e c a u g h t b y a n a n g l e r f i s h , t h e risk o f this h a p p e n i n g t o a r a n d o m l y d e s i g n a t e d i n d i v i d u a l i s n o t h i g h . A n y a d a p t a t i o n costs s o m e t h i n g . F o r a small
fish
to
discriminate
angler
fish
lures
from
real
worms
it
needs
s o p h i s t i c a t e d v i s u a l p r o c e s s i n g a p p a r a t u s . T o m a k e this a p p a r a t u s m a y cost i t r e s o u r c e s w h i c h c o u l d o t h e r w i s e h a v e b e e n p u t i n t o , s a y g o n a d s (see C h a p t e r 3). T h e n a g a i n , using the a p p a r a t u s takes time, w h i c h could h a v e b e e n spent on c o u r t i n g females or defending a territory, or indeed chasing the p r e y if it is j u d g e d to be a real w o r m . F i n a l l y , a fish that is v e r y c a u t i o u s a b o u t a p p r o a c h i n g w o r m - l i k e o b j e c t s m a y c u t its risk o f b e i n g e a t e n , b u t i t a l s o i n c r e a s e s its risk o f s t a r v i n g . T h i s i s b e c a u s e i t m a y a v o i d m a n y p e r f e c t l y g o o d w o r m s b e c a u s e t h e y might h a v e b e e n a n g l e r f i s h lures. I t may
well
be
that
the
balance
o f costs
and
benefits
favours
complete
r e c k l e s s n e s s o n t h e p a r t o f s o m e p r e y a n i m a l s . I n d i v i d u a l s t h a t always try t o e a t s m a l l w r i g g l i n g o b j e c t s , a n d d a m n the c o n s e q u e n c e s , m a y , o n a v e r a g e , d o b e t t e r t h a n i n d i v i d u a l s t h a t p a y t h e costs o f a t t e m p t i n g t o d i s c r i m i n a t e r e a l w o r m s f r o m a n g l e r f i s h l u r e s . W i l l i a m J a m e s m a d e m u c h the s a m e p o i n t in 1 9 1 0 : ' T h e r e are m o r e w o r m s unattached to hooks than impaled upon t h e m ; therefore, on the w h o l e , says N a t u r e to her fishy children, bite at every w o r m a n d take y o u r c h a n c e s ' (quoted by S t a d d o n in press). N o w l o o k a t i t f r o m t h e p o i n t o f v i e w o f the a n g l e r fish. It, t o o , n e e d s t o s p e n d r e s o u r c e s o n a p p a r a t u s t o o u t w i t its o p p o n e n t s i n t h e a r m s r a c e . T h e resources that go into m a k i n g a lure c o u l d h a v e been put into gonads. T h e t i m e s p e n t s i t t i n g m o t i o n l e s s w a i t i n g p a t i e n t l y for p r e y c o u l d h a v e b e e n spent
in
actively searching
for
a
mate.
But
the
angler fish absolutely
d e p e n d s o n t h e s u c c e s s o f its l u r e for s u r v i v a l . A n a n g l e r f i s h t h a t i s n o t w e l l e q u i p p e d to lure p r e y will starve. A prey fish that is not well e q u i p p e d to a v o i d b e i n g l u r e d m a y r u n o n l y a s m a l l risk o f b e i n g e a t e n , a n d m a y m o r e t h a n c o m p e n s a t e for t h e risk b y s a v i n g t h e c o s t o f m a k i n g a n d u s i n g the equipment. I n this e x a m p l e t h e a n g l e r w i n s t h e a r m s r a c e a g a i n s t its p r e y , s i m p l y b e c a u s e its s i d e o f t h e a r m s r a c e c o n s t i t u t e s a r e l a t i v e l y n e g l i g i b l e t h r e a t t o a n y g i v e n i n d i v i d u a l o f t h e o t h e r s i d e , t h r o u g h b e i n g r a r e . T h i s d o e s not, b y t h e w a y , m e a n t h a t s e l e c t i o n w i l l f a v o u r p r e d a t o r s t h a t t a k e steps t o b e r a r e , or
to
constitute
a
small
threat
to
their
prey!
Within
the
angler fish
p o p u l a t i o n s e l e c t i o n w i l l f a v o u r those i n d i v i d u a l s w h o a r e t h e m o s t efficient killers a n d the most prolific contributors to r e d u c i n g the rarity of their species. B u t t h e a n g l e r fish l i n e a g e m a y ' k e e p a h e a d ' i n t h e a r m s r a c e a g a i n s t t h e i r
A r m s Races and Manipulation
67
p r e y , s i m p l y a s a n i n c i d e n t a l c o n s e q u e n c e o f b e i n g r a r e for s o m e o t h e r r e a s o n , r a r e i n s p i t e o f a l l t h e i r efforts. I n a d d i t i o n , t h e r e a r e l i k e l y t o b e f r e q u e n c y - d e p e n d e n t effects for v a r i o u s reasons ( S l a t k i n & M a y n a r d S m i t h 1 9 7 9 ) . F o r i n s t a n c e , a s i n d i v i d u a l s o n o n e side i n a n a r m s r a c e , s a y a n g l e r fish, b e c o m e r a r e r , t h e y w i l l c o n s t i t u t e a steadily w e a k e r threat to i n d i v i d u a l s on the other side of the a r m s race. T h e r e f o r e i n d i v i d u a l s o n t h e o t h e r side w i l l b e s e l e c t e d t o shift p r e c i o u s r e s o u r c e s a w a y f r o m a d a p t a t i o n s c o n c e r n e d w i t h this p a r t i c u l a r a r m s r a c e . I n the p r e s e n t e x a m p l e , p r e y fish a r e s e l e c t e d t o shift r e s o u r c e s a w a y f r o m anti-angler adaptations and into other things such as g o n a d s , possibly to the e x t e n t o f t o t a l r e c k l e s s n e s s a s s u g g e s t e d a b o v e . T h i s w i l l m a k e life e a s i e r for individual anglers, w h o will therefore b e c o m e m o r e n u m e r o u s . A n g l e r s will t h e n c o m e t o c o n s t i t u t e a s e v e r e r t h r e a t t o t h e p r e y fish, w h o w i l l t h e n b e s e l e c t e d t o shift r e s o u r c e s b a c k i n t o a n t i - a n g l e r a d a p t a t i o n s . A s u s u a l i n s u c h arguments, we do not h a v e to imagine an oscillation. T h e r e m a y , instead, be a n e v o l u t i o n a r i l y s t a b l e e n d p o i n t t o t h e a r m s r a c e ; s t a b l e , t h a t is, u n t i l a n e n v i r o n m e n t a l c h a n g e shifts t h e r e l e v a n t costs a n d b e n e f i t s . O b v i o u s l y , u n t i l w e k n o w a g r e a t d e a l m o r e a b o u t costs a n d b e n e f i t s i n t h e field, w e c a n n o t p r e d i c t t h e o u t c o m e o f p a r t i c u l a r a r m s r a c e s . F o r p r e s e n t p u r p o s e s this d o e s n o t m a t t e r . A l l w e n e e d i s t o satisfy o u r s e l v e s t h a t i n a n y p a r t i c u l a r a r m s r a c e i n d i v i d u a l s o n o n e side m a y h a v e m o r e t o lose t h a n i n d i v i d u a l s o n t h e o t h e r s i d e . T h e r a b b i t h a s his life t o l o s e , t h e f o x o n l y h a s his d i n n e r . T h e i n c o m p e t e n t a n g l e r f i s h d i e s ; t h e i n c o m p e t e n t a v o i d e r o f a n g l e r f i s h o n l y r u n s a t i n y risk o f d y i n g , a n d m a y , b y s a v i n g c o s t s , e n d u p b e t t e r off t h a n t h e ' c o m p e t e n t ' p r e y f i s h . We only h a v e to accept the general plausibility of such asymmetries in order to a n s w e r the question raised by o u r discussion of m a n i p u l a t i o n . We agreed that if one o r g a n i s m c o u l d get a w a y w i t h m a n i p u l a t i n g the n e r v o u s s y s t e m o f a n o t h e r , a n d e x p l o i t i n g its m u s c l e p o w e r , s e l e c t i o n w o u l d f a v o u r such manipulation. But we w e r e b r o u g h t up short by the reflection that selection w o u l d also f a v o u r resistance t o b e i n g m a n i p u l a t e d . S h o u l d w e , t h e n , r e a l l y e x p e c t t o see e f f e c t i v e m a n i p u l a t i o n i n n a t u r e ? T h e l i f e / d i n n e r p r i n c i p l e , a n d o t h e r s u c h p r i n c i p l e s a s t h e r a r e - e n e m y effect, p r o v i d e u s w i t h an answer.
I f t h e i n d i v i d u a l m a n i p u l a t o r h a s m o r e t o lose b y f a i l i n g t o
manipulate
than
the
individual
victim
has
to
lose
by
failing
to
resist
m a n i p u l a t i o n , w e s h o u l d e x p e c t t o see successful m a n i p u l a t i o n i n n a t u r e . W e s h o u l d e x p e c t t o see a n i m a l s w o r k i n g i n t h e i n t e r e s t s o f o t h e r a n i m a l s ' g e n e s . Brood parasitism provides w h a t m a y be the most striking e x a m p l e . A p a r e n t b i r d s u c h as a r e e d w a r b l e r s w e e p s a c o p i o u s f l o w of f o o d f r o m a l a r g e c a t c h m e n t a r e a i n t o t h e n a r r o w f u n n e l o f its nest. T h e r e i s a l i v i n g t o b e m a d e by a n y c r e a t u r e that evolves the necessary a d a p t a t i o n s to insert itself in the f u n n e l a n d i n t e r c e p t t h e f l o w . T h a t i s w h a t c u c k o o s a n d o t h e r b r o o d parasites
have
done.
But
the
reed
warbler
is
not
an
uncomplaining
68
A r m s Races and Manipulation
c o r n u c o p i a o f free f o o d . I t i s a n a c t i v e , c o m p l e x m a c h i n e , w i t h sense o r g a n s , m u s c l e s a n d a b r a i n . T h e b r o o d p a r a s i t e m u s t n o t o n l y h a v e its b o d y inserted in the host's nest. It must also infiltrate the defences of the host's nervous s y s t e m , a n d its p o r t s o f e n t r y a r e t h e h o s t ' s sense o r g a n s . T h e c u c k o o uses k e y s t i m u l i t o u n l o c k t h e h o s t ' s m a c h i n e r y o f p a r e n t a l c a r e a n d s u b v e r t it. T h e a d v a n t a g e s o f t h e b r o o d - p a r a s i t e w a y o f life a r e s o m a n i f e s t t h a t t o d a y we are taken a b a c k to find H a m i l t o n and O r i a n s needing, in 1965, to defend the
proposition
theories
of
that
it
has
'degenerative
Hamilton and
been
favoured
breakdown'
O r i a n s went on
of
by
natural selection,
normal
breeding
against
behaviour.
t o p r o v i d e a s a t i s f y i n g d i s c u s s i o n o f the
p r o b a b l e e v o l u t i o n a r y origins o f b r o o d parasitism, the p r e a d a p t a t i o n s w h i c h p r e c e d e d its e v o l u t i o n , a n d t h e a d a p t a t i o n s w h i c h h a v e a c c o m p a n i e d its evolution. O n e o f these a d a p t a t i o n s i s e g g m i m i c r y . T h e perfection o f e g g m i m i c r y , i n a t least s o m e ' g e n t e s ' o f c u c k o o , s h o w s t h a t foster p a r e n t s a r e p o t e n t i a l l y c a p a b l e of keen-eyed discrimination against interlopers. T h i s only underlines t h e m y s t e r y o f w h y c u c k o o hosts s e e m t o b e s o p o o r a t d i s c r i m i n a t i n g a g a i n s t c u c k o o nestlings. H a m i l t o n and O r i a n s (1965) express the p r o b l e m v i v i d l y : ' Y o u n g b r o w n - h e a d e d c o w b i r d s a n d E u r o p e a n C u c k o o s , a s they reach their m a x i m u m d i m e n s i o n , d w a r f t h e i r foster p a r e n t s . C o n s i d e r t h e l u d i c r o u s s i g h t of a t i n y G a r d e n W a r b l e r . . . [ L a t i n n a m e l e a v e s e x a c t s p e c i e s i n t e n d e d u n clear] standing a t o p a c u c k o o to reach the m o u t h of the g a p i n g parasite. W h y d o e s n o t t h e G a r d e n W a r b l e r t a k e t h e a d a p t i v e m e a s u r e o f a b a n d o n i n g the n e s t l i n g p r e m a t u r e l y , e s p e c i a l l y w h e n to t h e h u m a n o b s e r v e r it is so c l e a r l y i d e n t i f i a b l e ? ' W h e n a p a r e n t is a s m a l l f r a c t i o n of the size of the n e s t l i n g it is f e e d i n g , the m o s t r u d i m e n t a r y e y e s i g h t s h o u l d suffice t o s h o w that s o m e t h i n g h a s g o n e s e r i o u s l y w r o n g w i t h t h e n o r m a l p a r e n t a l p r o c e s s . Y e t , a t the s a m e t i m e , the e x i s t e n c e o f e g g m i m i c r y s h o w s t h a t hosts a r e c a p a b l e o f fastidious d i s c r i m i n a t i o n , m a k i n g use o f k e e n e y e s i g h t . H o w a r e w e t o e x p l a i n this p a r a d o x (see a l s o Z a h a v i 1 9 7 9 ) ? O n e fact that helps to r e d u c e the m y s t e r y is that there must be stronger s e l e c t i o n p r e s s u r e o n hosts t o d i s c r i m i n a t e a g a i n s t c u c k o o s a t t h e e g g s t a g e than against c u c k o o s at the nestling stage, simply b e c a u s e eggs o c c u r earlier. T h e b e n e f i t o f d e t e c t i n g a c u c k o o e g g i s t h e p o t e n t i a l g a i n i n g o f a n entire b r e e d i n g c y c l e in the future. T h e benefit of d e t e c t i n g a nearly fledged c u c k o o is the s a v i n g of o n l y a few d a y s , at a time w h e n it m a y be too late to breed again
anyway.
Another
mitigating circumstance
in
the
c a s e o f Cuculus
canorus ( L a c k 1 9 6 8 ) i s t h a t t h e h o s t ' s o w n y o u n g i s u s u a l l y n o t t h e r e for s i m u l t a n e o u s c o m p a r i s o n , h a v i n g been tipped out by the b a b y c u c k o o . It is w e l l k n o w n t h a t d i s c r i m i n a t i o n i s e a s i e r i f t h e r e i s a m o d e l a c t u a l l y present for c o m p a r i s o n . V a r i o u s a u t h o r s h a v e i n v o k e d the ' s u p e r n o r m a l stimulus', in one form or a n o t h e r . T h u s L a c k r e m a r k s ( p . 88) t h a t ' t h e y o u n g c u c k o o , w i t h its h u g e
A r m s Races and Manipulation
69
g a p e and loud b e g g i n g call, has e v i d e n t l y e v o l v e d in e x a g g e r a t e d form the stimuli w h i c h elicit the feeding response of p a r e n t passerine birds. So m u c h is this s o t h a t t h e r e a r e m a n y r e c o r d s o f a d u l t p a s s e r i n e b i r d s f e e d i n g a f l e d g e d y o u n g C. canorus r a i s e d by a d i f f e r e n t host s p e c i e s ; this, l i k e l i p s t i c k in t h e courtship of m a n k i n d , d e m o n s t r a t e s successful e x p l o i t a t i o n by m e a n s of a "super-stimulus".' W i c k l e r (1968) makes a similar point, q u o t i n g Heinroth a s h a v i n g r e f e r r e d t o foster p a r e n t s a s b e h a v i n g l i k e ' a d d i c t s ' , a n d t o t h e c u c k o o n e s t l i n g a s a ' v i c e o f its foster p a r e n t s ' . A s i t s t a n d s , this k i n d o f suggestion will strike m a n y critics as unsatisfying, b e c a u s e it i m m e d i a t e l y p r o m p t s a q u e s t i o n a t least a s b i g a s t h e o n e i t a n s w e r s . W h y d o e s n ' t s e l e c t i o n e l i m i n a t e f r o m t h e host s p e c i e s t h e t e n d e n c y t o b e ' a d d i c t e d ' t o 'supernormal stimuli'? T h i s , of course, is w h e r e the arms race c o n c e p t c o m e s in a g a i n . W h e n a h u m a n b e h a v e s i n a w a y t h a t i s m a n i f e s t l y b a d for h i m , for i n s t a n c e w h e n h e c o n t i n u a l l y t a k e s p o i s o n , w e m a y e x p l a i n his b e h a v i o u r i n a t l e a s t t w o w a y s . He m a y not realize that the substance that he is d r i n k i n g is poison, so closely does it resemble a g e n u i n e l y nutritous s u b s t a n c e . T h i s c o r r e s p o n d s to the host b i r d ' s b e i n g f o o l e d b y the c u c k o o ' s e g g m i m i c r y . O r h e m a y b e u n a b l e to save himself because of some direct subverting influence of the poison on his n e r v o u s s y s t e m . S u c h i s t h e c a s e o f t h e h e r o i n a d d i c t w h o k n o w s t h e d r u g is killing him, but w h o c a n n o t stop taking it because the d r u g itself controls his n e r v o u s s y s t e m . W e h a v e a l r e a d y s e e n t h a t t h e c u c k o o n e s t l i n g ' s l i p s t i c k like g a p e i s r e g a r d e d a s a s u p e r n o r m a l s t i m u l u s , a n d t h a t foster p a r e n t s h a v e been described as a p p a r e n t l y ' a d d i c t e d ' to the s u p e r n o r m a l stimulus. C o u l d i t b e t h a t the host c a n n o m o r e resist t h e s u p e r n o r m a l m a n i p u l a t i v e p o w e r o f the c u c k o o n e s t l i n g t h a n t h e j u n k i e c a n resist his f i x , o r t h a n t h e b r a i n w a s h e d p r i s o n e r c a n resist t h e o r d e r s o f his c a p t o r , h o w e v e r m u c h i t w o u l d b e n e f i t him to do so? Perhaps c u c k o o s h a v e put their a d a p t i v e emphasis on m i m e t i c deception at the e g g stage, but on positive m a n i p u l a t i o n of the host's n e r v o u s s y s t e m a t the l a t e n e s t l i n g s t a g e . A n y nervous system c a n b e subverted i f treated i n the right w a y . A n y e v o l u t i o n a r y a d a p t a t i o n o f t h e host n e r v o u s s y s t e m t o resist m a n i p u l a t i o n b y c u c k o o nestlings lays itself o p e n to c o u n t e r - a d a p t a t i o n by the c u c k o o s . S e l e c t i o n a c t i n g o n c u c k o o s w i l l w o r k t o find w h a t e v e r c h i n k s t h e r e m a y b e i n the h o s t s ' n e w l y e v o l v e d p s y c h o l o g i c a l a r m o u r . H o s t b i r d s m a y b e v e r y g o o d a t resisting p s y c h o l o g i c a l m a n i p u l a t i o n , b u t c u c k o o s m i g h t b e c o m e e v e n b e t t e r a t m a n i p u l a t i n g . A l l w e n e e d t o p o s t u l a t e i s t h a t , for s o m e r e a s o n s u c h a s t h a t s u g g e s t e d b y t h e l i f e / d i n n e r p r i n c i p l e o r t h e r a r e - e n e m y effect, c u c k o o s h a v e w o n t h e a r m s r a c e : a c u c k o o i n t h e nest h a s got t o m a n i p u l a t e its host s u c c e s s f u l l y o r i t w i l l s u r e l y d i e ; its i n d i v i d u a l f o s t e r - p a r e n t w i l l benefit s o m e w h a t i f i t resists m a n i p u l a t i o n , b u t i t still h a s a g o o d c h a n c e o f future r e p r o d u c t i v e s u c c e s s i n o t h e r y e a r s e v e n i f i t
fails
t o resist this
p a r t i c u l a r c u c k o o . M o r e o v e r , c u c k o o s m i g h t b e s u f f i c i e n t l y r a r e t h a t t h e risk
7
A r m s R a c e s and M a n i p u l a t i o n
o f a n i n d i v i d u a l o f t h e foster s p e c i e s b e i n g p a r a s i t i z e d i s l o w ; c o n v e r s e l y the ' r i s k ' o f a n i n d i v i d u a l c u c k o o ' s b e i n g a p a r a s i t e i s 100 p e r c e n t , n o m a t t e r h o w c o m m o n or rare either party to the arms race m a y be. T h e c u c k o o is d e s c e n d e d f r o m a l i n e o f a n c e s t o r s , e v e r y s i n g l e o n e o f w h o m h a s successfully f o o l e d a host. T h e h o s t i s d e s c e n d e d f r o m a l i n e o f a n c e s t o r s , m a n y o f w h o m m a y n e v e r h a v e e n c o u n t e r e d a c u c k o o in their lives, or m a y h a v e reproduced s u c c e s s f u l l y after b e i n g p a r a s i t i z e d b y a c u c k o o . T h e a r m s r a c e c o n c e p t completes the classical supernormal stimulus explanation, by providing a functional a c c o u n t of the host's m a l a d a p t i v e b e h a v i o u r , instead of l e a v i n g it as an u n e x p l a i n e d limitation of the nervous system. I n o n e respect m y t r e a t m e n t o f c u c k o o s a s m a n i p u l a t o r s m a y b e found u n s a t i s f y i n g . T h e c u c k o o is, after a l l , o n l y d i v e r t i n g t h e n o r m a l p a r e n t a l b e h a v i o u r o f its h o s t .
It has not succeeded
in
b u i l d i n g i n t o t h e host's
b e h a v i o u r a l repertoire a w h o l e n e w b e h a v i o u r pattern that w a s not there, in s o m e f o r m , b e f o r e . S o m e m i g h t find a n a l o g i e s w i t h d r u g s , h y p n o t i s m a n d e l e c t r i c a l s t i m u l a t i o n o f t h e b r a i n m o r e p e r s u a s i v e i f a n e x a m p l e o f this m o r e extreme
kind
of m a n i p u l a t i o n
could
be
found.
A
possible
case
is
the
' p r e e n i n g i n v i t a t i o n ' display of a n o t h e r b r o o d parasite, the b r o w n - h e a d e d c o w b i r d Molothrus ater ( R o t h s t e i n
1980). A l l o p r e e n i n g , the p r e e n i n g of one
i n d i v i d u a l by another, is not u n c o m m o n within various species of birds. It is not
particularly
surprising,
therefore,
that
cowbirds
should
succeed
in
g e t t i n g o t h e r b i r d s o f s e v e r a l s p e c i e s t o p r e e n t h e m . A g a i n , this c a n b e seen a s a simple diversion of intraspecific a l l o p r e e n i n g , w i t h the c o w b i r d p r o v i d i n g a s u p e r n o r m a l e x a g g e r a t i o n o f t h e n o r m a l e l i c i t i n g s t i m u l i for a l l o p r e e n i n g . W h a t is rather surprising is that c o w b i r d s m a n a g e to get themselves preened by species that n e v e r e n g a g e in intraspecific allopreening. T h e d r u g a n a l o g y i s e s p e c i a l l y a p t for i n s e c t ' c u c k o o s ' t h a t use c h e m i c a l m e a n s t o c o e r c e t h e i r hosts i n t o a c t s t h a t a r e p r o f o u n d l y d a m a g i n g t o t h e i r o w n i n c l u s i v e f i t n e s s . S e v e r a l species o f ant h a v e n o w o r k e r s o f their o w n . T h e q u e e n s i n v a d e nests o f o t h e r s p e c i e s , d i s p o s e o f t h e host q u e e n , a n d use the host w o r k e r s t o b r i n g u p their o w n r e p r o d u c t i v e y o u n g . T h e m e t h o d o f d i s p o s i n g o f t h e host q u e e n v a r i e s . I n s o m e s p e c i e s , s u c h a s t h e d e s c r i p t i v e l y named
Bothriomyrmex
regicidus
and
B.
decapitans,
the
parasite
queen
rides
a b o u t o n t h e b a c k o f t h e host q u e e n a n d t h e n , i n W i l s o n ' s ( 1 9 7 1 ) d e l i g h t f u l d e s c r i p t i o n , ' b e g i n s t h e o n e a c t for w h i c h s h e i s u n i q u e l y s p e c i a l i z e d : s l o w l y c u t t i n g off t h e h e a d o f h e r v i c t i m ' ( p . 3 6 3 ) . Monomorium santschii a c h i e v e s t h e s a m e result b y m o r e s u b t l e m e a n s . T h e host w o r k e r s h a v e w e a p o n s w i e l d e d b y strong muscles, a n d nerves attached t o t h e m u s c l e s ; w h y s h o u l d t h e p a r a s i t e q u e e n e x e r t h e r o w n j a w s i f she c a n subvert
the
nervous systems controlling
the
n u m e r o u s j a w s o f the
host
w o r k e r s ? I t d o e s n o t s e e m t o b e k n o w n h o w she a c h i e v e s it, b u t she d o e s : the h o s t w o r k e r s kill
their o w n m o t h e r and
a d o p t the usurper.
A chemical
A r m s Races and Manipulation
secreted by the parasite q u e e n seems the likely w e a p o n , in w h i c h case it m i g h t be labelled a p h e r o m o n e , but it is p r o b a b l y m o r e i l l u m i n a t i n g to think of it a s a f o r m i d a b l y p o w e r f u l d r u g . I n l i n e w i t h this i n t e r p r e t a t i o n , W i l s o n ( 1 9 7 1 , p. 413) writes of s y m p h y l i c substances as b e i n g 'more than just e l e m e n t a r y nutritive
substances
or
even
analogues
of the
natural
host
pheromones.
S e v e r a l a u t h o r s h a v e s p o k e n o f a n a r c o t i z i n g effect o f s y m p h y l i c s u b s t a n c e s . ' W i l s o n also uses t h e w o r d ' i n t o x i c a n t ' a n d q u o t e s a c a s e i n w h i c h w o r k e r a n t s under the influence of such a substance b e c a m e t e m p o r a r i l y disoriented a n d less sure o f t h e i r f o o t i n g . Those w h o have never been brainwashed or addicted to a d r u g find it hard to understand their fellow m e n w h o are d r i v e n by such c o m p u l s i o n s . In the s a m e n a i v e w a y w e c a n n o t u n d e r s t a n d a host b i r d ' s b e i n g c o m p e l l e d t o feed a n a b s u r d l y o v e r s i z e d c u c k o o , o r w o r k e r a n t s w a n t o n l y m u r d e r i n g t h e only b e i n g in the w h o l e w o r l d that is vital to their g e n e t i c success. B u t such subjective
feelings
are
misleading,
even
where
the
relatively
crude
achievements of h u m a n p h a r m a c o l o g y are concerned. W i t h natural selection w o r k i n g o n the p r o b l e m , w h o w o u l d b e s o p r e s u m p t u o u s a s t o g u e s s w h a t feats o f m i n d c o n t r o l m i g h t n o t b e a c h i e v e d ? D o n o t e x p e c t t o see a n i m a l s always b e h a v i n g in such a w a y as to m a x i m i z e their o w n inclusive fitness. Losers in an arms race m a y b e h a v e in some v e r y odd w a y s i n d e e d . If they appear
disoriented
and
unsure
of their
footing,
this
may
be
only
the
beginning. L e t me stress a g a i n w h a t a feat of m i n d - c o n t r o l t h e Monomorium santschii q u e e n a c h i e v e s . T o a sterile w o r k e r a n t , h e r m o t h e r i s a k i n d o f g e n e t i c g o l d m i n e . F o r a w o r k e r a n t t o kill h e r o w n m o t h e r i s a n a c t o f g e n e t i c m a d n e s s . W h y d o the w o r k e r s d o i t ? I a m s o r r y I c a n d o n o m o r e t h a n , o n c e a g a i n , vaguely
talk
about
arms
races.
Any
nervous
system
is
vulnerable
to
manipulation by a c l e v e r - e n o u g h p h a r m a c o l o g i s t . T h e r e is no difficulty in b e l i e v i n g t h a t n a t u r a l s e l e c t i o n a c t i n g o n M . santschii w o u l d s e e k o u t t h e w e a k p o i n t s i n t h e host w o r k e r s ' n e r v o u s s y s t e m , a n d i n s e r t a p h a r m a c o logical key in the lock. S e l e c t i o n on the host species w o u l d soon h a v e plugged
those
improve
the d r u g ,
weak
points,
and
the
whereupon
selection
arms race was
on
the
under way.
parasite If M.
would
santschii i s
sufficiently r a r e , i t i s e a s y t o see t h a t i t m i g h t ' w i n ' t h e a r m s r a c e , e v e n t h o u g h r e g i c i d e i s s u c h a d i s a s t r o u s a c t for e a c h host c o l o n y w h o s e w o r k e r s s u c c u m b t o it. T h e o v e r a l l risk o f p a r a s i t i z a t i o n b y M . santschii c o u l d b e v e r y l o w e v e n t h o u g h t h e m a r g i n a l cost o f r e g i c i d e , g i v e n t h a t a n M . santschii q u e e n has e n t e r e d , is d i s a s t r o u s l y h i g h . E a c h i n d i v i d u a l M. santschii q u e e n is descended from a line of ancestors e v e r y o n e of w h o m has s u c c e e d e d in m a n i p u l a t i n g host w o r k e r s i n t o r e g i c i d e . E a c h host w o r k e r i s d e s c e n d e d from a line o f a n c e s t o r s w h o s e c o l o n i e s m a y s e l d o m h a v e b e e n w i t h i n 1 0 m i l e s o f a n M . santschii q u e e n . T h e costs o f ' b o t h e r i n g ' t o b e e q u i p p e d t o
72
A r m s R a c e s and M a n i p u l a t i o n
resist m a n i p u l a t i o n b y a n o c c a s i o n a l M . santschii q u e e n m a y o u t w e i g h the b e n e f i t s . R e f l e c t i o n s s u c h a s this l e a d m e t o b e l i e v e t h a t t h e hosts m i g h t w e l l lose t h e a r m s r a c e . O t h e r s p e c i e s o f p a r a s i t i c a n t s use a d i f f e r e n t s y s t e m . I n s t e a d o f s e n d i n g o u t q u e e n s t o i m p l a n t t h e i r e g g s i n host nests a n d u s i n g host l a b o u r t h e r e , t h e y t r a n s p o r t h o s t l a b o u r b a c k t o t h e i r o w n nests. T h e s e a r e t h e s o - c a l l e d s l a v e m a k i n g ants.
S l a v e m a k i n g species h a v e workers,
b u t these w o r k e r s
d e v o t e part, or in some cases all, of their energy to g o i n g on slaving e x p e d i t i o n s . T h e y r a i d nests o f o t h e r s p e c i e s a n d c a r r y off l a r v a e a n d p u p a e . T h e s e s u b s e q u e n t l y h a t c h i n t h e s l a v e r s ' nest, w h e r e t h e y w o r k n o r m a l l y , f o r a g i n g a n d t e n d i n g b r o o d , n o t ' r e a l i z i n g ' t h a t t h e y a r e , i n effect, s l a v e s . T h e a d v a n t a g e o f t h e s l a v e m a k i n g w a y o f life i s p r e s u m a b l y t h a t m o s t o f the c o s t o f f e e d i n g t h e w o r k f o r c e i n t h e l a r v a l s t a g e i s s a v e d . T h a t cost i s b o r n e b y the h o m e c o l o n y from w h i c h the slave p u p a e w e r e taken. T h e s l a v e m a k i n g h a b i t is interesting from
the
present point
of view,
b e c a u s e i t raises a n u n u s u a l a r m s r a c e a s y m m e t r y . P r e s u m a b l y t h e r e i s a n arms race b e t w e e n s l a v e m a k i n g species and slave species. A d a p t a t i o n s to c o u n t e r s l a v e r y , for i n s t a n c e e n l a r g e d s o l d i e r j a w s for d r i v i n g off s l a v e raiders, should be e x p e c t e d in species that are victims of slave raids. But surely the m o r e o b v i o u s c o u n t e r m e a s u r e the slaves c o u l d take w o u l d simply b e t o w i t h h o l d t h e i r l a b o u r i n t h e s l a v e r s ' nest, o r t o kill s l a v e m a k e r b r o o d i n s t e a d o f f e e d i n g t h e m ? I t seems t h e o b v i o u s c o u n t e r m e a s u r e , b u t t h e r e a r e f o r m i d a b l e o b s t a c l e s t o its e v o l u t i o n .
Consider an adaptation to 'go on
s t r i k e ' , t o refuse t o w o r k i n t h e s l a v e m a k e r s ' nest. T h e s l a v e w o r k e r s w o u l d o f course h a v e to h a v e some m e a n s of r e c o g n i z i n g that they had hatched in a f o r e i g n nest, b u t t h a t s h o u l d n o t b e difficult i n p r i n c i p l e . T h e p r o b l e m arises w h e n we think in detail of h o w the a d a p t a t i o n s w o u l d be passed on. S i n c e w o r k e r s d o n ' t r e p r o d u c e , a l l w o r k e r a d a p t a t i o n s , i n a n y s o c i a l insect species, h a v e to be passed on by r e p r o d u c t i v e relatives of the workers. T h i s n o r m a l l y p r e s e n t s n o i n s u p e r a b l e p r o b l e m s , b e c a u s e w o r k e r s d i r e c t l y assist t h e i r o w n r e p r o d u c t i v e r e l a t i v e s , s o g e n e s g i v i n g rise t o w o r k e r a d a p t a t i o n s d i r e c t l y assist c o p i e s o f t h e m s e l v e s i n r e p r o d u c t i v e s . B u t t a k e t h e e x a m p l e o f a m u t a n t g e n e c a u s i n g slave workers to go on strike. It m a y v e r y effectively s a b o t a g e t h e s l a v e m a k e r s ' nest, p o s s i b l y w i p e i t o u t a l t o g e t h e r . A n d t o w h a t e f f e c t ? T h e a r e a n o w c o n t a i n s o n e less s l a v e m a k i n g nest, p r e s u m a b l y a g o o d t h i n g for all p o t e n t i a l v i c t i m nests i n t h e a r e a , n o t j u s t t h e nest f r o m w h i c h t h e r e b e l s l a v e s c a m e , b u t nests c o n t a i n i n g n o n - s t r i k i n g g e n e s a s w e l l . T h e s a m e k i n d o f p r o b l e m arises i n the g e n e r a l c a s e o f t h e s p r e a d o f ' s p i t e f u l ' behaviour (Hamilton 1970; K n o w l t o n & Parker 1979). T h e o n l y e a s y w a y t h e g e n e s for s t r i k i n g c a n b e p r e f e r e n t i a l l y p a s s e d o n i s for s t r i k i n g t o b e n e f i t , s e l e c t i v e l y , t h e s t r i k e r s ' o w n h o m e nest, t h e nest t h e y left b e h i n d a n d i n w h i c h t h e i r o w n r e p r o d u c t i v e r e l a t i v e s a r e b e i n g r e a r e d . T h i s c o u l d h a p p e n i f s l a v e m a k e r s h a b i t u a l l y returned t o m a k e repeat raids
A r m s Races and Manipulation
on
the
same
nest,
but
otherwise
we
must
conclude
that
73
anti-slavery
a d a p t a t i o n s m u s t b e c o n f i n e d t o t h e p e r i o d before t h e s l a v e p u p a e h a v e left t h e i r h o m e nest. O n c e t h e s l a v e s h a v e a r r i v e d i n t h e s l a v e m a k e r s ' nest t h e y effectively d r o p out of the arms race since they no l o n g e r h a v e a n y p o w e r to influence the success o f their r e p r o d u c t i v e relatives. T h e s l a v e m a k e r s c a n develop manipulative adaptations of any degree of sophistication, physical or chemical,
pheromones or powerful drugs,
and
the slaves c a n n o t e v o l v e
countermeasures. A c t u a l l y , t h e v e r y fact t h a t t h e s l a v e s c a n n o t e v o l v e c o u n t e r m e a s u r e s w i l l tend to r e d u c e the likelihood that the m a n i p u l a t i v e t e c h n i q u e s e v o l v e d by the s l a v e m a k e r s w i l l b e v e r y s o p h i s t i c a t e d : t h e f a c t t h a t t h e s l a v e s c a n n o t r e t a l i a t e , i n a n e v o l u t i o n a r y sense, m e a n s t h a t t h e s l a v e m a k e r s d o n o t n e e d to
spend
costly
resources
on
elaborate
and
sophisticated
manipulation
adaptations, because simple a n d c h e a p ones will d o . T h e e x a m p l e of slavery in a n t s is r a t h e r a s p e c i a l o n e , b u t it i l l u s t r a t e s a p a r t i c u l a r l y i n t e r e s t i n g sense i n w h i c h o n e s i d e i n a n a r m s r a c e c a n b e s a i d t o lose c o m p l e t e l y . A c a s e c o u l d b e m a d e for d r a w i n g a n a n a l o g y h e r e w i t h t h e h y b r i d f r o g Rana esculenta ( W h i t e 1 9 7 8 ) . T h i s c o m m o n E u r o p e a n f r o g , t h e e d i b l e frog o f French
restaurants,
is
not
a species
in
the
normal
sense
of the
word.
Individuals o f the 'species' are really v a r i o u s kinds o f h y b r i d s b e t w e e n t w o o t h e r species, Rana ridibunda a n d R. lessonae. T h e r e a r e t w o different d i p l o i d forms a n d t w o different t r i p l o i d f o r m s of R. esculenta. F o r s i m p l i c i t y I s h a l l c o n s i d e r o n l y o n e o f t h e d i p l o i d f o r m s , b u t t h e a r g u m e n t h o l d s for a l l t h e varieties. consists
These of one
frogs set
coexist of
with
lessonae
R.
lessonae.
chromosomes
Their diploid and
one
set
karyotype of
ridibunda
c h r o m o s o m e s . A t m e i o s i s t h e y d i s c a r d the lessonae c h r o m o s o m e s a n d p r o d u c e pure
ridibunda
gametes.
They
mate
with
lessonae
individuals,
thereby
r e s t o r i n g the h y b r i d g e n o t y p e i n the n e x t g e n e r a t i o n . I n this r a c e o f Rana esculenta b o d i e s , t h e r e f o r e , ridibunda g e n e s a r e g e r m - l i n e r e p l i c a t o r s , lessonae g e n e s d e a d - e n d o n e s . D e a d - e n d r e p l i c a t o r s c a n e x e r t p h e n o t y p i c effects. T h e y c a n even b e n a t u r a l l y selected. B u t the c o n s e q u e n c e s o f that n a t u r a l selection are irrelevant to evolution paragraph
e a s i e r to f o l l o w ,
ridibunda G
(for g e r m - l i n e )
I
(see C h a p t e r 5 ) . T o m a k e t h e n e x t
s h a l l c a l l R.
a n d R.
lessonae D
esculenta
H
(for h y b r i d ) , R.
(for d e a d - e n d ,
a l t h o u g h it
should be r e m e m b e r e d that ' D ' genes are d e a d - e n d replicators o n l y w h e n in H f r o g s ; w h e n i n ' D ' frogs t h e y a r e n o r m a l g e r m - l i n e r e p l i c a t o r s ) . N o w , c o n s i d e r a g e n e in t h e D g e n e - p o o l w h i c h e x e r t s an effect on D b o d i e s t o m a k e t h e m refuse t o m a t e w i t h H . S u c h a g e n e s h o u l d b e f a v o u r e d b y n a t u r a l s e l e c t i o n o v e r its H - t o l e r a t i n g a l l e l e , s i n c e t h e l a t t e r w i l l t e n d t o end up in H bodies of the next generation, a n d will be d i s c a r d e d at meiosis. G genes are not discarded at meiosis, a n d they w i l l tend to be selected if they influence H bodies so that they o v e r c o m e the r e l u c t a n c e of D i n d i v i d u a l s to m a t e w i t h t h e m . W e s h o u l d t h e r e f o r e see a n a r m s r a c e b e t w e e n G g e n e s
74
A r m s Races and Manipulation
a c t i n g o n H b o d i e s , a n d D g e n e s a c t i n g o n D b o d i e s . I n those r e s p e c t i v e b o d i e s , b o t h sets o f g e n e s a r e g e r m - l i n e r e p l i c a t o r s . B u t w h a t a b o u t D g e n e s acting on H bodies? T h e y should h a v e just as powerful an influence over H p h e n o t y p e s as G genes, since they constitute e x a c t l y h a l f of the H g e n o m e . N a i v e l y , we m i g h t e x p e c t them to carry their arms race against G genes over i n t o t h e H b o d i e s w h i c h t h e y s h a r e . B u t in H b o d i e s , those D g e n e s a r e in the s a m e position as ants that h a v e been taken as slaves. A n y adaptation that t h e y m e d i a t e i n t h e H b o d y c a n n o t b e p a s s e d o n t o t h e n e x t g e n e r a t i o n ; for t h e g a m e t e s p r o d u c e d b y t h e H i n d i v i d u a l , r e g a r d l e s s o f h o w his d e v e l o p i n g p h e n o t y p e , a n d i n d e e d his s u r v i v a l , m a y h a v e b e e n i n f l u e n c e d b y D g e n e s , a r e s t r i c t l y G g a m e t e s . J u s t a s w o u l d - b e s l a v e a n t s c a n b e s e l e c t e d t o resist b e i n g t a k e n i n t o c a p t i v i t y w h i l e t h e y a r e still i n t h e i r h o m e nest, b u t c a n n o t b e s e l e c t e d t o s u b v e r t t h e s l a v e m a k i n g nest o n c e t h e y a r e i n it, s o D g e n e s c a n b e s e l e c t e d t o i n f l u e n c e D b o d i e s s o t h a t t h e y resist b e i n g i n c o r p o r a t e d i n H g e n o m e s i n t h e first p l a c e , b u t o n c e s o i n c o r p o r a t e d t h e y a r e n o l o n g e r u n d e r s e l e c t i o n , e v e n t h o u g h t h e y c a n still h a v e p h e n o t y p i c effects. T h e y lose the a r m s r a c e b e c a u s e they are a d e a d - e n d . A similar a r g u m e n t could be m a d e for fish o f t h e h y b r i d ' s p e c i e s ' Poeciliopsis monacha-occidentalis ( M a y n a r d Smith 1978a). T h e inability of slaves to e v o l v e counter-adaptations w a s originally invoked by T r i v e r s a n d H a r e ( 1 9 7 6 ) , in their theory of the sex-ratio arms race in s o c i a l H y m e n o p t e r a . T h i s i s o n e o f t h e best k n o w n o f r e c e n t d i s c u s s i o n s o f a p a r t i c u l a r a r m s r a c e , a n d i t i s w o r t h c o n s i d e r i n g further. E l a b o r a t i n g o n ideas of Fisher (1930a) and H a m i l t o n ( 1 9 7 2 ) , T r i v e r s and H a r e reasoned that the e v o l u t i o n a r i l y stable sex ratio in ant species w i t h one singly mated q u e e n per nest c a n n o t be s i m p l y p r e d i c t e d . If the q u e e n is assumed to h a v e all p o w e r o v e r the sex o f r e p r o d u c t i v e offspring ( y o u n g q u e e n s and males), the stable ratio of e c o n o m i c investment in m a l e and female reproductives is 1 : 1 . If, o n t h e o t h e r h a n d , n o n - l a y i n g w o r k e r s a r e a s s u m e d t o h o l d all p o w e r o v e r i n v e s t m e n t in y o u n g , the stable ratio will be 3 : 1 in favour of females, u l t i m a t e l y b e c a u s e o f t h e h a p l o d i p l o i d g e n e t i c s y s t e m . T h e r e is, t h e r e f o r e , a potential conflict b e t w e e n q u e e n and workers. Trivers and H a r e reviewed t h e , a d m i t t e d l y i m p e r f e c t , a v a i l a b l e d a t a , a n d r e p o r t e d a g o o d a v e r a g e fit t o the 3 : 1 p r e d i c t i o n , from w h i c h they c o n c l u d e d that they h a d found e v i d e n c e for w o r k e r p o w e r w i n n i n g t h e b a t t l e a g a i n s t q u e e n p o w e r . I t w a s a c l e v e r a t t e m p t to u s e r e a l d a t a to test a h y p o t h e s i s of a k i n d t h a t is often c r i t i c i z e d as u n t e s t a b l e , b u t l i k e o t h e r i n n o v a t i v e first a t t e m p t s it is e a s y to find fault with
it.
Alexander and
Sherman
(1977)
complained
about Trivers and
H a r e ' s h a n d l i n g o f t h e d a t a , a n d also s u g g e s t e d a n a l t e r n a t i v e e x p l a n a t i o n for t h e f e m a l e - b i a s e d s e x r a t i o c o m m o n i n a n t s . T h e i r e x p l a n a t i o n ( ' l o c a l m a t e c o m p e t i t i o n ' ) , like that of T r i v e r s and H a r e , was originally derived f r o m H a m i l t o n , i n this c a s e his p a p e r o n e x t r a o r d i n a r y s e x r a t i o s ( 1 9 6 7 ) . T h i s controversy has had
the g o o d
effect o f s t i m u l a t i n g f u r t h e r w o r k .
A r m s R a c e s and M a n i p u l a t i o n
75
Especially i l l u m i n a t i n g in the c o n t e x t of arms races a n d m a n i p u l a t i o n is the paper by C h a r n o v ( 1 9 7 8 ) , w h i c h is c o n c e r n e d w i t h the origins of eusociality, and
which
introduces
a
potentially
important
version
of the
life/dinner
p r i n c i p l e . H i s a r g u m e n t w o r k s for d i p l o i d a s w e l l a s h a p l o d i p l o i d o r g a n i s m s , a n d I s h a l l c o n s i d e r t h e d i p l o i d c a s e first. C o n s i d e r a m o t h e r w h o s e e l d e r c h i l d r e n h a v e still n o t left t h e nest w h e n t h e n e x t b r o o d h a t c h e s . W h e n t h e t i m e c o m e s for t h e m t o l e a v e t h e nest a n d b e g i n t h e i r o w n r e p r o d u c t i o n , t h e y o u n g h a v e the option, instead, of s t a y i n g b e h i n d a n d h e l p i n g to rear their y o u n g siblings. As is n o w w e l l k n o w n , all other things b e i n g e q u a l such a fledgling should
be g e n e t i c a l l y indifferent b e t w e e n
rearing offspring and
r e a r i n g full s i b l i n g s ( H a m i l t o n 1 9 6 4 a , b ) . B u t s u p p o s e t h e o l d m o t h e r c o u l d exert any m a n i p u l a t i v e p o w e r o v e r the decision of her elder c h i l d r e n : w o u l d she ' p r e f e r ' t h a t t h e y l e a v e a n d r e a r f a m i l i e s o f t h e i r o w n , o r s t a y a n d r e a r her next b r o o d ? O b v i o u s l y that they should stay and rear her next brood, since g r a n d c h i l d r e n a r e h a l f a s v a l u a b l e t o h e r a s c h i l d r e n . ( T h e a r g u m e n t a s i t s t a n d s i s i n c o m p l e t e . I f she m a n i p u l a t e d all h e r c h i l d r e n for t h e w h o l e o f h e r life i n t o r e a r i n g y e t m o r e n o n - p r o d u c i n g c h i l d l a b o u r e r s , h e r g e r m - l i n e w o u l d p e t e r o u t . W e m u s t a s s u m e t h a t she m a n i p u l a t e s s o m e o f f s p r i n g o f t h e same
genetic
type
developing as
into
developing
workers.)
Selection
into
reproductives
will,
then,
selection
in
and
favour such
others
into
manipulative
tendencies in parents. Normally, dutifully
pay
when lip
we
postulate
service
to
favour
counter-selection
on
of manipulation we the
victim
to
resist
m a n i p u l a t i o n . T h e b e a u t y o f C h a r n o v ' s p o i n t i s t h a t i n this c a s e t h e r e w i l l b e no counter-selection. T h e 'arms race' is a w a l k - o v e r b e c a u s e one side, so to speak, doesn't e v e n try. T h e offspring b e i n g m a n i p u l a t e d are, a s w e h a v e a l r e a d y seen, indifferent to w h e t h e r t h e y rear y o u n g siblings or offspring of their o w n ( a g a i n a s s u m i n g all other things e q u a l ) . T h e r e f o r e , a l t h o u g h w e m a y postulate r e v e r s e m a n i p u l a t i o n b y o f f s p r i n g o f p a r e n t s , this i s b o u n d , a t least i n t h e s i m p l e e x a m p l e v i s u a l i z e d b y C h a r n o v , t o b e o u t w e i g h e d b y parental m a n i p u l a t i o n of offspring. T h i s is an a s y m m e t r y to be a d d e d to the list o f p a r e n t a l a d v a n t a g e s offered b y A l e x a n d e r ( 1 9 7 4 ) , b u t I find i t m o r e g e n e r a l l y c o n v i n c i n g t h a n a n y o t h e r s o n t h e list. A t first s i g h t i t m i g h t a p p e a r t h a t C h a r n o v ' s a r g u m e n t d o e s n o t a p p l y t o haplodiploid animals, a n d that w o u l d be a pity since most social insects are h a p l o d i p l o i d . B u t this v i e w i s m i s t a k e n . C h a r n o v h i m s e l f s h o w s this for t h e special assumption that the p o p u l a t i o n has an u n b i a s e d sex ratio, in w h i c h case e v e n in h a p l o d i p l o i d species females are indifferent b e t w e e n r e a r i n g siblings ( r = t h e a v e r a g e o f ¾ a n d ¼ ) a n d r e a r i n g o f f s p r i n g ( r = ½ ) . B u t C r a i g (1980) a n d G r a f e n (in p r e p a r a t i o n ) i n d e p e n d e n t l y s h o w t h a t C h a r n o v d i d n o t e v e n n e e d t o a s s u m e a n u n b i a s e d sex r a t i o . T h e p o t e n t i a l w o r k e r i s still indifferent b e t w e e n r e a r i n g s i b l i n g s a n d r e a r i n g o f f s p r i n g a t a n y c o n c e i v a b l e p o p u l a t i o n sex r a t i o . T h u s s u p p o s e t h e p o p u l a t i o n sex r a t i o i s f e m a l e - b i a s e d ,
76
A r m s Races and Manipulation
e v e n s u p p o s e i t c o n f o r m s t o T r i v e r s a n d H a r e ' s p r e d i c t e d 3 : 1 . S i n c e the w o r k e r is
more
closely
related
t o h e r sister t h a n
to
her
brother or her
o f f s p r i n g o f e i t h e r s e x , i t m i g h t s e e m t h a t she w o u l d ' p r e f e r ' t o r e a r s i b l i n g s o v e r o f f s p r i n g g i v e n s u c h a f e m a l e - b i a s e d sex r a t i o : i s she n o t g a i n i n g m o s t l y v a l u a b l e sisters ( p l u s o n l y a f e w r e l a t i v e l y w o r t h l e s s b r o t h e r s ) w h e n she o p t s for s i b l i n g s ? B u t this r e a s o n i n g n e g l e c t s t h e r e l a t i v e l y g r e a t r e p r o d u c t i v e v a l u e of m a l e s in such a p o p u l a t i o n as a c o n s e q u e n c e of their rarity. T h e w o r k e r m a y not be closely related to e a c h of her brothers, but if males are r a r e i n t h e p o p u l a t i o n a s a w h o l e e a c h o n e o f those b r o t h e r s i s c o r r e s p o n d i n g l y h i g h l y likely t o b e a n a n c e s t o r o f future g e n e r a t i o n s . T h e m a t h e m a t i c s confirm that C h a r n o v ' s conclusion is even more general than
he
suggested.
In
both
diploid
and
haplodiploid
species,
at
any
p o p u l a t i o n sex r a t i o , a n i n d i v i d u a l f e m a l e i s t h e o r e t i c a l l y i n d i f f e r e n t w h e t h e r she h e r s e l f r e a r s o f f s p r i n g o r y o u n g e r s i b l i n g s . S h e i s n o t , h o w e v e r , indifferent w h e t h e r h e r o f f s p r i n g r e a r t h e i r o w n c h i l d r e n o r t h e i r s i b l i n g s : she prefers t h e m to rear their siblings
( h e r offspring)
o v e r their offspring (her g r a n d -
c h i l d r e n ) . T h e r e f o r e i f t h e r e i s a n y q u e s t i o n o f m a n i p u l a t i o n i n this s i t u a t i o n , p a r e n t a l m a n i p u l a t i o n of offspring is m o r e likely t h a n offspring m a n i p u l a tion o f parents. It
might
radically
appear
contradict
that
Charnov's,
Craig's
those
of Trivers
and
and
Hare
Grafen's
on
sex
conclusions
ratios
in
social
H y m e n o p t e r a . T h e s t a t e m e n t t h a t , a t a n y sex r a t i o , a f e m a l e h y m e n o p t e r a n is
indifferent
between
rearing
siblings
and
rearing
offspring,
sounds
t a n t a m o u n t t o s a y i n g t h a t s h e i s a l s o i n d i f f e r e n t t o w h a t t h e sex r a t i o i n h e r nest is. B u t this i s n o t s o . I t i s still t r u e t h a t , g i v e n t h e a s s u m p t i o n o f w o r k e r control over investment evolutionarily
stable
sex
in
male
ratio
and
will
female
not
be
reproductives, necessarily
the
the
resulting
same
as
the
e v o l u t i o n a r i l y s t a b l e sex r a t i o g i v e n q u e e n c o n t r o l . I n this sense a w o r k e r i s n o t i n d i f f e r e n t t o t h e s e x r a t i o : she m a y w e l l w o r k t o shift the sex r a t i o a w a y from w h a t the q u e e n is ' t r y i n g ' to a c h i e v e . T r i v e r s a n d H a r e ' s analysis of the e x a c t nature of the conflict b e t w e e n q u e e n a n d w o r k e r s o v e r t h e sex r a t i o c a n b e e x t e n d e d i n w a y s t h a t further illuminate the c o n c e p t of m a n i p u l a t i o n (e.g. O s t e r & W i l s o n
1978). T h e
following account
I
is d e r i v e d
from
Grafen
(in p r e p a r a t i o n ) .
shall
not
a n t i c i p a t e his c o n c l u s i o n s i n d e t a i l , b u t w i s h t o e m p h a s i z e o n e p r i n c i p l e w h i c h i s e x p l i c i t i n his a n a l y s i s a s w e l l a s i m p l i c i t i n t h a t o f T r i v e r s a n d Hare.
The
question
is
not
'Has
the
"best"
sex
ratio
been
successfully
a c h i e v e d ? ' On the contrary, we m a k e a w o r k i n g assumption that natural s e l e c t i o n h a s p r o d u c e d a r e s u l t , g i v e n s o m e c o n s t r a i n t s , a n d t h e n ask w h a t t h o s e c o n s t r a i n t s a r e (see C h a p t e r 3 ) . I n t h e p r e s e n t c a s e w e f o l l o w T r i v e r s and
H a r e in r e c o g n i z i n g that
the evolutionarily stable sex ratio d e p e n d s
crucially u p o n w h i c h parties to the arms race h a v e practical power, but we r e c o g n i z e a w i d e r range of possible dispositions of p o w e r than they did. In
A r m s Races and Manipulation
effect,
Trivers
and
Hare
deduced
the
consequences
of two
77
alternative
a s s u m p t i o n s a b o u t p r a c t i c a l p o w e r ; firstly t h e a s s u m p t i o n t h a t t h e q u e e n e x e r t s all t h e p o w e r , a n d s e c o n d l y t h e a s s u m p t i o n t h a t t h e w o r k e r s e x e r t a l l the p o w e r . B u t m a n y o t h e r p o s s i b l e a s s u m p t i o n s c o u l d b e m a d e , a n d e a c h g i v e s rise t o a different p r e d i c t i o n o f t h e e v o l u t i o n a r i l y s t a b l e s e x r a t i o . I n other parts o f their p a p e r , i n d e e d , T r i v e r s a n d H a r e c o n s i d e r s o m e o f these, for i n s t a n c e t h e a s s u m p t i o n t h a t w o r k e r s a r e a b l e t o l a y t h e i r o w n m a l e e g g s . Grafen,
like
Bulmer
and
Taylor
(in
preparation),
has
explored
the
c o n s e q u e n c e s o f a s s u m i n g t h a t p o w e r i s divided a s f o l l o w s : t h e q u e e n h a s a b s o l u t e p o w e r o v e r t h e sex o f t h e e g g s t h a t s h e l a y s ; t h e w o r k e r s h a v e absolute p o w e r o v e r feeding the l a r v a e . T h e w o r k e r s c a n thus d e t e r m i n e h o w m a n y o f the a v a i l a b l e female eggs shall d e v e l o p into q u e e n s a n d h o w m a n y into workers. T h e y h a v e the p o w e r to starve the y o u n g of o n e sex or the other, but they h a v e to w o r k w i t h i n the constraint of w h a t the q u e e n g i v e s them in the w a y of eggs. Q u e e n s h a v e the p o w e r to l a y eggs in a n y sex ratio they choose, i n c l u d i n g w i t h h o l d i n g , totally, eggs of o n e sex or the other. B u t , o n c e l a i d , t h o s e e g g s a r e a t t h e m e r c y o f t h e w o r k e r s . A q u e e n m i g h t , for i n s t a n c e , p l a y t h e s t r a t e g y (in t h e g a m e t h e o r y sense) o f l a y i n g o n l y m a l e eggs in a given year. R e l u c t a n t as we m i g h t e x p e c t them to be, the workers h a v e n o o p t i o n b u t t o r e a r t h e i r b r o t h e r s . T h e q u e e n , i n this c a s e , c a n p r e e m p t c e r t a i n w o r k e r s t r a t e g i e s , s u c h a s ' p r e f e r e n t i a l l y feed sisters', s i m p l y b e c a u s e she ' p l a y s ' first. B u t t h e r e a r e o t h e r t h i n g s w o r k e r s c a n d o . Using g a m e theory, Grafen shows that only certain q u e e n strategies are evolutionarily stable replies to p a r t i c u l a r w o r k e r strategies, a n d o n l y certain worker
strategies
are
evolutionarily
stable
replies
to
particular
queen
s t r a t e g i e s . T h e i n t e r e s t i n g q u e s t i o n is, W h a t a r e t h e e v o l u t i o n a r i l y s t a b l e combinations of w o r k e r and q u e e n strategies? It turns out that there is m o r e than one answer, and there can be as m a n y as three e v o l u t i o n a r i l y stable states for a g i v e n set o f p a r a m e t e r s . G r a f e n ' s p a r t i c u l a r c o n c l u s i o n s a r e n o t my concern here, although I will remark that they are interestingly 'counterintuitive'. W h a t is my c o n c e r n is that the e v o l u t i o n a r i l y stable state of the model
population
depends
upon
the
assumptions we
make
a b o u t power.
Trivers and H a r e contrasted two possible absolute assumptions worker
power
versus
absolute
queen
power).
Grafen
(absolute
investigated
one
p l a u s i b l e division o f p o w e r ( q u e e n s h a v e p o w e r o v e r e g g s , w o r k e r s o v e r l a r v a l feeding). But, as I h a v e already noted, numerous other assumptions a b o u t p o w e r could b e m a d e . E a c h assumption generates different predictions a b o u t e v o l u t i o n a r i l y s t a b l e sex r a t i o s , a n d tests o f t h e p r e d i c t i o n s c a n t h e r e f o r e be regarded as p r o v i d i n g e v i d e n c e a b o u t the disposition of p o w e r in the nest. For instance, we m i g h t focus o u r research attention on the e x a c t m o m e n t w h e n a q u e e n ' d e c i d e s ' w h e t h e r to fertilize a g i v e n e g g or not. It is p l a u s i b l e to assume that, since the e v e n t takes p l a c e w i t h i n the q u e e n ' s o w n b o d y , that
78
A r m s R a c e s and M a n i p u l a t i o n
p a r t i c u l a r decision is likely to h a v e b e e n selected to benefit the queen's g e n e s . P l a u s i b l e i t m a y b e , b u t i t i s p r e c i s e l y this k i n d o f a s s u m p t i o n t h a t t h e d o c t r i n e of the e x t e n d e d p h e n o t y p e is g o i n g to call in question. F o r the m o m e n t , w e s i m p l y note the possibility that workers m i g h t m a n i p u l a t e the q u e e n ' s n e r v o u s system, by p h e r o m o n a l or other m e a n s , so as to subvert her b e h a v i o u r in
their g e n e t i c interests.
Similarly,
it is w o r k e r nerves and
m u s c l e s t h a t a r e i m m e d i a t e l y r e s p o n s i b l e for f e e d i n g t h e l a r v a e , b u t w e a r e not, therefore, necessarily entitled to assume that w o r k e r limbs m o v e only in the interests of w o r k e r genes. As is w e l l k n o w n , there is massive p h e r o m o n a l traffic f l o w f r o m q u e e n t o w o r k e r s , a n d i t i s e a s y t o i m a g i n e p o w e r f u l manipulation
of worker
behaviour
by
queens.
The
point
is
that
each
assumption a b o u t p o w e r w h i c h we m i g h t m a k e yields a testable prediction a b o u t sex r a t i o s , a n d i t i s for this i n s i g h t t h a t w e h a v e t o t h a n k T r i v e r s a n d H a r e , n o t for t h e p a r t i c u l a r m o d e l w h o s e p r e d i c t i o n s t h e y h a p p e n e d t o test. It is e v e n c o n c e i v a b l e , in some H y m e n o p t e r a , that males might exert p o w e r . B r o c k m a n n (1980) is m a k i n g an intensive study of m u d - d a u b i n g wasps Trypoxylon politum. T h e s e a r e ' s o l i t a r y ' (as o p p o s e d to t r u l y s o c i a l ) w a s p s , b u t they are not a l w a y s totally alone. As in other sphecids, e a c h female builds h e r o w n n e s t (in this c a s e o u t o f m u d ) , p r o v i s i o n s i t w i t h p a r a l y s e d p r e y ( s p i d e r s ) , l a y s o n e e g g o n t h e p r e y , t h e n seals u p t h e nest a n d b e g i n s the c y c l e a g a i n . In m a n y H y m e n o p t e r a , the female carries a lifetime's supply of s p e r m f r o m o n e b r i e f p e r i o d o f i n s e m i n a t i o n e a r l y i n life. however,
copulate frequently
t h r o u g h o u t a d u l t life.
T . politum f e m a l e s ,
M a l e s haunt female
nests, l o s i n g n o o p p o r t u n i t y t o c o p u l a t e w i t h t h e f e m a l e o n e a c h o f h e r returns to the nest. A m a l e m a y spend hours at a time sitting passively in the nest, p r o b a b l y h e l p i n g t o g u a r d i t a g a i n s t p a r a s i t e s , a n d f i g h t i n g w i t h o t h e r males w h o a t t e m p t t o enter. U n l i k e most m a l e H y m e n o p t e r a then, the m a l e T . politum i s p r e s e n t a t t h e s c e n e o f t h e a c t i o n . M i g h t h e n o t , t h e r e f o r e , b e potentially in a position to influence the sex ratio, in the same kind of w a y as h a s b e e n p o s t u l a t e d for w o r k e r a n t s ? I f m a l e s did exert p o w e r , w h a t w o u l d w e e x p e c t the c o n s e q u e n c e s t o b e ? S i n c e a m a l e p a s s e s a l l his g e n e s o n t o his d a u g h t e r s , a n d n o n e t o his m a t e ' s sons, g e n e s t e n d i n g t o m a k e m a l e s f a v o u r d a u g h t e r s o v e r sons w o u l d b e f a v o u r e d . If m a l e s exerted total p o w e r , c o m p l e t e l y d e t e r m i n i n g the sex ratio o f their m a t e s ' offspring, the c o n s e q u e n c e w o u l d b e o d d . N o males w o u l d b e b o r n in the first g e n e r a t i o n of m a l e p o w e r . As a result, in the f o l l o w i n g y e a r all eggs laid w o u l d be unfertilized and therefore m a l e . T h e population w o u l d therefore oscillate violently and then go extinct ( H a m i l t o n 1967). If males e x e r t e d a l i m i t e d a m o u n t o f p o w e r , less d r a s t i c c o n s e q u e n c e s w o u l d f o l l o w , the situation b e i n g f o r m a ll y a n a l o g o u s to that of the ' d r i v i n g X c h r o m o s o m e ' in
the n o r m a l d i p l o i d g e n e t i c system
(Chapter 8).
In any case a male
h y m e n o p t e r a n , i f h e f o u n d h i m s e l f i n a p o s i t i o n t o i n f l u e n c e t h e sex r a t i o o f his m a t e ' s c h i l d r e n , w o u l d b e e x p e c t e d t o t r y t o d o s o i n a f e m a l e d i r e c t i o n .
A r m s Races and Manipulation
79
H e m i g h t d o this b y t r y i n g t o i n f l u e n c e his m a t e ' s d e c i s i o n w h e t h e r t o r e l e a s e s p e r m f r o m h e r s p e r m a t h e c a . I t i s n o t o b v i o u s h o w h e m i g h t a c t u a l l y d o this, but it is k n o w n that h o n e y b e e queens take longer o v e r l a y i n g a female e g g than a m a l e one, p e r h a p s using the e x t r a time to a c h i e v e fertilization. It would
be
interesting
to
try
experimentally
interrupting
a
queen
in
the
m i d d l e o f e g g - l a y i n g , t o see i f t h e d e l a y i n c r e a s e d t h e c h a n c e o f a f e m a l e e g g emerging. D o m a l e T . politum s h o w a n y b e h a v i o u r t h a t w e m i g h t s u s p e c t o f b e i n g a n a t t e m p t a t s u c h m a n i p u l a t i o n , for e x a m p l e d o t h e y b e h a v e a s i f t r y i n g t o prolong egg-laying? B r o c k m a n n describes a curious b e h a v i o u r pattern called ' h o l d i n g ' . T h i s i s seen a l t e r n a t i n g w i t h c o p u l a t i o n d u r i n g t h e f i n a l m i n u t e s before t h e f e m a l e l a y s h e r e g g . I n a d d i t i o n t o b r i e f c o p u l a t i o n s t h r o u g h o u t the p r o v i s i o n i n g p h a s e o f t h e nest, t h e f i n a l e g g - l a y i n g a n d s e a l i n g u p o f t h e nest i s h e r a l d e d b y a p r o l o n g e d b o u t o f r e p e a t e d c o p u l a t i o n s , w h i c h lasts m a n y m i n u t e s . T h e f e m a l e g o e s h e a d first i n t o t h e v e r t i c a l , o r g a n p i p e shaped
mud
nest,
and
pushes her head up
into
the cluster of p a r a l y s e d
spiders l o d g e d i n the t o p o f t h e nest. H e r a b d o m e n i s f a c i n g t h e e n t r a n c e a t t h e b o t t o m o f t h e nest, a n d i n this p o s i t i o n t h e m a l e c o p u l a t e s w i t h h e r . T h e f e m a l e t h e n t u r n s r o u n d s o t h a t she i s h e a d d o w n w a r d s f a c i n g o u t o f t h e nest, a n d p r o b e s t h e s p i d e r s w i t h t h e tip o f h e r a b d o m e n , a s i f a b o u t t o l a y a n e g g . T h e m a l e m e a n w h i l e ' h o l d s ' h e r h e a d i n his f o r e l e g s for a b o u t h a l f a m i n u t e , grabs her a n t e n n a e a n d pulls her d o w n w a r d s a w a y from the spiders. S h e t h e n turns a r o u n d a n d t h e y c o p u l a t e a g a i n . S h e a g a i n t u r n s t o p r o b e t h e spiders w i t h h e r a b d o m e n , t h e m a l e a g a i n h o l d s h e r h e a d a n d d r a g s h e r d o w n . T h e w h o l e c y c l e r e p e a t s s o m e h a l f d o z e n t i m e s . F i n a l l y , after o n e especially long bout of h e a d - h o l d i n g , the female lays her e g g . O n c e the e g g i s l a i d , its sex i s d e t e r m i n e d . W e h a v e a l r e a d y c o n s i d e r e d t h e hypothetical possibility of w o r k e r ants m a n i p u l a t i n g their m o t h e r ' s nervous system, forcing her to c h a n g e her fertilizing decision in their g e n e t i c interest. Brockmann's
suggestion
is
that
male
T.
politum
might
attempt
similar
subversion, and that the h e a d - h o l d i n g a n d d r a g g i n g b e h a v i o u r m a y be a manifestation o f their m a n i p u l a t i o n t e c h n i q u e . W h e n the m a l e seizes the female's a n t e n n a e a n d drags her a w a y from the spiders w h i c h she is p r o b i n g with her a b d o m e n , is he forcing a p o s t p o n e m e n t of e g g - l a y i n g as a m e a n s of increasing the c h a n c e of the e g g ' s b e i n g fertilized
in
the o v i d u c t ? T h e
p l a u s i b i l i t y o f this s u g g e s t i o n m i g h t d e p e n d o n e x a c t l y w h e r e t h e e g g i s i n t h e female's b o d y d u r i n g the time o f h o l d i n g . O r i s he, a s D r W . D . H a m i l t o n has s u g g e s t e d t o us, b l a c k m a i l i n g t h e f e m a l e b y , i n effect, t h r e a t e n i n g t o b i t e h e r h e a d off unless she p o s t p o n e s e g g - l a y i n g u n t i l after f u r t h e r c o p u l a t i o n ? Perhaps he gains by repeated copulations, simply by flooding the female's i n t e r n a l p a s s a g e s w i t h his s p e r m , t h e r e b y r a i s i n g t h e c h a n c e t h a t t h e e g g w i l l encounter
a
sperm
without
s p e r m a t h e c a by the female.
one
being
deliberately
released
from
the
C l e a r l y these a r e j u s t s u g g e s t i o n s for f u r t h e r
A r m s Races and Manipulation
80
research, and B r o c k m a n n , together with Grafen and others, is following them u p . P r e l i m i n a r y i n d i c a t i o n s , I u n d e r s t a n d , d o n o t s u p p o r t the h y p o t h e s i s t h a t m a l e s a c t u a l l y s u c c e e d i n e x e r t i n g p o w e r o v e r t h e sex r a t i o . T h i s c h a p t e r is i n t e n d e d to b e g i n the process of u n d e r m i n i n g the reader's c o n f i d e n c e i n t h e c e n t r a l t h e o r e m o f t h e selfish o r g a n i s m . T h a t t h e o r e m states t h a t i n d i v i d u a l a n i m a l s a r e e x p e c t e d t o w o r k for t h e g o o d o f t h e i r o w n i n c l u s i v e f i t n e s s , for t h e g o o d o f c o p i e s o f t h e i r o w n g e n e s . T h e c h a p t e r has s h o w n t h a t a n i m a l s a r e q u i t e l i k e l y t o w o r k h a r d a n d v i g o r o u s l y for t h e g o o d o f s o m e o t h e r i n d i v i d u a l ' s g e n e s , a n d t o the d e t r i m e n t o f t h e i r o w n . T h i s i s not necessarily j u s t a t e m p o r a r y d e p a r t u r e from the central t h e o r e m , a brief i n t e r l u d e o f m a n i p u l a t i v e e x p l o i t a t i o n b e f o r e c o u n t e r s e l e c t i o n o n the v i c t i m lineage
redresses
the balance.
I
h a v e suggested
that fundamental asym-
m e t r i e s s u c h a s t h e l i f e / d i n n e r p r i n c i p l e , a n d t h e r a r e - e n e m y effect, w i l l see t o i t t h a t m a n y a r m s r a c e s r e a c h a s t a b l e s t a t e i n w h i c h a n i m a l s o n o n e side p e r m a n e n t l y w o r k for t h e b e n e f i t o f a n i m a l s o n t h e o t h e r s i d e , a n d t o t h e i r o w n d e t r i m e n t ; w o r k hard, energetically, w a n t o n l y against their o w n genetic i n t e r e s t s . W h e n w e see t h e m e m b e r s o f a s p e c i e s c o n s i s t e n t l y b e h a v i n g i n a c e r t a i n w a y , ' a n t i n g ' i n b i r d s o r w h a t e v e r i t is, w e a r e a p t t o s c r a t c h o u r h e a d s a n d w o n d e r h o w t h e b e h a v i o u r benefits the a n i m a l s ' i n c l u s i v e f i t n e s s . H o w d o e s i t b e n e f i t a b i r d t o a l l o w a n t s t o r u n a l l t h r o u g h its f e a t h e r s ? I s i t u s i n g t h e a n t s t o c l e a n i t o f p a r a s i t e s , o r w h a t ? T h e c o n c l u s i o n o f this c h a p t e r is
that
we
might
instead
ask
whose
inclusive
fitness
the
behaviour
is
benefiting!
Is it the a n i m a l ' s o w n , or that of some m a n i p u l a t o r lurking
behind
scenes?
the
In
the
case
of 'anting'
it does
seem
reasonable
to
s p e c u l a t e a b o u t a d v a n t a g e s t o t h e b i r d , b u t p e r h a p s w e s h o u l d g i v e a t least a s i d e w a y s g l a n c e a t t h e p o s s i b i l i t y t h a t i t i s a n a d a p t a t i o n for t h e g o o d o f the ants!
5 T h e Active Germ-line Replicator
In 1957, B e n z e r argued that 'the g e n e ' could no longer continue as a s i n g l e , u n i t a r y c o n c e p t . H e split i t i n t o t h r e e : t h e m u t o n w a s t h e m i n i m u m unit o f m u t a t i o n a l c h a n g e ; the recon w a s the m i n i m u m unit o f r e c o m b i nation; a n d the cistron w a s defined in a w a y that w a s directly a p p l i c a b l e only
to
microorganisms,
but
it
was
effectively
equivalent
to
the
unit
r e s p o n s i b l e for s y n t h e s i z i n g o n e p o l y p e p t i d e c h a i n . I h a v e s u g g e s t e d a d d i n g a fourth u n i t , t h e optimon, t h e u n i t o f n a t u r a l s e l e c t i o n
(Dawkins
Independently,
coined
'selecton'
E.
Mayr
(personal
to serve the same purpose.
communication) T h e optimon
1978b). the
(or s e l e c t o n )
term is
the
' s o m e t h i n g ' t o w h i c h w e refer w h e n w e s p e a k o f a n a d a p t a t i o n a s b e i n g 'for the g o o d o f ' s o m e t h i n g . T h e q u e s t i o n is, w h a t i s t h a t s o m e t h i n g ; w h a t i s t h e optimon? T h e question of w h a t is the 'unit of selection' has b e e n d e b a t e d from t i m e t o t i m e i n the l i t e r a t u r e b o t h o f b i o l o g y ( W y n n e - E d w a r d s 1 9 6 2 ; W i l l i a m s 1966; Lewontin 1970a; Leigh 1977; D a w k i n s 1978a; A l e x a n d e r & Borgia 1 9 7 8 ; W r i g h t 1980) a n d o f p h i l o s o p h y ( H u l l 1 9 8 0 a , b ; W i m s a t t i n p r e p a r a t i o n ) . A t f i r s t s i g h t i t s e e m s a r a t h e r uselessly t h e o l o g i c a l a r g u m e n t . H u l l , indeed,
explicitly
for t h a t ) .
I
regards
it
as
'metaphysical'
m u s t j u s t i f y m y i n t e r e s t i n it.
(though
none
the
worse
W h y does it matter w h a t we
consider to be the unit of selection? T h e r e are v a r i o u s reasons, b u t I shall give only one. I agree with W i l l i a m s (1966), C u r i o (1973) and others that t h e r e is a n e e d to d e v e l o p a s e r i o u s s c i e n c e of a d a p t a t i o n — t e l e o n o m y as P i t t e n d r i g h ( 1 9 5 8 ) c a l l e d it. T h e c e n t r a l t h e o r e t i c a l p r o b l e m o f t e l e o n o m y w i l l b e that o f t h e n a t u r e o f t h e e n t i t y for w h o s e b e n e f i t a d a p t a t i o n s m a y b e said t o exist. A r e t h e y for t h e b e n e f i t o f t h e i n d i v i d u a l o r g a n i s m , for t h e benefit o f the g r o u p o r s p e c i e s o f w h i c h i t i s a m e m b e r , o r for t h e b e n e f i t o f some smaller unit inside the i n d i v i d u a l o r g a n i s m ? As a l r e a d y e m p h a s i z e d in C h a p t e r 3 , this r e a l l y m a t t e r s . A d a p t a t i o n s for t h e g o o d o f a g r o u p w i l l l o o k q u i t e different f r o m a d a p t a t i o n s for the g o o d o f a n i n d i v i d u a l . 81
82
The Active Germ-line Replicator
G o u l d ( 1 9 7 7 b ) sets o u t w h a t , a t f i r s t s i g h t , a p p e a r s t o b e the i s s u e : T h e identification of i n d i v i d u a l s as the unit of selection is a central t h e m e in D a r w i n ' s t h o u g h t . . . I n d i v i d u a l s are the unit of selection; t h e ' s t r u g g l e for e x i s t e n c e ' i s a m a t t e r a m o n g i n d i v i d u a l s . . . I n the last fifteen y e a r s c h a l l e n g e s t o D a r w i n ' s f o c u s o n i n d i v i d u a l s h a v e c o m e from a b o v e and from b e l o w . F r o m a b o v e , Scottish biologist V . C . W y n n e - E d w a r d s raised o r t h o d o x hackles f i f t e e n years a g o b y a r g u i n g t h a t g r o u p s , n o t i n d i v i d u a l s , a r e u n i t s o f s e l e c t i o n , a t least for the
evolution
of social behaviour.
From below,
English
biologist
R i c h a r d D a w k i n s h a s r e c e n t l y r a i s e d m y h a c k l e s w i t h his c l a i m t h a t genes t h e m s e l v e s are units of selection, a n d i n d i v i d u a l s m e r e l y their temporary receptacles.
G o u l d is i n v o k i n g the i d e a of a h i e r a r c h y of levels in the o r g a n i z a t i o n of life. H e sees h i m s e l f a s p e r c h e d o n a n i n t e r m e d i a t e r u n g o f a l a d d e r , w i t h g r o u p selectionists a b o v e a n d g e n e selectionists b e l o w . T h e present chapter a n d t h e n e x t w i l l s h o w t h a t this k i n d o f a n a l y s i s i s false. T h e r e is, o f c o u r s e , a h i e r a r c h y o f l e v e l s o f b i o l o g i c a l o r g a n i z a t i o n (see n e x t c h a p t e r ) , b u t G o u l d i s a p p l y i n g it incorrectly. T h e c o n v e n t i o n a l dispute b e t w e e n g r o u p selection a n d i n d i v i d u a l selection is different in c a t e g o r y from the a p p a r e n t dispute b e t w e e n i n d i v i d u a l s e l e c t i o n a n d g e n e s e l e c t i o n . I t i s w r o n g t o t h i n k o f the three
as
arranged
on
a single-dimensional
ladder,
such
that
words
like
' a b o v e ' a n d ' b e l o w ' h a v e transitive m e a n i n g . I shall s h o w that the well-aired dispute b e t w e e n g r o u p a n d i n d i v i d u a l is c o n c e r n e d w i t h w h a t I shall call 'vehicle selection' and can be regarded as a factual biological dispute about units of n a t u r a l selection. T h e a t t a c k 'from b e l o w ' , on the other hand, is r e a l l y a n a r g u m e n t a b o u t w h a t w e o u g h t t o mean w h e n w e t a l k a b o u t a u n i t of natural selection. T o a n t i c i p a t e t h e c o n c l u s i o n o f these t w o c h a p t e r s , t h e r e a r e t w o w a y s i n w h i c h we c a n c h a r a c t e r i z e natural selection. B o t h are c o r r e c t ; they simply focus on different aspects of the same process. E v o l u t i o n is the external and visible
manifestation
of the
differential
survival
of alternative
replicators
( D a w k i n s 1978a). G e n e s are replicators; organisms and groups of organisms a r e b e s t n o t r e g a r d e d a s r e p l i c a t o r s ; t h e y a r e vehicles i n w h i c h r e p l i c a t o r s travel a b o u t . R e p l i c a t o r selection is the process by w h i c h some replicators s u r v i v e at the e x p e n s e of other replicators. V e h i c l e selection is the process by w h i c h s o m e v e h i c l e s a r e m o r e successful t h a n o t h e r v e h i c l e s i n e n s u r i n g the s u r v i v a l o f their replicators. T h e c o n t r o v e r s y a b o u t g r o u p selection versus i n d i v i d u a l selection is a c o n t r o v e r s y a b o u t the rival claims of t w o suggested k i n d s o f v e h i c l e . T h e c o n t r o v e r s y a b o u t g e n e s e l e c t i o n v e r s u s i n d i v i d u a l (or g r o u p ) s e l e c t i o n i s a c o n t r o v e r s y a b o u t w h e t h e r , w h e n w e t a l k a b o u t a unit o f selection, we o u g h t to m e a n a v e h i c l e at all, or a replicator. M u c h the same
The Active Germ-line Replicator
point has b e e n r e a l i z e d b y the p h i l o s o p h e r D . L . H u l l
(1980a,b),
83
b u t after
s o m e t h o u g h t I p r e f e r t o persist w i t h m y o w n t e r m i n o l o g y r a t h e r t h a n a d o p t his ' i n t e r a c t o r s ' a n d ' e v o l v o r s ' . I d e f i n e a replicator a s a n y t h i n g i n t h e u n i v e r s e o f w h i c h c o p i e s a r e m a d e . Examples are a D N A molecule,
a n d a sheet of p a p e r that is x e r o x e d .
R e p l i c a t o r s m a y b e classified i n t w o w a y s . T h e y m a y b e ' a c t i v e ' o r ' p a s s i v e ' , a n d , c u t t i n g a c r o s s this c l a s s i f i c a t i o n , t h e y m a y b e ' g e r m - l i n e ' o r ' d e a d - e n d ' replicators. A n active replicator i s a n y r e p l i c a t o r w h o s e n a t u r e h a s s o m e i n f l u e n c e o v e r its p r o b a b i l i t y o f b e i n g c o p i e d . F o r e x a m p l e a D N A m o l e c u l e , v i a p r o t e i n s y n t h e s i s , e x e r t s p h e n o t y p i c effects w h i c h i n f l u e n c e w h e t h e r i t i s c o p i e d : this is w h a t n a t u r a l s e l e c t i o n is a l l a b o u t . A passive replicator is a r e p l i c a t o r w h o s e n a t u r e h a s n o i n f l u e n c e o v e r its p r o b a b i l i t y o f b e i n g c o p i e d . A x e r o x e d s h e e t o f p a p e r a t f i r s t s i g h t s e e m s t o b e a n e x a m p l e , b u t s o m e m i g h t a r g u e t h a t its n a t u r e does i n f l u e n c e w h e t h e r i t i s c o p i e d , a n d t h e r e f o r e t h a t i t i s a c t i v e : h u m a n s are m o r e likely to x e r o x s o m e sheets of p a p e r t h a n others, b e c a u s e of w h a t is written on t h e m , a n d these copies are, in their turn, r e l a t i v e l y likely to be copied again. A section of D N A that is never transcribed m i g h t be a g e n u i n e e x a m p l e o f a p a s s i v e r e p l i c a t o r ( b u t see C h a p t e r 9 o n 'selfish D N A ' ) . A germ-line replicator ( w h i c h m a y be a c t i v e or p a s s i v e ) is a r e p l i c a t o r t h a t is potentially the ancestor of an indefinitely long line of d e s c e n d a n t replicators. A g e n e in a g a m e t e is a g e r m - l i n e r e p l i c a t o r . So is a g e n e in o n e of t h e g e r m line cells of a b o d y , a direct mitotic ancestor of a g a m e t e . So is a n y g e n e in Amoeba proteus. S o i s a n R N A m o l e c u l e i n o n e o f O r g e l ' s ( 1 9 7 9 ) t e s t - t u b e s . A dead-end replicator ( w h i c h a l s o m a y be a c t i v e or p a s s i v e ) is a r e p l i c a t o r w h i c h m a y b e c o p i e d a f i n i t e n u m b e r o f t i m e s , g i v i n g rise t o a s h o r t c h a i n o f descendants,
but
which
is
definitely
not
the
potential
ancestor
of an
indefinitely long line o f descendants. M o s t o f the D N A m o l e c u l e s i n o u r bodies are d e a d - e n d replicators. T h e y m a y be the ancestors of a few d o z e n generations of mitotic replication, but they will definitely not be long-term ancestors. A D N A m o l e c u l e in the g e r m - l i n e of an i n d i v i d u a l w h o h a p p e n s to die y o u n g , o r w h o o t h e r w i s e fails t o r e p r o d u c e , s h o u l d n o t b e c a l l e d a d e a d - e n d r e p l i c a t o r . S u c h g e r m - l i n e s a r e , a s i t t u r n s o u t , t e r m i n a l . T h e y fail i n w h a t m a y m e t a p h o r i c a l l y be c a l l e d their aspiration to i m m o r t a l i t y . Differential failure o f this k i n d i s w h a t w e m e a n b y n a t u r a l s e l e c t i o n . B u t w h e t h e r i t s u c c e e d s i n p r a c t i c e o r n o t , a n y g e r m - l i n e r e p l i c a t o r i s potentially i m m o r t a l . I t 'aspires' to i m m o r t a l i t y but in practice is in d a n g e r of failing. A l l the D N A m o l e c u l e s i n fully sterile s o c i a l i n s e c t w o r k e r s , h o w e v e r , a r e t r u e d e a d - e n d replicators. T h e y do not even aspire to replicate indefinitely. W o r k e r s lack a g e r m - l i n e , n o t a s a m a t t e r o f m i s f o r t u n e b u t a s a m a t t e r o f d e s i g n . I n this respect they resemble h u m a n liver cells rather than the s p e r m a t o g o n i a of a human who happens to be celibate. T h e r e m a y be a w k w a r d intermediate
The Active Germ-line Replicator
84
c a s e s , for i n s t a n c e t h e ' s t e r i l e ' w o r k e r w h o b e c o m e s f a c u l t a t i v e l y fertile i f h e r m o t h e r d i e s , a n d t h e Streptocarpus l e a f w h i c h i s not e x p e c t e d t o p r o p a g a t e a n e w p l a n t b u t w h i c h c a n d o s o i f p l a n t e d a s a c u t t i n g . B u t this i s g e t t i n g t h e o l o g i c a l : l e t u s n o t w o r r y precisely h o w m a n y a n g e l s c a n d a n c e o n a p i n ' s head. As I said, the a c t i v e / p a s s i v e distinction cuts across the g e r m - l i n e / d e a d - e n d distinction.
All
four
combinations
are
conceivable.
Particular
interest
a t t a c h e s t o o n e o f t h e four, t h e a c t i v e g e r m - l i n e r e p l i c a t o r , for i t is, I s u g g e s t , t h e ' o p t i m o n ' , t h e u n i t for w h o s e b e n e f i t a d a p t a t i o n s e x i s t . T h e r e a s o n a c t i v e g e r m - l i n e r e p l i c a t o r s a r e i m p o r t a n t u n i t s i s t h a t , w h e r e v e r i n the u n i v e r s e t h e y m a y b e f o u n d , t h e y a r e l i k e l y t o b e c o m e t h e basis for n a t u r a l s e l e c t i o n a n d h e n c e e v o l u t i o n . I f r e p l i c a t o r s exist t h a t a r e a c t i v e , v a r i a n t s o f t h e m with
certain
phenotypic
effects
tend
to
out-replicate
those
with
other
p h e n o t y p i c effects. I f t h e y a r e a l s o g e r m - l i n e r e p l i c a t o r s , these c h a n g e s i n relative frequency can
have long-term, evolutionary impact. T h e world
tends a u t o m a t i c a l l y to b e c o m e populated by germ-line replicators whose a c t i v e p h e n o t y p i c effects a r e s u c h a s t o e n s u r e t h e i r successful r e p l i c a t i o n . I t i s t h e s e p h e n o t y p i c effects t h a t w e see a s a d a p t a t i o n s t o s u r v i v a l . W h e n w e ask whose s u r v i v a l t h e y a r e a d a p t e d t o e n s u r e , t h e f u n d a m e n t a l a n s w e r h a s t o be not the g r o u p , nor the i n d i v i d u a l o r g a n i s m , but the relevant replicators themselves. I h a v e p r e v i o u s l y s u m m e d u p t h e q u a l i t i e s o f a successful r e p l i c a t o r ' i n a slogan
reminiscent
of
the
French
Revolution:
Longevity,
Fecundity,
F i d e l i t y ' ( D a w k i n s 1 9 7 8 a ) . H u l l (1980b) explains the point clearly. R e p l i c a t o r s n e e d n o t last f o r e v e r . T h e y n e e d o n l y last l o n g e n o u g h t o p r o d u c e a d d i t i o n a l replicators [fecundity] that retain their structure largely intact [fidelity]. T h e relevant l o n g e v i t y concerns the retention of structure
through
descent.
Some
entities,
though
structurally
similar, are not copies b e c a u s e they are not related by descent. For e x a m p l e , a l t h o u g h a t o m s of gold are structurally similar, they are not c o p i e s o f o n e a n o t h e r b e c a u s e a t o m s o f g o l d d o n o t g i v e rise t o o t h e r a t o m s of g o l d . C o n v e r s e l y , a large m o l e c u l e c a n break d o w n into successively secondary
smaller
bonds
molecules
are severed.
as
its
quaternary,
A l t h o u g h descent
is
tertiary, present,
and these
successively smaller molecules cannot count as copies because they l a c k the requisite structural similarity. A r e p l i c a t o r m a y b e s a i d t o ' b e n e f i t ' f r o m a n y t h i n g t h a t i n c r e a s e s the n u m b e r o f its d e s c e n d a n t
('germ-line')
copies.
T o the e x t e n t t h a t a c t i v e
g e r m - l i n e r e p l i c a t o r s b e n e f i t f r o m t h e s u r v i v a l o f t h e b o d i e s i n w h i c h t h e y sit, w e m a y e x p e c t t o see a d a p t a t i o n s t h a t c a n b e i n t e r p r e t e d a s for b o d i l y s u r v i v a l . A l a r g e n u m b e r o f a d a p t a t i o n s a r e o f this t y p e . T o t h e e x t e n t t h a t
The Active Germ-line Replicator
85
a c t i v e g e r m - l i n e r e p l i c a t o r s b e n e f i t f r o m t h e s u r v i v a l o f b o d i e s other t h a n those i n w h i c h t h e y sit, w e m a y e x p e c t t o see ' a l t r u i s m ' , p a r e n t a l c a r e , e t c . T o the extent that a c t i v e g e r m - l i n e replicators benefit from the s u r v i v a l o f the g r o u p o f i n d i v i d u a l s i n w h i c h t h e y sit, o v e r a n d a b o v e t h e t w o effects j u s t m e n t i o n e d , w e m a y e x p e c t t o see a d a p t a t i o n s for t h e p r e s e r v a t i o n o f t h e group.
But
all
these
adaptations
will
exist,
fundamentally,
through
differential r e p l i c a t o r s u r v i v a l . T h e b a s i c b e n e f i c i a r y o f a n y a d a p t a t i o n i s t h e active g e r m - l i n e replicator, the o p t i m o n . It is i m p o r t a n t not to forget the ' g e r m - l i n e ' proviso in the specification of the o p t i m o n . T h i s i s t h e p o i n t o f H u l l ' s g o l d a t o m a n a l o g y . K r e b s ( 1 9 7 7 ) a n d I ( D a w k i n s 1 9 7 9 a ) h a v e p r e v i o u s l y c r i t i c i z e d B a r a s h ( 1 9 7 7 ) for s u g g e s t i n g t h a t sterile w o r k e r i n s e c t s c a r e for other workers b e c a u s e t h e y s h a r e g e n e s w i t h t h e m . I w o u l d n o t h a r p o n this a g a i n , h a d t h e e r r o r n o t b e e n r e p e a t e d t w i c e recently in print (Barash 1 9 7 8 ; K i r k 1980). It w o u l d be m o r e correct to say t h a t w o r k e r s c a r e for t h e i r reproductive s i b l i n g s w h o c a r r y g e r m - l i n e c o p i e s o f the c a r i n g g e n e s . I f t h e y c a r e for o t h e r w o r k e r s , i t i s b e c a u s e t h o s e o t h e r w o r k e r s a r e l i k e l y t o w o r k o n b e h a l f o f t h e s a m e r e p r o d u c t i v e s (to w h o m t h e y also a r e k i n ) , not b e c a u s e t h e w o r k e r s a r e k i n t o e a c h o t h e r . W o r k e r g e n e s m a y be active, but they are dead-end, not germ-line replicators. No c o p y i n g process
is infallible.
It is no part of the definition of a
r e p l i c a t o r t h a t its c o p i e s m u s t a l l b e p e r f e c t . I t i s f u n d a m e n t a l t o t h e i d e a o f a replicator that w h e n a mistake or ' m u t a t i o n ' does o c c u r it is passed on to future c o p i e s : t h e m u t a t i o n b r i n g s i n t o e x i s t e n c e a n e w k i n d o f r e p l i c a t o r w h i c h 'breeds true' until there is a further m u t a t i o n . W h e n a sheet of p a p e r is x e r o x e d , a blemish m a y a p p e a r on the c o p y w h i c h w a s not present on the o r i g i n a l . I f the x e r o x c o p y itself i s n o w c o p i e d , the b l e m i s h i s i n c o r p o r a t e d i n t o t h e s e c o n d c o p y ( w h i c h m a y a l s o i n t r o d u c e a n e w b l e m i s h o f its o w n ) . The
important
principle
is
that
in
a
chain
of replicators
errors
are
cumulative. I h a v e p r e v i o u s l y u s e d t h e w o r d ' g e n e ' i n t h e s a m e sense a s I w o u l d n o w use ' g e n e t i c r e p l i c a t o r ' , t o refer t o a g e n e t i c f r a g m e n t w h i c h , for a l l t h a t i t serves a s a u n i t o f s e l e c t i o n , d o e s n o t h a v e r i g i d l y f i x e d b o u n d a r i e s . T h i s h a s not m e t w i t h uniform a p p r o v a l . T h e e m i n e n t m o l e c u l a r biologist G u n t h e r Stent ( 1 9 7 7 ) w r o t e that ' O n e o f the great t r i u m p h s o f 20th c e n t u r y b i o l o g y was the e v e n t u a l u n a m b i g u o u s identification o f the M e n d e l i a n h e r e d i t a r y factor, o r g e n e . . . a s that unit o f genetic m a t e r i a l . . . i n w h i c h the a m i n o a c i d sequence
of a
particular
protein
is
encoded.'
Stent
therefore
violently
objected to my a d o p t i n g the e q u i v a l e n t of W i l l i a m s ' s (1966) definition of a gene as 'that w h i c h segregates and recombines with a p p r e c i a b l e frequency', d e s c r i b i n g it as a ' h e i n o u s t e r m i n o l o g i c a l s i n ' . Such motherly protectiveness towards a rather recently usurped technical t e r m i s n o t u n i v e r s a l a m o n g m o l e c u l a r b i o l o g i s t s , for o n e o f t h e g r e a t e s t o f them has r e c e n t l y w r i t t e n that 'the t h e o r y o f the "selfish g e n e " w i l l h a v e t o
T h e Active Germ-line Replicator
86
b e e x t e n d e d t o a n y stretch o f D N A ' ( C r i c k 1 9 7 9 ) . A n d , a s w e saw a t the beginning
o f this
chapter,
another
molecular
biologist
of the
first
rank,
S e y m o u r B e n z e r ( 1 9 5 7 ) , r e c o g n i z e d the shortcomings of the traditional gene concept,
but
rather
than
grab
the
traditional
word
gene
itself for
one
p a r t i c u l a r m o l e c u l a r usage, he chose the m o r e modest course of coining a useful set o f n e w t e r m s — m u t o n , r e c o n a n d c i s t r o n , t o w h i c h w e m a y a d d the optimon.
Benzer recognized
t h a t a l l t h r e e o f his u n i t s h a d
regarded
as
the
equivalent
to
gene
of
the
earlier
claims to be
literature.
Stent's
u n c o m p r o m i s i n g elevation of the cistron to the h o n o u r is arbitrary, though a d m i t t e d l y it is q u i t e c o m m o n . A m o r e b a l a n c e d v i e w w a s g i v e n by the lamented
W.
T.
Keeton
(1980):
'It
may
seem
strange
that
geneticists
c o n t i n u e t o e m p l o y d i f f e r e n t d e f i n i t i o n s o f t h e g e n e for different p u r p o s e s . T h e fact is that, at the present stage of k n o w l e d g e , o n e definition is more useful i n o n e c o n t e x t a n d a n o t h e r i n a n o t h e r c o n t e x t ; a r i g i d t e r m i n o l o g y w o u l d only h a m p e r the formulation of current ideas and
research
Lewontin
'it i s o n l y t h e
(1970b),
too,
gets
it
right
when
he says
that
aims.'
chromosomes that obey M e n d e l ' s L a w of Independent Assortment, and only t h e n u c l e o t i d e b a s e t h a t i s i n d i v i s i b l e . T h e c o d o n s a n d t h e g e n e s [ c i s t r o n s ] lie in
between,
being
neither unitary nor independent
in
their
behavior at
meiosis.' B u t let u s n o t b e c o m e w o r k e d u p o v e r t e r m i n o l o g y . M e a n i n g s o f w o r d s a r e i m p o r t a n t , b u t not i m p o r t a n t e n o u g h to justify the ill-feeling they sometimes p r o v o k e , as in the present case of Stent (and also as in Stent's passionate and apparently
sincere
denunciation
of my
following
the
standard
modern
f a s h i o n o f r e d e f i n i n g 'selfishness' a n d ' a l t r u i s m ' i n n o n - s u b j e c t i v e s e n s e s — s e e Dawkins,
1 9 8 1 , for a r e p l y t o a s i m i l a r c r i t i c i s m ) . I a m h a p p y t o r e p l a c e
'gene' with 'genetic replicator' where there is any doubt. H e i n o u s t e r m i n o l o g i c a l sins a s i d e , S t e n t m a k e s t h e m o r e i m p o r t a n t p o i n t t h a t m y u n i t i s n o t p r e c i s e l y d e l i m i t e d i n t h e w a y t h a t t h e c i s t r o n is. W e l l , p e r h a p s I s h o u l d s a y ' i n t h e w a y t h a t t h e c i s t r o n o n c e s e e m e d t o b e ' , for the recent
discovery
of 'embedded'
cistrons
in
virus
ΦXi74,
and
of 'exons'
s u r r o u n d i n g ' i n t r o n s ' m u s t b e c a u s i n g a little d i s c o m f o r t t o a n y o n e w h o likes his u n i t s r i g i d . C r i c k ( 1 9 7 9 ) e x p r e s s e s t h e sense o f n o v e l t y w e l l : ' I n t h e last 2 years there has b e e n a mini-revolution in m o l e c u l a r genetics. W h e n I c a m e to California, in S e p t e m b e r 1976, I h a d no idea that a typical gene might be s p l i t i n t o s e v e r a l p i e c e s a n d I d o u b t i f a n y o n e else h a d . ' C r i c k s i g n i f i c a n t l y adds
a
footnote
to
the
word
gene:
'Throughout
this
article
I
have
d e l i b e r a t e l y u s e d t h e w o r d " g e n e " i n a l o o s e sense s i n c e a t this t i m e a n y precise definition called
it
gene
would
(Dawkins
be premature.' 1976a)
or
My unit of selection,
replicator
(1978a)
never
whether had
I
any
p r e t e n s i o n s t o u n i t a r i n e s s a n y w a y . F o r t h e p u r p o s e s for w h i c h i t w a s d e f i n e d , u n i t a r i n e s s i s n o t a n i m p o r t a n t c o n s i d e r a t i o n , a l t h o u g h I r e a d i l y see t h a t i t m i g h t b e i m p o r t a n t for o t h e r p u r p o s e s .
The Active Germ-line Replicator
87
T h e w o r d replicator is purposely defined in a g e n e r a l w a y , so that it does n o t e v e n h a v e t o refer t o D N A . I a m , i n d e e d , q u i t e s y m p a t h e t i c t o w a r d s t h e idea that h u m a n c u l t u r e p r o v i d e s a n e w m i l i e u in w h i c h an entirely different kind of replicator selection c a n go on. In the next c h a p t e r we shall look briefly a t this m a t t e r , a n d a l s o a t t h e c l a i m s o f s p e c i e s g e n e - p o o l s t o b e regarded
as
replicators
'macroevolutionary'
in
trends.
a
large-scale
But in
selection
t h e rest o f this
process
governing
chapter we
shall
be
concerned only with genetic fragments, and 'replicator' will be used as an a b b r e v i a t i o n for ' g e n e t i c r e p l i c a t o r ' . In principle, we m a y consider any portion of c h r o m o s o m e as a potential c a n d i d a t e for the title o f r e p l i c a t o r . N a t u r a l s e l e c t i o n m a y u s u a l l y b e s a f e l y r e g a r d e d a s the d i f f e r e n t i a l s u r v i v a l o f r e p l i c a t o r s r e l a t i v e t o t h e i r a l l e l e s . T h e w o r d allele is n o w a d a y s c u s t o m a r i l y used of cistrons b u t it is c l e a r l y e a s y , a n d i n t h e spirit o f this c h a p t e r , t o g e n e r a l i z e i t t o a n y p o r t i o n o f c h r o m o s o m e . I f w e l o o k a t a p o r t i o n o f c h r o m o s o m e f i v e c i s t r o n s l o n g , its a l l e l e s a r e t h e a l t e r n a t i v e sets o f f i v e c i s t r o n s t h a t e x i s t a t t h e h o m o l o g o u s l o c i o f a l l the c h r o m o s o m e s i n t h e p o p u l a t i o n . A n a l l e l e o f a n a r b i t r a r y s e q u e n c e of twenty-six codons is an alternative homologous sequence of twenty-six codons s o m e w h e r e i n the p o p u l a t i o n . A n y stretch o f D N A , b e g i n n i n g a n d e n d i n g at arbitrarily chosen points on the c h r o m o s o m e , c a n be considered to b e c o m p e t i n g w i t h a l l e l o m o r p h i c s t r e t c h e s for t h e r e g i o n o f c h r o m o s o m e c o n c e r n e d . It further follows that we c a n g e n e r a l i z e the terms h o m o z y g o u s and heterozygous. H a v i n g picked out an arbitrary length of c h r o m o s o m e as our c a n d i d a t e replicator, we look at the h o m o l o g o u s c h r o m o s o m e in the same diploid individual. whole
length
of the
If the t w o c h r o m o s o m e s are i d e n t i c a l o v e r the
replicator,
the
individual
is
homozygous
for
that
r e p l i c a t o r , o t h e r w i s e it is h e t e r o z y g o u s . W h e n I said 'arbitrarily c h o s e n portion of c h r o m o s o m e ' , I r e a l l y m e a n t arbitrarily. T h e twenty-six c o d o n s that I chose m i g h t w e l l span the b o r d e r b e t w e e n t w o c i s t r o n s . T h e s e q u e n c e still p o t e n t i a l l y f i t s t h e d e f i n i t i o n o f a r e p l i c a t o r , i t i s still p o s s i b l e t o t h i n k o f i t a s h a v i n g a l l e l e s , a n d i t still m a y b e thought of as h o m o z y g o u s or h e t e r o z y g o u s to the c o r r e s p o n d i n g portion of the h o m o l o g o u s c h r o m o s o m e i n a d i p l o i d candidate
replicator.
But
a
candidate
genotype.
should
be
This,
regarded
then, as
an
is our actual
r e p l i c a t o r o n l y i f i t possesses s o m e m i n i m u m d e g r e e o f l o n g e v i t y / f e c u n d i t y / fidelity ( t h e r e m a y b e trade-offs a m o n g t h e t h r e e ) . O t h e r t h i n g s b e i n g e q u a l , it is clear that larger candidates will h a v e l o w e r l o n g e v i t y / f e c u n d i t y / f i d e l i t y than smaller ones because they are m o r e v u l n e r a b l e to b e i n g b r o k e n by r e c o m b i n a t i o n e v e n t s . S o , how l a r g e a n d h o w s m a l l a p o r t i o n o f c h r o m o s o m e is it useful to t r e a t as a r e p l i c a t o r ? T h i s d e p e n d s o n t h e a n s w e r t o a n o t h e r q u e s t i o n : ' u s e f u l for w h a t ? ' T h e r e a s o n a r e p l i c a t o r is i n t e r e s t i n g to D a r w i n i a n s is t h a t it is p o t e n t i a l l y i m m o r t a l , o r a t least v e r y l o n g - l i v e d i n t h e f o r m o f c o p i e s . A s u c c e s s f u l
The Active Germ-line Replicator
88
r e p l i c a t o r i s o n e t h a t s u c c e e d s i n l a s t i n g , i n t h e f o r m o f c o p i e s , for a v e r y l o n g time measured in generations, and succeeds in p r o p a g a t i n g m a n y copies of itself. A n u n s u c c e s s f u l r e p l i c a t o r i s o n e t h a t p o t e n t i a l l y m i g h t h a v e b e e n l o n g - l i v e d , b u t in fact failed to survive, say because it caused the successive b o d i e s i n w h i c h i t f o u n d i t s e l f t o b e s e x u a l l y u n a t t r a c t i v e . W e m a y a p p l y the terms 'successful'
and
'unsuccessful'
to a n y arbitrarily defined portion of
c h r o m o s o m e . Its s u c c e s s i s m e a s u r e d r e l a t i v e t o its a l l e l e s , a n d , i f t h e r e i s h e t e r o z y g o s i t y at the r e p l i c a t o r locus in the p o p u l a t i o n , natural selection will change
the
relative
frequencies
of the
allelomorphic
replicators
in
the
population. B u t if the arbitrarily chosen portion of c h r o m o s o m e is very long it is n o t e v e n potentially l o n g - l i v e d in its p r e s e n t f o r m , for it is l i k e l y to be split a p a r t b y c r o s s i n g - o v e r i n a n y g i v e n g e n e r a t i o n , r e g a r d l e s s o f h o w successful i t m a y b e i n m a k i n g a b o d y s u r v i v e a n d r e p r o d u c e . T o g o t o a n e x t r e m e , i f the potential
replicator we
consider
is
a whole
chromosome,
the difference
b e t w e e n a 'successful' a n d an unsuccessful c h r o m o s o m e is of no significance, s i n c e b o t h a r e a l m o s t b o u n d t o b e split b y c r o s s i n g - o v e r b e f o r e t h e n e x t generation in a n y c a s e : their 'fidelity' is zero. This
can
be
put
in
another
way.
An
arbitrarily
defined
length
of
c h r o m o s o m e , o r p o t e n t i a l r e p l i c a t o r , m a y b e said t o h a v e a n e x p e c t e d halflife, m e a s u r e d i n g e n e r a t i o n s . T w o k i n d s o f f a c t o r w i l l affect this half-life. F i r s t l y , r e p l i c a t o r s w h o s e p h e n o t y p i c effects r e n d e r t h e m successful a t t h e i r business
of p r o p a g a t i n g
themselves
will
tend
to
have
a
long
half-life.
R e p l i c a t o r s w i t h l o n g e r half-lives than their alleles will c o m e to p r e d o m i n a t e i n t h e p o p u l a t i o n , a n d this i s t h e f a m i l i a r p r o c e s s o f n a t u r a l s e l e c t i o n . B u t i f w e set s e l e c t i o n p r e s s u r e s o n o n e s i d e , w e c a n s a y s o m e t h i n g a b o u t the halflife
of a
replicator
on
the
basis
o f its
length
alone.
If the
stretch
of
c h r o m o s o m e we c h o o s e to define as o u r r e p l i c a t o r of interest is long, it will t e n d to h a v e a s h o r t e r h a l f - l i f e t h a n a s h o r t e r r e p l i c a t o r , s i m p l y b e c a u s e it is more
likely
to
be
broken
by
crossing-over.
A
very
long
portion
of
c h r o m o s o m e c e a s e s t o d e s e r v e t h e title o f r e p l i c a t o r a t a l l . A c o r o l l a r y i s t h a t a l o n g p o r t i o n o f c h r o m o s o m e , e v e n i f successful i n t e r m s o f its p h e n o t y p i c effects, w i l l n o t b e r e p r e s e n t e d i n m a n y c o p i e s i n t h e p o p u l a t i o n . T h e Y c h r o m o s o m e e x c e p t e d , and d e p e n d i n g upon crossover rates, it seems u n l i k e l y that I share a n y w h o l e c h r o m o s o m e s w i t h a n y other individual.
I
assuredly share
m a n y small
portions of chromosomes with
others, a n d if we choose o u r portions small e n o u g h their likelihood of being s h a r e d b e c o m e s v e r y h i g h i n d e e d . I t i s n o t n o r m a l l y useful t o s p e a k o f interc h r o m o s o m e selection, therefore, since each c h r o m o s o m e is p r o b a b l y unique. N a t u r a l selection is the process by w h i c h replicators c h a n g e in frequency in the p o p u l a t i o n relative to their alleles. If the replicator under consideration i s s o l a r g e t h a t i t i s p r o b a b l y u n i q u e , i t c a n n o t b e said t o h a v e a ' f r e q u e n c y ' to c h a n g e . We must choose our arbitrary portion of c h r o m o s o m e so that it is s m a l l e n o u g h t o last, a t least p o t e n t i a l l y , for m a n y g e n e r a t i o n s b e f o r e b e i n g
The Active Germ-line Replicator
split
by crossing-over; small
enough to h a v e a
'frequency'
89
that can
be
c h a n g e d by n a t u r a l s e l e c t i o n . Is it p o s s i b l e to c h o o s e it loo s m a l l ? I s h a l l r e t u r n t o this q u e s t i o n b e l o w , after a p p r o a c h i n g i t f r o m a n o t h e r d i r e c t i o n . I
shall
make
no
attempt
to
specify
exactly
how
long
a
portion
of
c h r o m o s o m e c a n be permitted to be before it ceases to be usefully r e g a r d e d a s a r e p l i c a t o r . T h e r e i s n o h a r d a n d fast r u l e , a n d w e d o n ' t n e e d o n e . I t depends on the strength of the selection pressure of interest.
We are not
seeking an absolutely rigid definition, but 'a kind of fading-out definition, like t h e d e f i n i t i o n o f " b i g "
or " o l d " ' .
I f the selection pressure w e are
d i s c u s s i n g i s v e r y s t r o n g , t h a t i s i f o n e r e p l i c a t o r m a k e s its possessors v e r y m u c h m o r e l i k e l y t o s u r v i v e a n d r e p r o d u c e t h a n its a l l e l e s d o , t h e r e p l i c a t o r c a n b e q u i t e l a r g e a n d still b e u s e f u l l y r e g a r d e d a s a u n i t t h a t i s n a t u r a l l y selected.
If,
between
a
on
the other hand,
putative
replicator
the difference in survival
and
its
alleles
is
almost
consequences
negligible,
the
replicators under discussion w o u l d h a v e to be quite small if the difference in t h e i r s u r v i v a l v a l u e s i s t o m a k e i t s e l f felt. T h i s i s t h e r a t i o n a l e b e h i n d W i l l i a m s ' s ( 1 9 6 6 , p . 25) d e f i n i t i o n : ' I n e v o l u t i o n a r y t h e o r y , a g e n e c o u l d b e d e f i n e d a s a n y h e r e d i t a r y i n f o r m a t i o n for w h i c h t h e r e i s a f a v o r a b l e o r unfavorable
selection
bias
equal
to
several
or
many
times
its
rate
of
endogenous change.' T h e possibility o f strong linkage d i s e q u i l i b r i u m ( C l e g g 1978) does not w e a k e n the c a s e . I t s i m p l y i n c r e a s e s t h e s i z e o f t h e c h u n k o f g e n o m e t h a t w e can
usefully
treat
as
a
replicator.
If,
which
seems
disequilibrium is so strong that populations contain
doubtful,
linkage
'only a few g a m e t i c
types' ( L e w o n t i n 1974, p. 3 1 2 ) , the effective replicator will be a v e r y large c h u n k o f D N A . W h e n w h a t L e w o n t i n calls lc, the ' c h a r a c t e r i s t i c l e n g t h ' (the 'distance over
which
coupling
is
effective'),
is
only
'a
fraction
of the
c h r o m o s o m e l e n g t h , e a c h g e n e i s o u t o f l i n k a g e e q u i l i b r i u m o n l y w i t h its neighbors but is assorted essentially i n d e p e n d e n t l y of other genes farther a w a y . T h e c h a r a c t e r i s t i c l e n g t h is, i n s o m e s e n s e , t h e u n i t o f e v o l u t i o n s i n c e genes within it are highly correlated. T h e c o n c e p t is a subtle one, h o w e v e r . It does not m e a n that the g e n o m e is b r o k e n up into discrete a d j a c e n t c h u n k s of length lc. E v e r y locus is the center of such a c o r r e l a t e d s e g m e n t a n d e v o l v e s i n l i n k a g e w i t h t h e g e n e s n e a r it' ( L e w o n t i n 1 9 7 4 ) . Similarly, Slatkin linkage
(1972) w r o t e that 'It is clear that w h e n p e r m a n e n t
disequilibrium
is
maintained
in
a
population,
the
higher
order
interactions are i m p o r t a n t a n d the c h r o m o s o m e tends to act as a unit. T h e d e g r e e t o w h i c h this i s t r u e i n a n y g i v e n s y s t e m i s a m e a s u r e o f w h e t h e r t h e g e n e or the c h r o m o s o m e is the unit of selection, or, m o r e a c c u r a t e l y , w h a t parts o f t h e g e n o m e c a n b e said t o b e a c t i n g i n u n i s o n ' . A n d T e m p l e t o n e t al. (1976)
wrote
that
' . . . t h e unit of selection
is a function
in
part of the
intensity of selection: the m o r e intense the selection, the m o r e the w h o l e g e n o m e t e n d s t o h o l d t o g e t h e r a s a u n i t ' . I t w a s i n this s p i r i t t h a t I p l a y f u l l y
90
The Active Germ-line Replicator
c o n t e m p l a t e d t i t l i n g an e a r l i e r w o r k The slightly selfish big bit of chromosome and the even more selfish little bit of chromosome ( D a w k i n s 1 9 7 6 a , p. 3 5 ) . It has often b e e n s u g g e s t e d to me that a fatal o b j e c t i o n to replicator selectionism is the existence of within-cistron crossing-over. If chromosomes w e r e like b e a d necklaces,
the a r g u m e n t runs, w i t h crossing-over a l w a y s
b r e a k i n g the n e c k l a c e b e t w e e n beads and not within them, you might hope to
define
discrete
replicators
in
the
population,
containing
an
integral
n u m b e r of cistrons. B u t since crossover can o c c u r a n y w h e r e (Watson 1976), not just b e t w e e n beads, all hope of defining discrete units disappears. T h i s criticism underestimates the elasticity that the replicator c o n c e p t is p e r m i t t e d b y t h e p u r p o s e for w h i c h i t w a s c o i n e d . A s I h a v e j u s t s h o w n , w e are
not
looking
for
discrete
units,
but
for
pieces
of chromosome
of
i n d e t e r m i n a t e l e n g t h w h i c h b e c o m e m o r e o r less n u m e r o u s t h a n a l t e r n a t i v e s of e x a c t l y the same length. M o r e o v e r , as M a r k R i d l e y reminds me, most w i t h i n - c i s t r o n c r o s s o v e r s a r e , i n a n y c a s e , i n d i s t i n g u i s h a b l e i n t h e i r effects from b e t w e e n - c i s t r o n crossovers. O b v i o u s l y , if the cistron c o n c e r n e d h a p p e n s t o b e h o m o z y g o u s , p a i r e d a t m e i o s i s w i t h a n i d e n t i c a l a l l e l e , t h e t w o sets o f g e n e t i c m a t e r i a l e x c h a n g e d in a crossover will be identical, and the crossover might just
as
well
never have happened.
If the cistrons c o n c e r n e d
are
h e t e r o z y g o u s , differing at one nucleotide locus, a n y within-cistron crossover that occurs 'north' of the h e t e r o z y g o u s nucleotide will be indistinguishable from
one
at
the
northern
boundary
of the
cistron;
crossover 'south' of the h e t e r o z y g o u s nucleotide will
any
within-cistron
be indistinguishable
f r o m o n e a t t h e s o u t h e r n b o u n d a r y o f t h e c i s t r o n . O n l y i f t h e c i s t r o n s differ a t t w o loci, a n d the crossover occurs b e t w e e n t h e m , will it be identifiable as a within-cistron crossover. T h e general point is that it does not particularly matter
where
crossovers
occur
in
relation
to
cistron
boundaries.
What
m a t t e r s i s w h e r e c r o s s o v e r s o c c u r i n r e l a t i o n t o h e t e r o z y g o u s n u c l e o t i d e s . If, for i n s t a n c e , a s e q u e n c e o f six a d j a c e n t c i s t r o n s h a p p e n s t o b e h o m o z y g o u s t h r o u g h o u t a n e n t i r e b r e e d i n g p o p u l a t i o n , a c r o s s o v e r a n y w h e r e w i t h i n the six w i l l b e e x a c t l y e q u i v a l e n t i n effect t o a c r o s s o v e r a t e i t h e r e n d o f t h e six. N a t u r a l s e l e c t i o n c a n c a u s e c h a n g e s i n f r e q u e n c y o n l y a t n u c l e o t i d e loci that
are
heterozygous
in
the
population.
If there
are
large
intervening
c h u n k s o f n u c l e o t i d e s e q u e n c e s t h a t n e v e r differ a m o n g i n d i v i d u a l s , these c a n n o t b e s u b j e c t t o n a t u r a l s e l e c t i o n , for t h e r e i s n o t h i n g t o c h o o s e b e t w e e n t h e m . N a t u r a l s e l e c t i o n m u s t f o c u s its a t t e n t i o n o n h e t e r o z y g o u s n u c l e o t i d e s . It
is
changes
evolutionarily
at
the
single
significant
nucleotide
phenotypic
level
changes,
that
are
although
responsible
for
of
the
course
u n v a r y i n g r e m a i n d e r of the g e n o m e is necessary to p r o d u c e a p h e n o t y p e at a l l . H a v e w e , t h e n , a r r i v e d a t a n a b s u r d l y r e d u c t i o n i s t i c reductio a d absurdum? S h a l l we w r i t e a b o o k c a l l e d
The Selfish Nucleotide? Is a d e n i n e e n g a g e d in a
r e m o r s e l e s s s t r u g g l e a g a i n s t c y t o s i n e for possession o f l o c u s n u m b e r 30004? A t t h e v e r y l e a s t , this i s n o t a h e l p f u l w a y t o e x p r e s s w h a t i s g o i n g o n . I t
T h e Active Germ-line Replicator
91
becomes d o w n r i g h t misleading if it suggests to the student that a d e n i n e at o n e l o c u s is, i n s o m e sense, a l l i e d w i t h a d e n i n e a t o t h e r l o c i , p u l l i n g t o g e t h e r for a n a d e n i n e t e a m . I f t h e r e i s a n y sense i n w h i c h p u r i n e s a n d p y r i m i d i n e s c o m p e t e w i t h e a c h o t h e r for h e t e r o z y g o u s l o c i , t h e s t r u g g l e a t e a c h l o c u s i s i n s u l a t e d from t h e s t r u g g l e a t o t h e r l o c i . T h e m o l e c u l a r b i o l o g i s t m a y , for his o w n important purposes ( C h a r g a f f cited in Judson
1979), count adenines
a n d c y t o s i n e s i n t h e g e n o m e a s a w h o l e , b u t t o d o s o i s a n i d l e e x e r c i s e for t h e student
of natural
selection.
If they
are
competitors
at
all,
they
are
c o m p e t i t o r s for e a c h l o c u s s e p a r a t e l y . T h e y a r e i n d i f f e r e n t t o t h e fate o f t h e i r e x a c t r e p l i c a s a t o t h e r l o c i (see a l s o C h a p t e r 8). B u t t h e r e i s a m o r e i n t e r e s t i n g r e a s o n for r e j e c t i n g t h e c o n c e p t o f t h e selfish n u c l e o t i d e , i n f a v o u r o f s o m e l a r g e r r e p l i c a t i n g e n t i t y . T h e w h o l e p u r p o s e o f o u r s e a r c h for a ' u n i t o f s e l e c t i o n ' i s t o d i s c o v e r a s u i t a b l e a c t o r t o p l a y the l e a d i n g r o l e i n o u r m e t a p h o r s o f p u r p o s e . W e l o o k a t a n a d a p t a t i o n a n d w a n t t o s a y , ' I t i s for t h e g o o d o f . . . ' . O u r q u e s t i n this c h a p t e r i s for t h e right w a y to c o m p l e t e that sentence. It is w i d e l y a d m i t t e d that serious error follows from
t h e u n c r i t i c a l a s s u m p t i o n t h a t a d a p t a t i o n s a r e for t h e g o o d
o f the s p e c i e s . I h o p e I s h a l l b e a b l e t o s h o w , i n this b o o k , t h a t y e t o t h e r t h e o r e t i c a l d a n g e r s , a l b e i t lesser o n e s , a t t e n d t h e a s s u m p t i o n t h a t a d a p t a t i o n s a r e for the g o o d o f the i n d i v i d u a l o r g a n i s m . I a m s u g g e s t i n g h e r e t h a t , s i n c e w e m u s t s p e a k o f a d a p t a t i o n s a s b e i n g for t h e g o o d o f s o m e t h i n g , t h e c o r r e c t something is the a c t i v e , g e r m - l i k e replicator. A n d w h i l e it m a y not be strictly w r o n g t o s a y t h a t a n a d a p t a t i o n i s for t h e g o o d o f t h e n u c l e o t i d e , i.e. t h e s m a l l e s t r e p l i c a t o r r e s p o n s i b l e for t h e p h e n o t y p i c d i f f e r e n c e s c o n c e r n e d i n the e v o l u t i o n a r y c h a n g e , i t i s n o t h e l p f u l t o d o s o . W e a r e g o i n g t o use t h e m e t a p h o r o f p o w e r . A n a c t i v e r e p l i c a t o r i s a c h u n k o f g e n o m e t h a t , w h e n c o m p a r e d t o its a l l e l e s , e x e r t s p h e n o t y p i c p o w e r o v e r its w o r l d , s u c h t h a t its f r e q u e n c y i n c r e a s e s o r d e c r e a s e s r e l a t i v e t o t h a t o f its a l l e l e s .
W h i l e it is u n d o u b t e d l y m e a n i n g f u l
to speak of a
single
n u c l e o t i d e a s e x e r t i n g p o w e r i n this sense, i t i s m u c h m o r e u s e f u l , s i n c e t h e nucleotide only exerts a given type of p o w e r w h e n e m b e d d e d in a larger unit,
to
treat
the larger unit as exerting p o w e r a n d
hence altering
the
f r e q u e n c y o f its c o p i e s . I t m i g h t b e t h o u g h t t h a t t h e s a m e a r g u m e n t c o u l d b e used t o j u s t i f y t r e a t i n g a n e v e n l a r g e r u n i t , s u c h a s t h e w h o l e g e n o m e , a s t h e u n i t t h a t e x e r t s t h e p o w e r . T h i s i s n o t s o , a t l e a s t for s e x u a l g e n o m e s . W e reject the w h o l e s e x u a l g e n o m e a s a c a n d i d a t e r e p l i c a t o r , b e c a u s e o f its h i g h risk o f b e i n g f r a g m e n t e d a t m e i o s i s . T h e s i n g l e n u c l e o t i d e d o e s n o t suffer from this p r o b l e m b u t , a s w e h a v e j u s t s e e n , i t raises a n o t h e r p r o b l e m . I t c a n n o t b e s a i d t o h a v e a p h e n o t y p i c effect e x c e p t i n t h e c o n t e x t o f t h e o t h e r n u c l e o t i d e s t h a t s u r r o u n d i t i n its c i s t r o n . I t i s m e a n i n g l e s s t o s p e a k o f the p h e n o t y p i c effect o f a d e n i n e . B u t i t i s e n t i r e l y s e n s i b l e t o s p e a k o f t h e p h e n o t y p i c effect o f s u b s t i t u t i n g a d e n i n e for c y t o s i n e a t a n a m e d l o c u s w i t h i n a n a m e d cistron. T h e case of a cistron w i t h i n a g e n o m e is not a n a l o g o u s .
The Active Germ-line Replicator
92
U n l i k e a n u c l e o t i d e , a c i s t r o n is l a r g e e n o u g h to h a v e a c o n s i s t e n t p h e n o t y p i c effect, r e l a t i v e l y , t h o u g h n o t c o m p l e t e l y , i n d e p e n d e n t l y o f w h e r e i t lies o n the c h r o m o s o m e ( b u t n o t r e g a r d l e s s o f w h a t o t h e r g e n e s s h a r e its g e n o m e ) . F o r a c i s t r o n , its s e q u e n t i a l c o n t e x t vis-a-vis o t h e r c i s t r o n s is n o t o v e r w h e l m i n g l y i m p o r t a n t i n d e t e r m i n i n g its p h e n o t y p i c effect i n c o m p a r i s o n w i t h its a l l e l e s . F o r a nucleotide's p h e n o t y p i c effect, o n t h e o t h e r h a n d , its s e q u e n t i a l c o n t e x t is e v e r y t h i n g . Bateson
(1981)
expresses
the
following
misgiving
about
'replicator
selection'. A w i n n i n g c h a r a c t e r i s d e f i n e d i n relation t o a n o t h e r o n e w h i l e g e n e t i c r e p l i c a t o r s a r e t h o u g h t a b o u t i n absolute a n d difficulty
is
brought
home
if y o u
ask
atomistic terms. T h e
yourself,
what
exactly
is
D a w k i n s ' r e p l i c a t o r ? Y o u m i g h t a n s w e r : ' T h a t bit o f genetic material m a k i n g the difference b e t w e e n the w i n n i n g a n d losing characters.' Y o u w o u l d h a v e stated that a replicator must be defined in relation to s o m e t h i n g else. A l t e r n a t i v e l y , y o u r r e p l y m i g h t b e :
'A replicator
c o n s i s t s o f a l l t h e g e n e s r e q u i r e d for t h e e x p r e s s i o n o f t h e s u r v i v i n g character'. In that case y o u are saddled with a c o m p l e x and unwieldy concept. Either w a y your answer would show how misleading it is to think of replicators as the atoms of e v o l u t i o n .
I
certainly
would join
Bateson
in
rejecting
the
second
o f his
two
a l t e r n a t i v e a n s w e r s , t h e u n w i e l d l y o n e . T h e f i r s t o f his a l t e r n a t i v e s , o n the other h a n d , expresses e x a c t l y my position, and
I do not share Bateson's
m i s g i v i n g s a b o u t it. F o r m y p u r p o s e s a g e n e t i c r e p l i c a t o r i s d e f i n e d b y r e f e r e n c e to its a l l e l e s , b u t this is n o t a w e a k n e s s of t h e c o n c e p t . O r , if it is d e e m e d t o b e a w e a k n e s s , i t i s a w e a k n e s s t h a t afflicts t h e w h o l e s c i e n c e o f p o p u l a t i o n g e n e t i c s , n o t j u s t the p a r t i c u l a r idea of g e n e t i c units of selection. It is a f u n d a m e n t a l t r u t h , t h o u g h it is n o t a l w a y s r e a l i z e d , t h a t whenever a geneticist studies a g e n e 'for' a n y p h e n o t y p i c c h a r a c t e r , he is a l w a y s referring to a difference b e t w e e n t w o a l l e l e s . T h i s is a r e c u r r i n g t h e m e t h r o u g h o u t this book. T o p r o v e t h e p u d d i n g , let m e s h o w h o w e a s y i t i s t o u s e t h e g e n e a s a c o n c e p t u a l unit of selection, w h i l e a d m i t t i n g that it is o n l y defined by c o m p a r i s o n w i t h its a l l e l e s . I t i s n o w a c c e p t e d t h a t a p a r t i c u l a r m a j o r g e n e for d a r k c o l o r a t i o n i n t h e p e p p e r e d m o t h Biston betularia h a s i n c r e a s e d i n frequency
in
industrial
areas
because
it
produces
phenotypes
that
are
superior in industrial areas ( K e t t l e w e l l 1 9 7 3 ) . At the s a m e time, we h a v e to a d m i t t h a t this g e n e i s o n l y o n e o f t h o u s a n d s t h a t a r e n e c e s s a r y i n o r d e r for t h e d a r k c o l o r a t i o n t o s h o w itself. A m o t h c a n n o t h a v e d a r k w i n g s unless i t has w i n g s , a n d it c a n n o t h a v e w i n g s unless it has h u n d r e d s of genes and hundreds
of
equally
necessary
environmental
factors.
But
this
is
all
The Active Germ-line Replicator
93
i r r e l e v a n t . T h e difference b e t w e e n t h e carbonaria a n d t h e typica p h e n o t y p e c a n still
be d u e
to
a difference
at
one
locus,
even
though
the p h e n o t y p e s
t h e m s e l v e s c o u l d n o t exist w i t h o u t t h e p a r t i c i p a t i o n o f t h o u s a n d s o f g e n e s . A n d it is the s a m e difference that is the basis of the n a t u r a l selection. B o t h g e n e t i c i s t s and n a t u r a l s e l e c t i o n a r e c o n c e r n e d w i t h d i f f e r e n c e s ! H o w e v e r c o m p l e x the g e n e t i c basis o f f e a t u r e s t h a t a l l m e m b e r s o f a s p e c i e s h a v e i n common, n a t u r a l s e l e c t i o n i s c o n c e r n e d w i t h d i f f e r e n c e s . E v o l u t i o n a r y c h a n g e is a l i m i t e d set of s u b s t i t u t i o n s at i d e n t i f i a b l e l o c i . F u r t h e r difficulties w i l l b e d e a l t w i t h i n t h e n e x t c h a p t e r . M e a n w h i l e , I e n d this c h a p t e r w i t h a s m a l l d i v e r s i o n w h i c h m a y b e h e l p f u l i n i l l u s t r a t i n g the r e p l i c a t o r o r ' g e n e ' s - e y e ' v i e w o f e v o l u t i o n . A n a p p e a l i n g a s p e c t o f t h e view appears if we look b a c k w a r d s in time. T h e replicators in frequent existence t o d a y constitute a relatively successful subset of those that h a v e existed in the past. A g i v e n replicator in me c o u l d , in theory, be traced b a c k w a r d s through a straight line of ancestors. T h e s e ancestors, and the e n v i r o n m e n t s t h a t t h e y p r o v i d e d for t h e r e p l i c a t o r , c a n b e r e g a r d e d a s t h e replicator's 'past e x p e r i e n c e ' . The
past
experience of autosomal
genetic
fragments
in
a
species
is,
s t a t i s t i c a l l y s p e a k i n g , s i m i l a r . I t consists o f a n e n s e m b l e o f t y p i c a l s p e c i e s bodies, approximately 50 per cent male and 50 per cent female bodies, bodies
which
grew
through
a
wide
spectrum
of ages
at
least
up
to
r e p r o d u c t i v e a g e ; a n d it includes a g o o d r a n d o m shuffling of ' c o m p a n i o n ' g e n e s a t o t h e r l o c i . T h e g e n e s t h a t exist t o d a y t e n d t o b e t h e o n e s t h a t a r e good at surviving in that statistical e n s e m b l e of bodies, a n d in c o m p a n y w i t h that statistical e n s e m b l e of c o m p a n i o n genes. As we shall see, it is selection in f a v o u r o f the q u a l i t i e s n e e d e d for s u r v i v a l i n company w i t h o t h e r , s i m i l a r l y s e l e c t e d , g e n e s , t h a t g i v e s rise t o t h e a p p e a r a n c e o f ' c o a d a p t e d g e n o m e s ' . I shall s h o w i n C h a p t e r 1 3 t h a t this i s a m u c h m o r e i l l u m i n a t i n g i n t e r p r e t a t i o n o f the p h e n o m e n o n o f c o a d a p t a t i o n t h a n its a l t e r n a t i v e , t h a t ' t h e c o a d a p t e d g e n o m e is the true unit of selection'. P r o b a b l y no t w o genes in an organism h a v e identical past experiences, though a linked pair m a y c o m e close, and, mutants aside, all the genes on a Y c h r o m o s o m e h a v e t r a v e l l e d t o g e t h e r t h r o u g h t h e s a m e set o f b o d i e s for a large n u m b e r of generations. But the e x a c t n a t u r e of a g e n e ' s past e x p e r i e n c e i s o f less i n t e r e s t t h a n t h e g e n e r a l i z a t i o n s o n e c a n m a k e a b o u t t h e p a s t e x p e r i e n c e s o f a l l g e n e s t h a t exist t o d a y . F o r i n s t a n c e , h o w e v e r v a r i a b l e t h e set o f m y a n c e s t o r s m a y b e , t h e y a l l h a d i n c o m m o n t h a t t h e y s u r v i v e d a t least t o r e p r o d u c t i v e a g e , t h e y c o p u l a t e d h e t e r o s e x u a l l y a n d w e r e f e r t i l e . T h e s a m e g e n e r a l i z a t i o n c a n n o t b e m a d e a b o u t t h e h i s t o r i c a l set o f b o d i e s that were not my ancestors. T h e bodies that p r o v i d e d the past e x p e r i e n c e of existing genes are a n o n - r a n d o m subset of all the b o d i e s that h a v e e v e r existed. T h e g e n e s t h a t exist t o d a y r e f l e c t t h e set o f e n v i r o n m e n t s t h a t t h e y h a v e
94
The Active Germ-line Replicator
e x p e r i e n c e d in the past. T h i s includes the internal e n v i r o n m e n t s p r o v i d e d by t h e b o d i e s t h e g e n e s h a v e i n h a b i t e d , a n d also e x t e r n a l e n v i r o n m e n t s , d e s e r t , forest, s e a s h o r e ,
predators,
p a r a s i t e s , s o c i a l c o m p a n i o n s , e t c . T h i s is, o f
c o u r s e , n o t b e c a u s e t h e e n v i r o n m e n t s h a v e i m p r i n t e d t h e i r q u a l i t i e s o n the g e n e s — t h a t w o u l d b e L a m a r c k i s m (see C h a p t e r 9 ) — b u t b e c a u s e the g e n e s t h a t e x i s t t o d a y a r e a s e l e c t e d set, a n d t h e q u a l i t i e s t h a t m a d e t h e m s u r v i v e reflect t h e q u a l i t i e s o f t h e e n v i r o n m e n t s i n w h i c h t h e y s u r v i v e d . I said t h a t a g e n e ' s e x p e r i e n c e consists of t i m e s p e n t in a p p r o x i m a t e l y 50 p e r c e n t m a l e a n d 5 0 p e r c e n t f e m a l e b o d i e s , b u t this i s n o t , o f c o u r s e , true o f genes
on
sex
chromosomes.
In
mammals,
assuming
no
Y-chromosome
c r o s s i n g - o v e r , a g e n e on a Y c h r o m o s o m e h a s e x p e r i e n c e d o n l y m a l e b o d i e s , a n d a g e n e o n a n X c h r o m o s o m e h a s s p e n t t w o - t h i r d s o f its h i s t o r y i n f e m a l e bodies and one-third in m a l e bodies. In birds, Y - c h r o m o s o m e genes h a v e e x p e r i e n c e d o n l y f e m a l e bodies, a n d in p a r t i c u l a r cases such as c u c k o o s we c a n s a y s o m e t h i n g f u r t h e r . F e m a l e Cuculus canorus a r e d i v i d e d i n t o ' g e n t e s ' , e a c h g e n s p a r a s i t i z i n g a d i f f e r e n t s p e c i e s o f host ( L a c k 1 9 6 8 ) . A p p a r e n t l y e a c h f e m a l e l e a r n s t h e q u a l i t i e s o f h e r o w n foster p a r e n t s a n d t h e i r nest, a n d returns w h e n adult to parasitize the same species. M a l e s do not seem to discriminate as to gens in their c h o i c e of m a t e , and therefore they act as v e h i c l e s for g e n e f l o w b e t w e e n g e n t e s . O f t h e g e n e s i n a f e m a l e c u c k o o , therefore, those on a u t o s o m e s a n d the X c h r o m o s o m e h a v e p r o b a b l y had r e c e n t e x p e r i e n c e o f a l l g e n t e s i n t h e p o p u l a t i o n , a n d b e e n ' r e a r e d ' b y foster parents b e l o n g i n g to all the species parasitized by the c u c k o o p o p u l a t i o n . But
the
Y
chromosome,
uniquely,
is
confined
for
long
sequences
of
g e n e r a t i o n s t o o n e g e n s a n d o n e foster s p e c i e s . O f a l l t h e g e n e s s i t t i n g i n a r o b i n ' s nest, o n e s u b s e t — r o b i n g e n e s a n d c u c k o o Y - c h r o m o s o m e g e n e s ( a n d robin
flea
Another
genes)—has
subset—cuckoo
sat
in
robins'
autosomal
nests
and
for
many
generations
X-chromosome
back.
genes—has
ex-
p e r i e n c e d a m i x t u r e o f nests. O f c o u r s e t h e f i r s t s u b s e t s h a r e o n l y p a r t o f their e x p e r i e n c e , a l o n g series o f r o b i n nests. I n o t h e r a s p e c t s o f t h e i r e x p e r i e n c e , cuckoo Y - c h r o m o s o m e genes will have more in c o m m o n with other cuckoo genes
than
with
robin
genes.
But
a s far a s
certain
particular selection
p r e s s u r e s f o u n d i n nests a r e c o n c e r n e d , c u c k o o Y - c h r o m o s o m e g e n e s h a v e more in c o m m o n with robin genes than with c u c k o o autosome genes. It is n a t u r a l , t h e n , t h a t c u c k o o Y c h r o m o s o m e s s h o u l d h a v e e v o l v e d t o reflect their peculiar experience, w h i l e other c u c k o o genes simultaneously evolved to reflect their m o r e g e n e r a l e x p e r i e n c e — a kind of incipient intragenomic ' s p e c i a t i o n ' a t t h e c h r o m o s o m a l l e v e l . I t is, i n d e e d , w i d e l y a s s u m e d for this r e a s o n t h a t g e n e s for foster s p e c i e s - s p e c i f i c e g g m i m i c r y m u s t b e c a r r i e d o n t h e Y c h r o m o s o m e , w h i l e g e n e s for g e n e r a l p a r a s i t i c a d a p t a t i o n s m i g h t b e carried on any chromosome. I a m n o t s u r e w h e t h e r t h e f a c t h a s s i g n i f i c a n c e , b u t this b a c k w a r d s w a y o f l o o k i n g s h o w s X c h r o m o s o m e s , t o o , to h a v e a p e c u l i a r h i s t o r y . A g e n e on an
The Active Germ-line Replicator
95
autosome in a female c u c k o o is as likely to h a v e c o m e from the father as from the m o t h e r , i n w h i c h l a t t e r c a s e i t e x p e r i e n c e s t h e s a m e h o s t s p e c i e s for t w o g e n e r a t i o n s r u n n i n g . A g e n e on an X c h r o m o s o m e in a f e m a l e c u c k o o is b o u n d to h a v e c o m e from the father, a n d therefore is not e s p e c i a l l y likely to e x p e r i e n c e the s a m e host species t w o g e n e r a t i o n s r u n n i n g . A statistical 'runs test' o n the s e q u e n c e o f foster s p e c i e s e x p e r i e n c e d b y a n a u t o s o m a l g e n e w o u l d t h e r e f o r e r e v e a l a s l i g h t r u n s effect, g r e a t e r t h a n t h a t for a g e n e o n a n X c h r o m o s o m e , a n d m u c h less t h a n t h a t for a g e n e on a Y c h r o m o s o m e . In any animal, an inverted portion of c h r o m o s o m e m a y resemble a Y c h r o m o s o m e i n b e i n g u n a b l e t o cross o v e r . T h e ' e x p e r i e n c e ' o f a n y p a r t o f the ' i n v e r s i o n s u p e r g e n e ' t h e r e f o r e r e p e a t e d l y i n c l u d e s t h e o t h e r p a r t s o f t h e supergene
and
their
phenotypic
consequences.
A
habitat
selection
gene
a n y w h e r e in such a supergene, say a g e n e that m a k e s i n d i v i d u a l s c h o o s e d r y microclimates,
would
then
provide
a consistent
successive generations of the w h o l e s u p e r g e n e .
habitat
'experience'
for
Thus a given gene may
' e x p e r i e n c e ' c o n s i s t e n t l y d r y h a b i t a t s for t h e s a m e k i n d o f r e a s o n a s a g e n e o n a c u c k o o ' s Y c h r o m o s o m e c o n s i s t e n t l y e x p e r i e n c e s m e a d o w - p i p i t nests. T h i s will
provide
a
consistent
selection
pressure
bearing
upon
that
locus,
favouring alleles that are a d a p t e d to a d r y h a b i t a t in the s a m e w a y as alleles for m i m i c k i n g m e a d o w - p i p i t e g g s a r e f a v o u r e d i n Y c h r o m o s o m e s o f f e m a l e cuckoos o f the m e a d o w - p i p i t gens. T h i s p a r t i c u l a r inversion s u p e r g e n e w i l l t e n d t o b e f o u n d for g e n e r a t i o n s i n d r y h a b i t a t s , e v e n t h o u g h t h e rest o f t h e g e n o m e m a y b e r a n d o m l y shuffled o v e r t h e w h o l e r a n g e o f h a b i t a t s a v a i l a b l e t o the s p e c i e s . M a n y d i f f e r e n t l o c i o n t h e i n v e r t e d p o r t i o n o f c h r o m o s o m e m a y therefore c o m e to be a d a p t e d to a d r y c l i m a t e , a n d a g a i n s o m e t h i n g a k i n t o i n t r a g e n o m i c i n c i p i e n t s p e c i a t i o n m a y g o o n . I find this b a c k w a r d s w a y of l o o k i n g at the past ' e x p e r i e n c e ' of genetic replicators helpful. Germ-line replicators,
then,
are units
t h a t a c t u a l l y s u r v i v e o r fail
to
survive, the difference constituting n a t u r a l selection. A c t i v e replicators h a v e s o m e effect o n t h e w o r l d , w h i c h i n f l u e n c e s t h e i r c h a n c e s o f s u r v i v i n g . I t i s t h e effects o n t h e w o r l d o f s u c c e s s f u l a c t i v e g e r m - l i n e r e p l i c a t o r s t h a t w e see a s adaptations.
Fragments of D N A qualify as
active
germ-line
replicators.
W h e r e t h e r e i s s e x u a l r e p r o d u c t i o n , these f r a g m e n t s m u s t n o t b e d e f i n e d t o o large if they are to retain the p r o p e r t y of self-duplication. A n d they must not be defined too small if they are to be usefully r e g a r d e d as a c t i v e . I f t h e r e w e r e sex b u t n o c r o s s i n g - o v e r , e a c h c h r o m o s o m e w o u l d b e a r e p l i c a t o r , a n d w e s h o u l d s p e a k o f a d a p t a t i o n s a s b e i n g for t h e g o o d o f t h e c h r o m o s o m e . If there is no sex we c a n , by the s a m e token, treat the entire g e n o m e of an a s e x u a l o r g a n i s m as a r e p l i c a t o r . B u t t h e o r g a n i s m i t s e l f is not a r e p l i c a t o r . T h i s i s for t w o q u i t e d i s t i n c t r e a s o n s w h i c h s h o u l d n o t b e c o n f u s e d w i t h e a c h o t h e r . T h e first r e a s o n f o l l o w s f r o m t h e a r g u m e n t s d e v e l o p e d i n this
chapter,
and
applies
only
where
there
is
sexual
reproduction
and
m e i o s i s : m e i o s i s a n d s e x u a l fusion see t o i t t h a t n o t e v e n o u r g e n o m e s a r e
96
The Active Germ-line Replicator
replicators, so we ourselves are not replicators either. T h e second reason a p p l i e s t o a s e x u a l a s w e l l a s s e x u a l r e p r o d u c t i o n . I t w i l l b e e x p l a i n e d i n the n e x t c h a p t e r , w h i c h goes o n t o discuss w h a t o r g a n i s m s , a n d also groups o f o r g a n i s m s , are, g i v e n t h a t t h e y a r e n o t r e p l i c a t o r s .
6 O r g a n i s m s , G r o u p s and M e m e s : Replicators or V e h i c l e s ?
I h a v e m a d e s o m u c h o f t h e f r a g m e n t i n g effects o f m e i o s i s a s a r e a s o n for n o t r e g a r d i n g s e x u a l l y r e p r o d u c e d o r g a n i s m s a s r e p l i c a t o r s , t h a t i t i s t e m p t i n g t o see this a s t h e o n l y r e a s o n . I f this w e r e t r u e , i t s h o u l d f o l l o w t h a t asexually
reproduced
organisms
are
true
replicators,
and
that
where
r e p r o d u c t i o n i s a s e x u a l w e c o u l d l e g i t i m a t e l y s p e a k o f a d a p t a t i o n s a s 'for t h e g o o d o f t h e o r g a n i s m ' . B u t t h e f r a g m e n t i n g effect o f m e i o s i s i s n o t t h e o n l y r e a s o n for d e n y i n g t h a t o r g a n i s m s a r e t r u e r e p l i c a t o r s .
T h e r e is a m o r e
fundamental reason, and it applies to asexual organisms as m u c h as to sexual ones. To regard an organism as a replicator, even an asexual organism like a f e m a l e stick i n s e c t , i s t a n t a m o u n t t o a v i o l a t i o n o f t h e ' c e n t r a l d o g m a ' o f t h e non-inheritance replicator,
in
of a c q u i r e d that
we
may
characteristics. lay
out
a
A
stick
sequence
insect
consisting
looks
like
a
of daughter,
g r a n d d a u g h t e r , g r e a t - g r a n d d a u g h t e r , etc., in w h i c h e a c h a p p e a r s to be a r e p l i c a o f the p r e c e d i n g o n e i n t h e series. B u t s u p p o s e a f l a w o r b l e m i s h a p p e a r s s o m e w h e r e i n t h e c h a i n , s a y a stick i n s e c t i s u n f o r t u n a t e e n o u g h t o lose a l e g . T h e b l e m i s h m a y last for t h e w h o l e o f h e r l i f e t i m e , b u t i t i s n o t p a s s e d o n t o t h e n e x t l i n k i n t h e c h a i n . E r r o r s t h a t affect stick i n s e c t s b u t n o t t h e i r g e n e s a r e n o t p e r p e t u a t e d . N o w l a y o u t a p a r a l l e l series c o n s i s t i n g o f daughter's g e n o m e , etc.
genome,
granddaughter's
genome,
great-granddaughter's
I f a b l e m i s h a p p e a r s s o m e w h e r e a l o n g this series i t w i l l b e
passed o n t o all s u b s e q u e n t l i n k s i n t h e c h a i n . I t m a y a l s o b e r e f l e c t e d i n t h e b o d i e s o f all s u b s e q u e n t links i n the c h a i n , b e c a u s e i n e a c h g e n e r a t i o n t h e r e are c a u s a l a r r o w s l e a d i n g f r o m g e n e s t o b o d y . B u t t h e r e i s n o c a u s a l a r r o w l e a d i n g from b o d y to genes. No part of the stick insect's p h e n o t y p e is a r e p l i c a t o r . N o r i s h e r b o d y a s a w h o l e . I t i s w r o n g t o s a y t h a t 'just a s g e n e s c a n pass o n t h e i r s t r u c t u r e i n g e n e l i n e a g e s , o r g a n i s m s c a n pass o n t h e i r structure in organism lineages'. I a m s o r r y i f I a m a b o u t t o l a b o u r this a r g u m e n t , b u t I f e a r i t w a s m y failure t o b e c l e a r a b o u t i t b e f o r e t h a t l e d t o a n u n n e c e s s a r y d i s a g r e e m e n t 97
O r g a n i s m s , G r o u p s and M e m e s : Replicators or Vehicles?
98
w i t h B a t e s o n , a d i s a g r e e m e n t w h i c h i t i s w o r t h g o i n g t o s o m e t r o u b l e t o sort out.
Bateson
(1978b)
made
the
development are necessary but
point
that
n o t sufficient.
genetic A gene
determinants may
'program'
of a
p a r t i c u l a r bit of b e h a v i o u r ' w i t h o u t it b e i n g the o n l y thing to do so'. He goes on: D a w k i n s a c c e p t s a l l this b u t t h e n r e v e a l s his u n c e r t a i n t y a b o u t w h i c h l a n g u a g e h e i s u s i n g b y i m m e d i a t e l y g i v i n g s p e c i a l s t a t u s b a c k t o the gene as the p r o g r a m m e r . environmental
temperature
C o n s i d e r a case
in
which
during development
the a m b i e n t
is crucial
for
the
expression of a particular p h e n o t y p e . If the temperature changes by a few degrees the s u r v i v a l m a c h i n e is b e a t e n by a n o t h e r one. W o u l d not that g i v e as m u c h status to a necessary t e m p e r a t u r e v a l u e as to a necessary
gene?
The
temperature
value
is
also
required
for
the
e x p r e s s i o n o f a p a r t i c u l a r p h e n o t y p e . I t i s a l s o s t a b l e ( w i t h i n limits) f r o m o n e g e n e r a t i o n t o t h e n e x t . I t m a y e v e n b e t r a n s m i t t e d from o n e g e n e r a t i o n t o t h e n e x t i f t h e s u r v i v a l m a c h i n e m a k e s a nest for its offspring. I n d e e d , using D a w k i n s ' o w n style of teleological a r g u m e n t o n e c o u l d c l a i m t h a t t h e b i r d i s t h e nest's w a y o f m a k i n g a n o t h e r nest [Bateson 1978b]. I r e p l i e d t o B a t e s o n , b u t d i d s o t o o b r i e f l y , p i c k i n g o n t h e last r e m a r k a b o u t b i r d s ' nests a n d s a y i n g , ' A nest i s n o t a t r u e r e p l i c a t o r b e c a u s e a [ n o n g e n e t i c ] " m u t a t i o n " w h i c h o c c u r s i n t h e c o n s t r u c t i o n o f a nest, for e x a m p l e the a c c i d e n t a l i n c o r p o r a t i o n of a pine needle instead of the usual grass, is not p e r p e t u a t e d in future " g e n e r a t i o n s of nests".
Similarly, protein molecules
are not replicators, nor is messenger R N A ' (Dawkins 1978a). Bateson had taken the c a t c h p h r a s e a b o u t a bird being a gene's w a y of m a k i n g another g e n e , a n d i n v e r t e d it, s u b s t i t u t i n g ' n e s t ' for ' g e n e ' . B u t the p a r a l l e l i s n o t a v a l i d o n e . T h e r e i s a c a u s a l a r r o w g o i n g f r o m g e n e t o b i r d , b u t n o n e i n the reverse direction.
A changed gene may
perpetuate
itself b e t t e r
than
its
u n m u t a t e d a l l e l e . A c h a n g e d nest w i l l d o n o s u c h t h i n g u n l e s s , o f c o u r s e , the c h a n g e is d u e to a c h a n g e d g e n e , in w h i c h case it is the g e n e that is p e r p e t u a t e d , n o t t h e nest. A nest, l i k e a b i r d , is a g e n e ' s w a y of m a k i n g another gene. Bateson
is
worried
that
I
seem
to
give
'special
status'
to
genetic
d e t e r m i n a n t s o f b e h a v i o u r . H e fears t h a t a n e m p h a s i s o n t h e g e n e a s the e n t i t y for w h o s e b e n e f i t o r g a n i s m s l a b o u r , r a t h e r t h a n t h e o t h e r w a y a r o u n d , leads to an u n d u e e m p h a s i s on the i m p o r t a n c e of genetic as opposed to e n v i r o n m e n t a l d e t e r m i n a n t s o f d e v e l o p m e n t . T h e a n s w e r t o this i s t h a t w h e n w e a r e t a l k i n g a b o u t development i t i s a p p r o p r i a t e t o e m p h a s i z e n o n - g e n e t i c a s w e l l as g e n e t i c factors. B u t w h e n we are t a l k i n g a b o u t units of selection a d i f f e r e n t e m p h a s i s i s c a l l e d for, a n e m p h a s i s o n t h e p r o p e r t i e s o f r e p l i c a t o r s .
O r g a n i s m s , G r o u p s and M e m e s : R e p l i c a t o r s o r V e h i c l e s ?
T h e special
status
of genetic
factors
rather
than
non-genetic
99
factors
is
d e s e r v e d for o n e r e a s o n o n l y : g e n e t i c f a c t o r s r e p l i c a t e t h e m s e l v e s , b l e m i s h e s and all, but non-genetic factors do not. L e t u s g r a n t w i t h b o t h h a n d s t h a t t h e t e m p e r a t u r e i n t h e nest h o u s i n g a d e v e l o p i n g b i r d i s i m p o r t a n t b o t h for its i m m e d i a t e s u r v i v a l a n d for t h e w a y i t d e v e l o p s a n d t h e r e f o r e for its l o n g - t e r m s u c c e s s a s a n a d u l t . T h e i m m e d i a t e effects o f g e n e p r o d u c t s o n t h e b i o c h e m i c a l s p r i n g s o f d e v e l o p m e n t m a y , i n d e e d , c l o s e l y r e s e m b l e t h e effects o f t e m p e r a t u r e c h a n g e s 1957). We Bunsen
could
burners,
biochemical
tree
even
i m a g i n e the
selectively
applied
of embryonic
enzyme at
products
crucial
causation,
(Waddington
of genes
nodes
of the
controlling
as
little
branching
development
by
s e l e c t i v e c o n t r o l o f b i o c h e m i c a l r e a c t i o n r a t e s . A n e m b r y o l o g i s t r i g h t l y sees no
fundamental
distinction
between
genetic
and
environmental
causal
factors, a n d h e c o r r e c t l y r e g a r d s e a c h a s n e c e s s a r y b u t n o t s u f f i c i e n t . B a t e s o n was putting the e m b r y o l o g i s t ' s point of v i e w , a n d no ethologist is better q u a l i f i e d t o d o so. B u t I w a s n o t t a l k i n g e m b r y o l o g y . I w a s n o t c o n c e r n e d with the rival claims of d e t e r m i n a n t s of d e v e l o p m e n t . I w a s t a l k i n g a b o u t replicators surviving in evolutionary time, and Bateson certainly agrees that n e i t h e r a nest, n o r t h e t e m p e r a t u r e i n s i d e it, n o r t h e b i r d t h a t b u i l t it, a r e r e p l i c a t o r s . W e c a n q u i c k l y see t h a t t h e y a r e n o t r e p l i c a t o r s b y e x p e r i m e n t a l l y a l t e r i n g o n e o f t h e m . T h e c h a n g e m a y w r e a k h a v o c o n t h e a n i m a l , o n its d e v e l o p m e n t a n d its c h a n c e s of s u r v i v a l , but the change will not be passed on to the next generation. N o w m a k e a s i m i l a r m u t i l a t i o n ( m u t a t i o n ) to a g e n e in t h e g e r m - l i n e : t h e c h a n g e m a y o r m a y n o t affect t h e b i r d ' s d e v e l o p m e n t a n d its s u r v i v a l , b u t i t can b e p a s s e d o n t o t h e n e x t g e n e r a t i o n ; i t c a n b e r e p l i c a t e d . A s i s s o often t h e c a s e , a n a p p a r e n t d i s a g r e e m e n t t u r n s o u t t o b e d u e t o mutual
misunderstanding.
I
thought
that
Bateson
was
denying
proper
respect to the I m m o r t a l R e p l i c a t o r . Bateson t h o u g h t that I w a s d e n y i n g proper respect to the G r e a t N e x u s of c o m p l e x causal factors i n t e r a c t i n g in d e v e l o p m e n t . I n f a c t , e a c h o f u s w a s l a y i n g l e g i t i m a t e stress o n c o n s i d e r a t i o n s w h i c h a r e i m p o r t a n t for t w o d i f f e r e n t m a j o r fields o f b i o l o g y , t h e s t u d y o f d e v e l o p m e n t a n d the study of n a t u r a l selection. An
organism,
then,
is
not
a
replicator,
not
even
(despite
Lewontin
1 9 7 0 a — s e e D a w k i n s i n press) a c r u d e r e p l i c a t o r w i t h p o o r c o p y i n g f i d e l i t y . I t i s t h e r e f o r e b e t t e r n o t t o s p e a k o f a d a p t a t i o n s a s b e i n g for t h e g o o d o f t h e organism.
W h a t a b o u t larger units,
groups of organisms,
species,
com-
munities of species, e t c . ? S o m e of these l a r g e r g r o u p i n g s are c l e a r l y subject to a version of the 'internal f r a g m e n t a t i o n destroys c o p y i n g fidelity' a r g u m e n t . T h e f r a g m e n t i n g a g e n t i n this c a s e i s n o t t h e r e c o m b i n i n g effects o f m e i o s i s , but i m m i g r a t i o n a n d e m i g r a t i o n , the destruction o f the integrity o f g r o u p s b y the m o v e m e n t o f i n d i v i d u a l s i n t o a n d o u t o f t h e m . A s I h a v e p u t i t b e f o r e , t h e y a r e l i k e c l o u d s i n t h e sky o r d u s t - s t o r m s i n t h e d e s e r t . temporary
aggregations
or
federations.
They
are
not
stable
T h e y are through
100 O r g a n i s m s , G r o u p s and M e m e s :
Replicators or Vehicles?
e v o l u t i o n a r y t i m e . P o p u l a t i o n s m a y last a l o n g w h i l e , b u t t h e y a r e c o n s t a n t l y b l e n d i n g w i t h o t h e r p o p u l a t i o n s a n d s o l o s i n g t h e i r i d e n t i t y . T h e y a r e also s u b j e c t to e v o l u t i o n a r y c h a n g e f r o m w i t h i n . A p o p u l a t i o n is n o t a d i s c r e t e e n o u g h entity to be a unit of natural selection, not stable and unitary enough to
be
'selected'
in
preference
to
another
population.
But, just
as
the
' f r a g m e n t a t i o n ' a r g u m e n t a p p l i e d o n l y to a subset of organisms, sexual ones, so it also applies o n l y to a subset at the g r o u p level. It applies to groups c a p a b l e of i n t e r b r e e d i n g , but it does not a p p l y to r e p r o d u c t i v e l y isolated species. L e t us, t h e n , e x a m i n e w h e t h e r s p e c i e s b e h a v e s u f f i c i e n t l y like c o h e r e n t e n t i t i e s , m u l t i p l y i n g a n d g i v i n g rise t o o t h e r s p e c i e s , t o d e s e r v e t o b e c a l l e d replicators. N o t e that that is not the same as Ghiselin's (1974b) logical claim that species are 'individuals'
(see a l s o H u l l
1976).
O r g a n i s m s , too, are
i n d i v i d u a l s in G h i s e l i n ' s sense, a n d I h o p e I h a v e established that organisms are not replicators. Do species, or, to be m o r e precise, do r e p r o d u c t i v e l y isolated g e n e - p o o l s , really a n s w e r to the definition of replicators? It is i m p o r t a n t to r e m e m b e r t h a t m e r e i m m o r t a l i t y is n o t a sufficient q u a l i f i c a t i o n . A l i n e a g e , s u c h a s a s e q u e n c e o f p a r e n t s a n d o f f s p r i n g from the l o n g - u n c h a n g e d b r a c h i o p o d g e n u s Lingula, i s u n e n d i n g i n t h e s a m e sense, a n d t o t h e s a m e e x t e n t , a s a l i n e a g e o f g e n e s . I n d e e d , for this e x a m p l e w e p e r h a p s n e e d n o t h a v e c h o s e n a ' l i v i n g fossil' l i k e Lingula. E v e n a r a p i d l y e v o l v i n g l i n e a g e c a n , in a sense, be treated as an entity w h i c h is either extinct or e x t a n t at a n y m o m e n t in g e o l o g i c a l time. N o w , certain kinds of lineage m a y be m o r e likely to go extinct than others, and we m a y be able to discern statistical l a w s of extinction. F o r e x a m p l e , lineages w h o s e females r e p r o d u c e a s e x u a l l y m a y b e s y s t e m a t i c a l l y m o r e o r less l i k e l y t o g o e x t i n c t than lineages w h o s e females stick to sex ( W i l l i a m s 1 9 7 5 ; M a y n a r d S m i t h 1978a). It has been suggested that a m m o n i t e and bivalve lineages with a h i g h r a t e o f e v o l v i n g l a r g e r s i z e (i.e. w i t h a h i g h r a t e o f o b e y i n g C o p e ' s R u l e ) are m o r e likely to go extinct than more slowly evolving lineages (Hallam 1 9 7 5 ) . L e i g h ( 1 9 7 7 ) m a k e s some excellent points a b o u t differential lineage e x t i n c t i o n , a n d its r e l a t i o n s h i p t o l o w e r l e v e l s o f s e l e c t i o n : ' . . . t h o s e s p e c i e s a r e f a v o r e d w h e r e s e l e c t i o n w i t h i n p o p u l a t i o n s w o r k s m o r e n e a r l y for the g o o d o f t h e s p e c i e s ' . S e l e c t i o n ' . . . f a v o r s s p e c i e s t h a t h a v e , for w h a t e v e r reason, evolved genetic systems w h e r e a gene's selective a d v a n t a g e more n e a r l y m a t c h e s its c o n t r i b u t i o n t o f i t n e s s ' . H u l l
(1980a,b)
is particularly
c l e a r a b o u t t h e l o g i c a l s t a t u s o f t h e l i n e a g e , a n d a b o u t its d i s t i n c t i o n from t h e r e p l i c a t o r a n d t h e i n t e r a c t o r ( H u l l ' s n a m e for w h a t I a m c a l l i n g the 'vehicle'). Differential lineage extinction, t h o u g h technically a form of selection, is not e n o u g h in itself to g e n e r a t e progressive e v o l u t i o n a r y c h a n g e . L i n e a g e s m a y b e ' s u r v i v o r s ' , b u t this d o e s n o t m a k e t h e m r e p l i c a t o r s . G r a i n s o f s a n d
O r g a n i s m s , G r o u p s and M e m e s : R e p l i c a t o r s o r V e h i c l e s ?
101
a r e s u r v i v o r s . H a r d g r a i n s , m a d e o f q u a r t z o r d i a m o n d , w i l l last l o n g e r t h a n soft g r a i n s m a d e o f c h a l k . B u t n o b o d y h a s e v e r i n v o k e d h a r d n e s s s e l e c t i o n a m o n g s a n d g r a i n s a s t h e basis for a n e v o l u t i o n a r y p r o g r e s s i o n . T h e r e a s o n , fundamentally, is that grains of sand do not m u l t i p l y . O n e g r a i n m a y survive a l o n g t i m e , b u t i t d o e s n o t m u l t i p l y a n d m a k e c o p i e s o f itself. D o s p e c i e s , o r other groups of organisms, m u l t i p l y ? Do they replicate? Alexander and
Borgia
(1978)
assert
that they do,
and
that
they are
t h e r e f o r e true r e p l i c a t o r s : ' S p e c i e s g i v e rise t o s p e c i e s ; s p e c i e s m u l t i p l y . ' T h e best c a s e I c a n m a k e for r e g a r d i n g s p e c i e s , o r r a t h e r t h e i r g e n e - p o o l s , a s m u l t i p l y i n g r e p l i c a t o r s arises f r o m t h e t h e o r y o f ' s p e c i e s s e l e c t i o n ' a s s o c i a t e d w i t h the p a l a e o n t o l o g i c a l i d e a o f ' p u n c t u a t e d e q u i l i b r i a ' ( E l d r e d g e & G o u l d 1972; Stanley 1975, 1979; Gould & Eldredge 1977; G o u l d 1977c, 1980a,b; L e v i n t o n & S i m o n 1 9 8 0 ) . I w i l l t a k e s o m e t i m e t o d i s c u s s this b o d y o f t h e o r y , since ' s p e c i e s s e l e c t i o n ' i s v e r y r e l e v a n t t o this c h a p t e r . A n o t h e r r e a s o n for t a k i n g t h e t i m e i s t h a t I r e g a r d the s u g g e s t i o n s o f E l d r e d g e a n d G o u l d a s o f g r e a t interest t o b i o l o g y g e n e r a l l y , b u t I a m a n x i o u s t h a t t h e y s h o u l d n o t b e oversold as more revolutionary than they actually are. G o u l d and E l d r e d g e ( 1 9 7 7 , p . 1 1 7 ) a r e t h e m s e l v e s c o n s c i o u s o f this d a n g e r , t h o u g h for d i f f e r e n t reasons. M y fear s t e m s f r o m t h e g r o w i n g i n f l u e n c e o f a v i g i l a n t c o r p s o f l a y c r i t i c s of
Darwinism,
either
religious
fundamentalists
or
Shavian/Koestlerian
L a m a r c k i s t s w h o , for r e a s o n s t h a t h a v e n o t h i n g t o d o w i t h s c i e n c e , e a g e r l y seize u p o n a n y t h i n g t h a t , w i t h i m p e r f e c t u n d e r s t a n d i n g , c a n b e m a d e t o sound a n t i - D a r w i n i a n . Journalists are often o n l y too r e a d y to p a n d e r to the unpopularity
of Darwinism
in
some
lay
circles.
One
of Britain's
least
d i s r e p u t a b l e d a i l y n e w s p a p e r s (The Guardian, 2 1 N o v e m b e r 1 9 7 8 ) s e r v e d u p a
journalistically
garbled
but
still
just
recognizable
version
of
the
E l d r e d g e / G o u l d theory in a l e a d i n g article, as e v i d e n c e that all is not w e l l with Darwinism.
P r e d i c t a b l y , this e l i c i t e d s o m e u n c o m p r e h e n d i n g f u n d a -
mentalist glee in the letter c o l u m n s of the paper, some of it from d i s q u i e t i n g l y influential
sources,
impression
that
and
even
the
'the
public could
scientists'
well
themselves
have
been
left
now
have
doubts
with
the
about
D a r w i n i s m . D r G o u l d i n f o r m s m e t h a t The Guardian d i d n o t f a v o u r h i m w i t h a r e p l y to his l e t t e r of p r o t e s t . A n o t h e r B r i t i s h n e w s p a p e r , (8 M a r c h
1981),
challenge Darwin', Eldredge/Gould
in a m u c h longer article called sensationally exaggerated
theory
and
other
versions
The Sunday Times
' T h e n e w clues that
the difference of Darwinism.
between The
the
British
B r o a d c a s t i n g C o r p o r a t i o n also g o t in on the a c t a r o u n d the s a m e time, in two separate p r o g r a m m e s m a d e by rival production teams. T h e y w e r e called The
Trouble with
Evolution
and
Did Darwin get it
Wrong?,
and
they
differed
h a r d l y a t all e x c e p t that o n e h a d E l d r e d g e a n d the o t h e r h a d G o u l d ! T h e second
programme
actually
went
to
the
lengths
of digging
up
some
102
O r g a n i s m s , G r o u p s and M e m e s : R e p l i c a t o r s o r V e h i c l e s ?
fundamentalists to c o m m e n t on the E l d r e d g e / G o u l d t h e o r y : not surprisingly, the ill-understood a p p e a r a n c e of dissension w i t h i n the ranks of Darwinists was meat and drink to them. J o u r n a l i s t i c s t a n d a r d s a r e n o t u n k n o w n i n l e a r n e d p e r i o d i c a l s t o o . Science (Vol.
210,
pp.
macroevolution
883 8 8 7 , under
1980)
reported
the d r a m a t i c
heading,
on
a
recent
conference
'Evolutionary
theory
on
under
fire', a n d w i t h the e q u a l l y sensational subtitle, ' A n historic conference in Chicago
challenges
the
four-decade
long
dominance
of
the
Modern
S y n t h e s i s ' (see c r i t i c i s m s b y F u t u y a m a e t al. 1 9 8 1 ) . A s M a y n a r d S m i t h i s quoted as saying at the same conference, ' Y o u are in d a n g e r of preventing understanding by suggesting that
there is intellectual antagonism
where
n o n e e x i s t s ' (see a l s o M a y n a r d S m i t h 1 9 8 1 ) . I n t h e f a c e o f a l l t h e b a l l y h o o , I am
anxious to be very clear about,
t o q u o t e o n e o f their o w n section
headings, exactly ' W h a t Eldredge and Gould Did Not (And Did) Say'. The
theory
of punctuated
equilibria
suggests
that
evolution
does not
consist in c o n t i n u o u s s m o o t h c h a n g e , 'stately unfolding', but goes in jerks, p u n c t u a t i n g l o n g p e r i o d s o f stasis. L a c k o f e v o l u t i o n a r y c h a n g e i n fossil l i n e a g e s s h o u l d n o t b e w r i t t e n off a s ' n o d a t a ' , b u t s h o u l d b e r e c o g n i z e d a s the n o r m , a n d a s w h a t w e s h o u l d r e a l l y e x p e c t t o see i f w e t a k e o u r m o d e r n s y n t h e s i s , p a r t i c u l a r l y its e m b e d d e d i d e a s o f a l l o p a t r i c s p e c i a t i o n , s e r i o u s l y : ' A s a c o n s e q u e n c e o f t h e a l l o p a t r i c t h e o r y , n e w fossil s p e c i e s d o not o r i g i n a t e i n t h e p l a c e w h e r e t h e i r a n c e s t o r s l i v e d . I t i s extremely i m p r o b a b l e t h a t w e shall be a b l e to trace the g r a d u a l splitting of a lineage m e r e l y by following a certain species up through a local rock c o l u m n ' (Eldredge & G o u l d 1972, p. 94). Of course microevolution by ordinary natural selection, w h a t I would call genetic replicator selection, goes on, but it is largely confined to brief b u r s t s o f a c t i v i t y a r o u n d t h e crisis t i m e s k n o w n a s s p e c i a t i o n e v e n t s . T h e s e bursts o f m i c r o e v o l u t i o n a r e u s u a l l y c o m p l e t e d t o o fast for p a l a e o n t o l o g i s t s t o t r a c k t h e m . A l l w e c a n see i s t h e s t a t e o f t h e l i n e a g e b e f o r e a n d after the n e w s p e c i e s i s f o r m e d . I t f o l l o w s t h a t ' g a p s ' i n t h e fossil r e c o r d b e t w e e n s p e c i e s , far f r o m b e i n g t h e e m b a r r a s s m e n t D a r w i n i a n s h a v e s o m e t i m e s t a k e n t h e m t o be, are exactly w h a t we should expect. T h e palaeontological evidence can be argued about
(Gingerich
1976;
G o u l d & E l d r e d g e 1 9 7 7 ; H a l l a m 1 9 7 8 ) , a n d I a m n o t q u a l i f i e d t o j u d g e it. A p p r o a c h i n g from a n o n - p a l a e o n t o l o g i c a l direction, indeed in lamentable ignorance
of
the
Wrightian/Mayrian
whole idea
Eldredge/Gould of
buffered
theory,
gene-pools
I
once
resisting
found
the
change,
but
o c c a s i o n a l l y s u c c u m b i n g to genetic revolutions, satisfyingly c o m p a t i b l e with one o f m y o w n enthusiasms, M a y n a r d Smith's (1974) 'evolutionarily stable strategy' concept: T h e g e n e p o o l w i l l b e c o m e a n evolutionarily stable set o f g e n e s , defined as a gene pool which cannot be invaded by any new gene. Most new
O r g a n i s m s , Groups and M e m e s : Replicators or Vehicles?
103
g e n e s w h i c h arise, e i t h e r b y m u t a t i o n o r r e a s s o r t m e n t o r i m m i g r a t i o n , are q u i c k l y p e n a l i z e d by n a t u r a l selection: the e v o l u t i o n a r i l y stable set
is
restored.
instability,
Occasionally . . . there
terminating
in
a
new
is
a
transitional
evolutionarily
period
stable
of
set . . . a
population might have more than one alternative stable point, and it m i g h t o c c a s i o n a l l y flip from o n e to a n o t h e r . P r o g r e s s i v e e v o l u t i o n m a y b e n o t s o m u c h a s t e a d y u p w a r d c l i m b a s a series o f d i s c r e t e steps from s t a b l e p l a t e a u t o s t a b l e p l a t e a u [ D a w k i n s 1 9 7 6 a , p . 9 3 ] . I a m also q u i t e i m p r e s s e d w i t h E l d r e d g e a n d G o u l d ' s r e i t e r a t e d p o i n t about time-scales: ' H o w can we view a steady progression yielding a 1 0 % increase in a million years as a n y t h i n g but a meaningless abstraction? C a n this v a r i e d w o r l d o f o u r s p o s s i b l y i m p o s e s u c h m i n u t e s e l e c t i o n p r e s s u r e s s o uninterruptedly
for
so
long?'
(Gould
&
Eldredge
1977).
'...to
see
g r a d u a l i s m a t all i n t h e fossil r e c o r d i m p l i e s s u c h a n e x c r u c i a t i n g l y s l o w r a t e o f p e r - g e n e r a t i o n c h a n g e t h a t w e m u s t s e r i o u s l y c o n s i d e r its i n v i s i b i l i t y t o natural selection in the c o n v e n t i o n a l m o d e — c h a n g e s that confer m o m e n t a r y adaptive a d v a n t a g e s ' ( G o u l d 1980a). I suppose the following a n a l o g y m i g h t be m a d e . If a cork floats from one side of the A t l a n t i c to the other, t r a v e l l i n g steadily without d e v i a t i n g o r g o i n g b a c k w a r d s , w e m i g h t i n v o k e the G u l f S t r e a m o r T r a d e W i n d s i n e x p l a n a t i o n . T h i s w i l l seem p l a u s i b l e i f the time the c o r k t a k e s t o cross t h e o c e a n i s o f t h e r i g h t o r d e r o f m a g n i t u d e , s a y a f e w weeks or m o n t h s . B u t if the cork should t a k e a million y e a r s to cross the o c e a n , a g a i n n o t d e v i a t i n g o r g o i n g b a c k w a r d s b u t s t e a d i l y i n c h i n g its w a y a c r o s s , w e s h o u l d n o t b e satisfied w i t h a n y e x p l a n a t i o n i n t e r m s o f c u r r e n t s and winds. Currents and winds just don't m o v e that slowly, or if they do they will be so w e a k that the cork will be o v e r w h e l m i n g l y buffeted by o t h e r forces, b a c k w a r d s a s m u c h a s f o r w a r d s . I f w e f o u n d a c o r k s t e a d i l y m o v i n g a t such an e x t r e m e l y slow rate, we w o u l d h a v e to seek a w h o l l y different kind of explanation,
an
phenomenon
observed.
explanation
commensurate
with
the
time-scale
of the
Incidentally, there is a mildly interesting historical irony here. O n e of the e a r l y a r g u m e n t s u s e d a g a i n s t D a r w i n w a s t h a t t h e r e w a s n ' t e n o u g h t i m e for the p r o p o s e d a m o u n t o f e v o l u t i o n t o h a v e h a p p e n e d . i m a g i n e that selection pressures w e r e strong e n o u g h
It seemed hard to achieve
all
to that
e v o l u t i o n a r y c h a n g e in the short time then t h o u g h t to be a v a i l a b l e . T h e a r g u m e n t of E l d r e d g e a n d G o u l d just g i v e n is almost the e x a c t o p p o s i t e : it is h a r d to i m a g i n e a s e l e c t i o n p r e s s u r e weak e n o u g h to s u s t a i n s u c h a s l o w r a t e of unidirectional evolution over such a long period! Perhaps we should take w a r n i n g f r o m this h i s t o r i c a l t w i s t . B o t h a r g u m e n t s r e s o r t t o t h e ' h a r d t o i m a g i n e ' style of reasoning that D a r w i n so wisely c a u t i o n e d us against. Although
I
find
Eldredge
and
Gould's
time-scale
point
somewhat
p l a u s i b l e , I a m less c o n f i d e n t a b o u t i t t h a n t h e y a r e , s i n c e I d o f e a r t h e
104
O r g a n i s m s , G r o u p s and M e m e s : R e p l i c a t o r s o r V e h i c l e s ?
limitations o f m y o w n i m a g i n a t i o n . After all, the gradualist theory does not r e a l l y n e e d t o a s s u m e unidirectional e v o l u t i o n for l o n g p e r i o d s . I n t e r m s o f m y c o r k a n a l o g y , w h a t if the w i n d is so w e a k that the cork takes a million years to
cross
the
Atlantic?
Waves
and
local
currents
may
indeed
send
it
b a c k w a r d s a l m o s t a s m u c h a s f o r w a r d s . B u t w h e n all i s a d d e d u p , the n e t s t a t i s t i c a l d i r e c t i o n o f t h e c o r k m a y still
be determined
by a slow and
relentless w i n d . I a l s o w o n d e r w h e t h e r E l d r e d g e a n d G o u l d g i v e sufficient a t t e n t i o n t o the p o s s i b i l i t i e s o p e n e d u p b y ' a r m s r a c e s ' ( C h a p t e r 4 ) . I n c h a r a c t e r i z i n g the gradualist theory that they attack, they write: ' T h e postulated mechanism for g r a d u a l u n i - d i r e c t i o n a l c h a n g e i s " o r t h o s e l e c t i o n " , u s u a l l y v i e w e d a s a constant a d j u s t m e n t to a u n i - d i r e c t i o n a l c h a n g e in one or m o r e features of the p h y s i c a l e n v i r o n m e n t '
(Eldredge &
Gould
1972).
If the winds a n d
currents of the p h y s i c a l e n v i r o n m e n t pressed steadily in the same direction over g e o l o g i c a l time-scales, it m i g h t indeed seem likely that animal lineages would
reach
the
other
side
of their
evolutionary
ocean
so
fast
that
palaeontologists c o u l d not track their passage. B u t c h a n g e ' p h y s i c a l ' t o ' b i o l o g i c a l ' a n d t h i n g s m a y l o o k different. I f e a c h small
adaptive
step
in
one
lineage
calls
forth
a
counteradaptation
in
a n o t h e r l i n e a g e — s a y its p r e d a t o r s — s l o w , d i r e c t i o n a l o r t h o s e l e c t i o n looks rather m o r e plausible. T h e s a m e is true of intraspecific competition, w h e r e t h e o p t i m u m s i z e , s a y , for a n i n d i v i d u a l c a n b e s l i g h t l y l a r g e r t h a n the p r e s e n t p o p u l a t i o n m o d e , whatever the present population mode may be. ' . . . in the p o p u l a t i o n as a w h o l e t h e r e is a c o n s t a n t t e n d e n c y to f a v o r a s i z e s l i g h t l y a b o v e t h e m e a n . T h e s l i g h t l y l a r g e r a n i m a l s h a v e a v e r y s m a l l b u t i n the long run, in large populations, decisive a d v a n t a g e in competition . . . T h u s , p o p u l a t i o n s t h a t a r e r e g u l a r l y e v o l v i n g i n this w a y a r e a l w a y s w e l l a d a p t e d a s r e g a r d s s i z e i n t h e sense t h a t t h e o p t i m u m i s c o n t i n u o u s l y i n c l u d e d i n t h e i r normal
range of variation,
but a constant a s y m m e t r y in the centripetal
s e l e c t i o n f a v o r s a s l o w u p w a r d shift i n t h e m e a n ' ( S i m p s o n 1 9 5 3 , p . 1 5 1 ) . A l t e r n a t i v e l y (and shamelessly h a v i n g it b o t h w a y s ! ) , if e v o l u t i o n a r y trends r e a l l y a r e p u n c t u a t e d a n d s t e p p e d , p e r h a p s this i n i t s e l f c o u l d b e e x p l a i n e d by the arms r a c e c o n c e p t , g i v e n time-lags b e t w e e n a d a p t i v e a d v a n c e s on one side of the a r m s r a c e a n d responses by the other. B u t let u s p r o v i s i o n a l l y a c c e p t t h e t h e o r y o f p u n c t u a t e d e q u i l i b r i a a s a n e x c i t i n g l y d i f f e r e n t w a y o f l o o k i n g a t f a m i l i a r p h e n o m e n a , a n d t u r n t o the other side o f G o u l d a n d E l d r e d g e ' s ( 1 9 7 7 ) e q u a t i o n , ' p u n c t u a t e d equilibria + W r i g h t ' s r u l e = s p e c i e s s e l e c t i o n ' . W r i g h t ' s R u l e (not his o w n c o i n i n g ) i s ' t h e p r o p o s i t i o n t h a t a set o f m o r p h o l o g i e s p r o d u c e d b y s p e c i a t i o n e v e n t s i s essentially r a n d o m w i t h respect to the direction of e v o l u t i o n a r y trends within a c l a d e ' ( G o u l d & E l d r e d g e 1 9 7 7 ) . F o r e x a m p l e , even if there is an overall t r e n d t o w a r d s l a r g e r s i z e i n a set o f r e l a t e d l i n e a g e s , W r i g h t ' s R u l e suggests t h a t t h e r e i s n o s y s t e m a t i c t e n d e n c y for n e w l y b r a n c h e d - o f f s p e c i e s t o b e
O r g a n i s m s , Groups and M e m e s : Replicators or Vehicles?
larger than mutation
their parent species.
is clear,
and
T h e analogy with
this l e a d s d i r e c t l y t o
the
105
'randomness'
the right-hand
of
side of the
e q u a t i o n . I f n e w s p e c i e s differ f r o m t h e i r p r e d e c e s s o r s r a n d o m l y w i t h r e s p e c t to
major
trends,
major
trends
themselves
must
be
due
e x t i n c t i o n a m o n g those n e w s p e c i e s — ' s p e c i e s s e l e c t i o n ' ,
to
differential
t o use S t a n l e y ' s
(1975) term. Gould
( 1 9 8 0 a ) r e g a r d s ' t h e t e s t i n g o f W r i g h t ' s r u l e a s a m a j o r task for
macroevolutionary
theory
and
paleobiology.
For
the
theory
of species
s e l e c t i o n , i n its p u r e f o r m , d e p e n d s u p o n it. C o n s i d e r , for e x a m p l e , a l i n e a g e displaying
C o p e ' s rule of increasing b o d y size—horses,
for e x a m p l e .
If
W r i g h t ' s r u l e b e v a l i d , a n d n e w s p e c i e s o f horses a r i s e e q u a l l y o f t e n a t sizes smaller and larger than their ancestors, then the trend is p o w e r e d by species s e l e c t i o n . B u t i f n e w s p e c i e s a r i s e p r e f e r e n t i a l l y a t sizes l a r g e r t h a n t h e i r ancestors,
then
we
don't
require
species
selection
at
all,
since
random
e x t i n c t i o n w o u l d still y i e l d t h e t r e n d . ' G o u l d h e r e s i m u l t a n e o u s l y s t i c k s his n e c k o u t a n d h a n d s O c c a m ' s R a z o r t o his o p p o n e n t s ! H e c o u l d e a s i l y h a v e c l a i m e d t h a t e v e n i f his m u t a t i o n - a n a l o g u e
(speciation)
was d i r e c t e d , t h e
t r e n d m i g h t still b e r e i n f o r c e d b y s p e c i e s s e l e c t i o n ( L e v i n t o n & S i m o n 1 9 8 0 ) . W i l l i a m s ( 1 9 6 6 , p . 99) i n a n i n t e r e s t i n g d i s c u s s i o n w h i c h I h a v e n o t s e e n c i t e d i n the l i t e r a t u r e o n p u n c t u a t e d e q u i l i b r i a , c o n s i d e r s a f o r m o f s p e c i e s s e l e c t i o n a c t i n g i n opposition to, a n d p e r h a p s o u t w e i g h i n g , t h e o v e r a l l t r e n d o f e v o l u t i o n w i t h i n s p e c i e s . H e a g a i n uses t h e h o r s e e x a m p l e , a n d t h e f a c t t h a t e a r l i e r fossils t e n d t o b e s m a l l e r t h a n l a t e r o n e s : F r o m this o b s e r v a t i o n , i t i s t e m p t i n g t o c o n c l u d e t h a t , a t l e a s t m o s t o f the
time
and
on
the
average,
a
larger
than
mean
size
was
an
a d v a n t a g e t o a n i n d i v i d u a l h o r s e i n its r e p r o d u c t i v e c o m p e t i t i o n w i t h the
rest
o f its
population.
So
the
component
populations
of the
T e r t i a r y horse-fauna are p r e s u m e d t o h a v e b e e n e v o l v i n g l a r g e r size most of the time a n d on the a v e r a g e . It is c o n c e i v a b l e , h o w e v e r , that precisely the opposite is true. It m a y be that at a n y g i v e n m o m e n t d u r i n g the T e r t i a r y , most of the horse p o p u l a t i o n s w e r e e v o l v i n g a s m a l l e r s i z e . T o a c c o u n t for t h e t r e n d t o w a r d s l a r g e r s i z e i t i s m e r e l y necessary
to
favoured
such
make a
the additional assumption tendency.
Thus,
while
only
that g r o u p selection a
minority
of the
populations m a y h a v e been e v o l v i n g a larger size, it c o u l d h a v e b e e n this m i n o r i t y t h a t g a v e rise t o m o s t o f t h e p o p u l a t i o n s o f a m i l l i o n years later.'
I do not find it hard to b e l i e v e that s o m e of the m a j o r m a c r o e v o l u t i o n a r y t r e n d s , o f the C o p e ' s R u l e t y p e ( b u t see H a l l a m 1 9 7 8 ) , o b s e r v e d b y p a l a e o n t o l ogists a r e d u e t o s p e c i e s s e l e c t i o n , i n t h e sense o f this p a s s a g e f r o m W i l l i a m s , w h i c h I think is the same as E l d r e d g e a n d G o u l d ' s sense. As I b e l i e v e all
106
O r g a n i s m s , G r o u p s and M e m e s : R e p l i c a t o r s o r V e h i c l e s ?
t h r e e a u t h o r s w o u l d a g r e e , this i s a v e r y d i f f e r e n t m a t t e r f r o m a c c e p t i n g g r o u p s e l e c t i o n a s a n e x p l a n a t i o n for i n d i v i d u a l s e l f - s a c r i f i c e : a d a p t a t i o n s for the g o o d o f the species. T h e r e w e are t a l k i n g a b o u t a n o t h e r kind o f g r o u p selection m o d e l , w h e r e the g r o u p is really seen not as a replicator but as a v e h i c l e for r e p l i c a t o r s . I s h a l l c o m e t o this s e c o n d k i n d o f g r o u p s e l e c t i o n later. M e a n w h i l e I shall a r g u e that a belief in the p o w e r of species selection t o s h a p e s i m p l e m a j o r t r e n d s i s n o t t h e s a m e a s a b e l i e f i n its p o w e r t o p u t together c o m p l e x adaptations such as eyes and brains. T h e m a j o r trends of p a l a e o n t o l o g y , simple increases in absolute size, or of r e l a t i v e sizes o f d i f f e r e n t p a r t s o f t h e b o d y , a r e i m p o r t a n t a n d i n t e r e s t i n g , b u t t h e y a r e , a b o v e all, s i m p l e . A c c e p t i n g E l d r e d g e a n d G o u l d ' s belief that n a t u r a l s e l e c t i o n i s a g e n e r a l t h e o r y t h a t c a n b e p h r a s e d o n m a n y l e v e l s , the putting together of a certain quantity of evolutionary c h a n g e demands a c e r t a i n m i n i m u m n u m b e r o f s e l e c t i v e r e p l i c a t o r - e l i m i n a t i o n s . W h e t h e r the replicators that are selectively eliminated are genes or species, a simple e v o l u t i o n a r y c h a n g e r e q u i r e s o n l y a few r e p l i c a t o r s u b s t i t u t i o n s . A l a r g e n u m b e r o f r e p l i c a t o r s u b s t i t u t i o n s , h o w e v e r , a r e n e e d e d for t h e e v o l u t i o n o f a
complex
adaptation.
The
minimum
replacement
cycle
time
when we
c o n s i d e r t h e g e n e a s r e p l i c a t o r i s o n e i n d i v i d u a l g e n e r a t i o n , from z y g o t e t o z y g o t e . I t i s m e a s u r e d i n y e a r s o r m o n t h s , o r s m a l l e r t i m e u n i t s . E v e n i n the l a r g e s t o r g a n i s m s i t i s m e a s u r e d i n o n l y tens o f y e a r s . W h e n w e c o n s i d e r the species as replicator, on the other h a n d , the r e p l a c e m e n t c y c l e time is the interval from speciation event to speciation event, and m a y be measured in t h o u s a n d s o f y e a r s , tens o f thousands, h u n d r e d s o f thousands. I n a n y given period of g e o l o g i c a l time, the n u m b e r of selective species extinctions that can h a v e t a k e n p l a c e i s m a n y o r d e r s o f m a g n i t u d e less t h a n
the n u m b e r of
selective allele replacements that can h a v e taken place. A g a i n it m a y be j u s t a limitation of the i m a g i n a t i o n , but w h i l e I c a n easily see
species
elongation
selection of horse
shaping legs,
I
a
simple
cannot
see
size such
trend slow
such
as
the
Tertiary
replicator-elimination
p u t t i n g t o g e t h e r a s u i t e o f a d a p t a t i o n s s u c h a s t h o s e o f w h a l e s t o a q u a t i c life. N o w , it m a y be said, surely that is unfair. H o w e v e r c o m p l e x the aquatic adaptations of whales m a y be w h e n taken as a w h o l e , c a n they not be broken d o w n i n t o a set o f s i m p l e s i z e t r e n d s w i t h a l l o m e t r i c c o n s t a n t s o f v a r y i n g m a g n i t u d e a n d sign in different parts of the b o d y ? If y o u can s t o m a c h oned i m e n s i o n a l e l o n g a t i o n in horses' legs as d u e to species selection, w h y not a w h o l e set o f e q u a l l y s i m p l e s i z e t r e n d s a d v a n c i n g i n p a r a l l e l , a n d e a c h o n e d r i v e n b y s p e c i e s s e l e c t i o n ? T h e w e a k n e s s i n this a r g u m e n t i s a s t a t i s t i c a l one. S u p p o s e there are ten such parallel trends, w h i c h is surely a highly c o n s e r v a t i v e e s t i m a t e for t h e e v o l u t i o n o f a q u a t i c a d a p t a t i o n s i n w h a l e s . I f W r i g h t ' s R u l e i s t o a p p l y t o a l l t e n , i n a n y o n e s p e c i a t i o n e v e n t e a c h o f the t e n t r e n d s i s a s l i k e l y t o b e r e v e r s e d a s t o b e a d v a n c e d . T h e c h a n c e t h a t all ten w i l l b e a d v a n c e d i n a n y o n e .speciation e v e n t i s o n e h a l f t o t h e p o w e r t e n ,
O r g a n i s m s , Groups and M e m e s : Replicators or Vehicles?
107
w h i c h i s less t h a n o n e i n a t h o u s a n d . I f t h e r e a r e t w e n t y p a r a l l e l t r e n d s , t h e chance of a n y one speciation event a d v a n c i n g all t w e n t y simultaneously is less t h a n o n e in a m i l l i o n . Admittedly,
some
advancement
towards
complex
multidimensional
a d a p t a t i o n m i g h t b e a c h i e v e d t h r o u g h s p e c i e s s e l e c t i o n e v e n i f n o t a l l t e n (or twenty) trends w e r e a d v a n c e d together in a n y o n e selective e v e n t . A f t e r all, m u c h the same critical point c a n b e m a d e a b o u t the selective d e a t h s o f i n d i v i d u a l o r g a n i s m s : i t i s r a r e t o find o n e i n d i v i d u a l a n i m a l t h a t i s o p t i m a l i n all the different d i m e n s i o n s o f m e a s u r e m e n t . T h e a r g u m e n t f i n a l l y r e t u r n s t o the d i f f e r e n c e i n c y c l e t i m e s . W e s h a l l h a v e t o m a k e a q u a n t i t a t i v e judgement
taking
into
account
the
vastly
greater
cycle
time
between
replicator deaths in the species selection case than in the g e n e selection case, a n d also t a k i n g i n t o a c c o u n t t h e c o m b i n a t o r i a l p r o b l e m r a i s e d a b o v e . I h a v e n e i t h e r t h e d a t a n o r t h e m a t h e m a t i c a l skills t o u n d e r t a k e this q u a n t i t a t i v e j u d g e m e n t , t h o u g h I h a v e a d i m f e e l i n g for t h e k i n d o f m e t h o d o l o g y t h a t w o u l d b e i n v o l v e d i n s e t t i n g u p a n a p p r o p r i a t e n u l l h y p o t h e s i s : i t w o u l d fall under the g e n e r a l
heading which
Thompson
might
have
appropriate
type
have
done
I
with
already
like a
been
to
think of as
computer', written
and
(Raup
'What
D'Arcy
programs et
al.
of the
1973).
My
provisional guess is that species selection will not be found to be a g e n e r a l l y satisfactory e x p l a n a t i o n o f c o m p l e x a d a p t a t i o n . Consider another adopt.
He
might
line protest
of argument that
it
is
that
the species
unreasonable
selectionist m i g h t
of me
to
base
my
combinatorial calculation on the assumption that the ten major trends in the evolution o f w h a l e s are i n d e p e n d e n t . S u r e l y the n u m b e r o f c o m b i n a t i o n s w e have to consider will be drastically reduced by correlations a m o n g the different t r e n d s ? I t i s i m p o r t a n t h e r e t o d i s t i n g u i s h t w o d i f f e r e n t s o u r c e s o f correlation,
which
may
be
called
incidental
correlation
and
adaptive
c o r r e l a t i o n . A n i n c i d e n t a l c o r r e l a t i o n i s a n i n t r i n s i c c o n s e q u e n c e o f t h e facts o f e m b r y o l o g y . F o r e x a m p l e , e l o n g a t i o n o f t h e left f o r e l e g i s u n l i k e l y t o b e independent o f e l o n g a t i o n o f the right foreleg. A n y m u t a t i o n that a c h i e v e s o n e i s i n t r i n s i c a l l y l i k e l y t o a c h i e v e t h e o t h e r s i m u l t a n e o u s l y . S l i g h t l y less obviously, the same m i g h t be partially true of e l o n g a t i o n of the forelegs a n d the h i n d l e g s . T h e r e a r e p r o b a b l y m a n y s i m i l a r c a s e s t h a t a r e less o b v i o u s still. An a d a p t i v e correlation, on the other h a n d , does not follow d i r ect l y from the m e c h a n i c s o f e m b r y o l o g y . A l i n e a g e t h a t m o v e s f r o m a t e r r e s t r i a l t o a n a q u a t i c e x i s t e n c e i s l i k e l y t o n e e d c h a n g e s t o its l o c o m o t o r y s y s t e m a n d its respiratory system, and there is no o b v i o u s reason to e x p e c t a n y intrinsic c o n n e c t i o n b e t w e e n t h e m . W h y should t r e n d s t h a t c o n v e r t w a l k i n g l i m b s t o flippers be intrinsically correlated w i t h trends to boost the efficiency of the l u n g s i n e x t r a c t i n g o x y g e n ? O f c o u r s e i t i s possible t h a t t w o s u c h c o a d a p t e d trends m i g h t b e c o r r e l a t e d a s a n i n c i d e n t a l c o n s e q u e n c e o f e m b r y o l o g i c a l
108
O r g a n i s m s , G r o u p s and M e m e s : Replicators or Vehicles?
mechanisms,
but
the
correlation
is
no
more
likely
to be positive
than
n e g a t i v e . W e are b a c k t o our c o m b i n a t o r i a l c a l c u l a t i o n , albeit w e must exercise care in counting our separate dimensions of change. F i n a l l y , the species selectionist m a y retreat and invoke ordinary low-level n a t u r a l selection to w e e d o u t i l l - c o a d a p t e d c o m b i n a t i o n s of c h a n g e , so that s p e c i a t i o n e v e n t s o n l y s e r v e u p a l r e a d y t r i e d a n d p r o v e d c o m b i n a t i o n s t o the s i e v e o f s p e c i e s s e l e c t i o n . B u t this ' s p e c i e s s e l e c t i o n i s t ' is, b y G o u l d ' s l i g h t s , n o species
selectionist
at
all!
He
has
conceded
that
all
the
interesting
e v o l u t i o n a r y c h a n g e results f r o m i n t e r - a l l e l e s e l e c t i o n a n d n o t f r o m i n t e r s p e c i e s s e l e c t i o n , a l b e i t i t m a y b e c o n c e n t r a t e d i n b r i e f bursts, p u n c t u a t i n g stasis. H e h a s c o n c e d e d t h e v i o l a t i o n o f W r i g h t ' s R u l e . A n d i f ' W r i g h t ' s R u l e ' n o w s e e m s u n f a i r l y e a s y t o v i o l a t e , t h a t i s w h a t I m e a n t w h e n I said t h a t G o u l d h a d s t u c k his n e c k o u t . I s h o u l d r e p e a t t h a t W r i g h t h i m s e l f i s n o t r e s p o n s i b l e for n a m i n g t h e r u l e . The
theory
of species a
selection,
equilibria,
is
stimulating
idea
dimensions
of quantitative c h a n g e
growing
which in
out
may
of that
well
of punctuated
explain
macroevolution.
I
some
would
single
be very
s u r p r i s e d i f i t c o u l d b e u s e d t o e x p l a i n t h e sort o f c o m p l e x m u l t i d i m e n s i o n a l a d a p t a t i o n t h a t I find i n t e r e s t i n g , t h e ' P a l e y ' s w a t c h ' , o r ' O r g a n s o f e x t r e m e Perfection a n d C o m p l i c a t i o n ' , kind of a d a p t a t i o n that seems to d e m a n d a s h a p i n g a g e n t a t l e a s t a s p o w e r f u l a s a d e i t y . R e p l i c a t o r s e l e c t i o n , w h e r e the replicators are alternative alleles,
m a y well be powerful
enough.
I f the
r e p l i c a t o r s a r e a l t e r n a t i v e species, h o w e v e r , I d o u b t if it is p o w e r f u l e n o u g h , b e c a u s e i t i s t o o s l o w . E l d r e d g e a n d C r a c r a f t ( 1 9 8 0 , p . 269) a p p e a r t o a g r e e : 'The
concept
reproduction roborated,
of
natural
selection
of individuals
within
within-population
(fitness
differences,
populations)
phenomenon,
appears
and
or
differential
to
be
constitutes
a
the
corbest
a v a i l a b l e e x p l a n a t i o n for t h e o r i g i n , m a i n t e n a n c e , a n d p o s s i b l e m o d i f i c a t i o n o f a d a p t a t i o n s . ' I f this i s i n d e e d t h e o p i n i o n o f ' p u n c t u a t i o n i s t s ' a n d ' s p e c i e s s e l e c t i o n i s t s ' g e n e r a l l y , i t i s h a r d t o see w h a t a l l t h e fuss i s a b o u t . F o r simplicity I h a v e discussed the theory of species selection as one in w h i c h the species is treated as a replicator. T h e reader will have noticed, however,
that
this
is
rather
like
speaking
of an
asexually
reproducing
o r g a n i s m a s a r e p l i c a t o r . E a r l i e r i n this c h a p t e r , w e s a w t h a t t h e test o f m u t i l a t i o n f o r c e s us s t r i c t l y to l i m i t t h e title of r e p l i c a t o r to t h e genome of, s a y , a s t i c k i n s e c t , n o t t h e s t i c k i n s e c t itself. S i m i l a r l y , i n t h e s p e c i e s s e l e c t i o n m o d e l , it is n o t t h e s p e c i e s t h a t is t h e r e p l i c a t o r b u t t h e gene-pool.
It is
t e m p t i n g , n o w , t o say, ' I n that case, w h y not g o the w h o l e h o g a n d regard the
gene
as
replicator
rather
than
some
larger
unit,
even
in
the
E l d r e d g e / G o u l d m o d e l ? ' T h e answer i s t h a t i f t h e y a r e r i g h t a b o u t a g e n e p o o l b e i n g a c o a d a p t e d unit, h o m e o s t a t i c a l l y buffered against c h a n g e , it m i g h t h a v e t h e s a m e k i n d o f r i g h t t o b e t r e a t e d a s a s i n g l e r e p l i c a t o r a s has t h e g e n o m e o f a s t i c k i n s e c t . T h e g e n e - p o o l h a s this r i g h t , h o w e v e r , o n l y i f i t
O r g a n i s m s , G r o u p s and M e m e s : R e p l i c a t o r s o r V e h i c l e s ?
109
is r e p r o d u c t i v e l y isolated, just as the g e n o m e has that right o n l y if it is reproduced asexually. E v e n then the right is a tenuous one. E a r l i e r i n this c h a p t e r , w e e s t a b l i s h e d t h a t a n o r g a n i s m i s d e f i n i t e l y n o t a r e p l i c a t o r , a l t h o u g h its g e n o m e m a y b e i f i t i s a s e x u a l l y r e p r o d u c e d . W e h a v e n o w s e e n t h a t t h e r e m a y b e a c a s e for r e g a r d i n g t h e g e n e - p o o l o f a reproductively isolated
g r o u p , such as a species,
as a replicator.
If we
p r o v i s i o n a l l y a c c e p t t h e l o g i c o f this c a s e , w e c a n v i s u a l i z e e v o l u t i o n d i r e c t e d b y s e l e c t i o n a m o n g s u c h r e p l i c a t o r s , b u t I h a v e j u s t c o n c l u d e d t h a t this k i n d of selection is unlikely to explain c o m p l e x a d a p t a t i o n . A p a r t from the small genetic fragment, w h i c h we discussed in the previous c h a p t e r , are there a n y o t h e r p l a u s i b l e c a n d i d a t e s for t h e title o f r e p l i c a t o r ? I h a v e p r e v i o u s l y s u p p o r t e d t h e c a s e for a c o m p l e t e l y n o n - g e n e t i c k i n d o f replicator, w h i c h flourishes o n l y i n the e n v i r o n m e n t p r o v i d e d b y c o m p l e x , communicating
brains.
I
called
it
the
'meme'
(Dawkins
1976a).
Unfortunately, unlike C l o a k (1975) but, if I understand t h e m aright, like L u m s d e n and W i l s o n (1980), I w a s insufficiently c l e a r a b o u t the distinction b e t w e e n the m e m e itself, a s r e p l i c a t o r , o n t h e o n e h a n d , a n d its ' p h e n o t y p i c effects' o r ' m e m e p r o d u c t s ' o n t h e o t h e r . A m e m e s h o u l d b e r e g a r d e d a s a unit of information residing in a brain ( C l o a k ' s ' i - c u l t u r e ' ) . It has a definite s t r u c t u r e , r e a l i z e d i n w h a t e v e r p h y s i c a l m e d i u m t h e b r a i n uses for s t o r i n g information.
If
the
brain
stores
information
as
a
pattern
of synaptic
c o n n e c t i o n s , a m e m e s h o u l d in p r i n c i p l e be v i s i b l e u n d e r a m i c r o s c o p e as a definite
pattern
of synaptic
structure.
If the
b r a i n stores
information
in
'distributed' form (Pribram 1974), the m e m e w o u l d not be l o c a l i z a b l e on a m i c r o s c o p e s l i d e , b u t still I w o u l d w a n t t o r e g a r d i t a s p h y s i c a l l y r e s i d i n g i n t h e b r a i n . T h i s i s t o d i s t i n g u i s h i t f r o m its p h e n o t y p i c effects, w h i c h a r e its consequences in the outside w o r l d ( C l o a k ' s ' m - c u l t u r e ' ) . T h e p h e n o t y p i c effects o f a m e m e m a y b e i n t h e f o r m o f w o r d s , m u s i c , v i s u a l i m a g e s , s t y l e s o f c l o t h e s , f a c i a l o r h a n d g e s t u r e s , skills s u c h a s o p e n i n g m i l k b o t t l e s i n tits, o r p a n n i n g w h e a t i n J a p a n e s e m a c a q u e s . T h e y a r e t h e o u t w a r d and visible (audible, etc.) manifestations of the m e m e s w i t h i n the b r a i n . T h e y m a y b e p e r c e i v e d b y t h e sense o r g a n s o f o t h e r i n d i v i d u a l s , a n d t h e y m a y s o i m p r i n t t h e m s e l v e s o n the b r a i n s o f t h e r e c e i v i n g i n d i v i d u a l s that a c o p y (not necessarily e x a c t ) of the o r i g i n a l m e m e is g r a v e n in the receiving brain. T h e n e w c o p y of the m e m e is then in a position to b r o a d c a s t its p h e n o t y p i c effects, w i t h t h e r e s u l t t h a t f u r t h e r c o p i e s o f i t s e l f m a y b e m a d e in yet other brains. R e t u r n i n g , for c l a r i f i c a t i o n ,
to D N A as our archetypal replicator,
its
consequences on the w o r l d are of t w o i m p o r t a n t types. Firstly, it m a k e s c o p i e s o f itself,
m a k i n g use o f t h e c e l l u l a r a p p a r a t u s
of replicases,
etc.
S e c o n d l y , i t h a s effects o n t h e o u t s i d e w o r l d , w h i c h i n f l u e n c e t h e c h a n c e s o f its c o p i e s ' s u r v i v i n g . T h e f i r s t o f these t w o effects c o r r e s p o n d s t o t h e m e m e ' s use o f t h e a p p a r a t u s o f i n t e r - i n d i v i d u a l
communication
and
imitation
to
no
O r g a n i s m s , G r o u p s and M e m e s : R e p l i c a t o r s o r V e h i c l e s ?
m a k e c o p i e s o f itself. I f i n d i v i d u a l s l i v e i n a s o c i a l c l i m a t e i n w h i c h i m i t a t i o n i s c o m m o n , this c o r r e s p o n d s t o a c e l l u l a r c l i m a t e r i c h i n e n z y m e s for c o p y i n g DNA. B u t w h a t a b o u t t h e s e c o n d k i n d o f effect o f D N A , t h e k i n d c o n v e n t i o n a l l y c a l l e d ' p h e n o t y p i c ' ? H o w d o a m e m e ' s p h e n o t y p i c effects c o n t r i b u t e t o its s u c c e s s o r f a i l u r e i n b e i n g r e p l i c a t e d ? T h e a n s w e r i s t h e s a m e a s for the g e n e t i c r e p l i c a t o r . A n y effect t h a t a m e m e h a s o n t h e b e h a v i o u r o f a b o d y b e a r i n g it m a y influence that m e m e ' s c h a n c e of surviving. A m e m e that m a d e its b o d i e s r u n o v e r cliffs w o u l d h a v e a fate l i k e t h a t o f a g e n e for m a k i n g its b o d i e s r u n o v e r cliffs. I t w o u l d t e n d t o b e e l i m i n a t e d from the m e m e - p o o l . B u t j u s t as p r o m o t i n g b o d i l y s u r v i v a l is only part of w h a t constitutes s u c c e s s i n g e n e t i c r e p l i c a t o r s , s o t h e r e a r e m a n y o t h e r w a y s i n w h i c h m e m e s m a y w o r k p h e n o t y p i c a l l y for t h e i r o w n p r e s e r v a t i o n . I f t h e p h e n o t y p i c effect of a m e m e is a t u n e , t h e c a t c h i e r it is t h e m o r e l i k e l y it is to be c o p i e d . If i t i s a s c i e n t i f i c i d e a , its c h a n c e s o f s p r e a d i n g t h r o u g h t h e w o r l d ' s scientific b r a i n s w i l l b e i n f l u e n c e d b y its c o m p a t i b i l i t y w i t h t h e a l r e a d y e s t a b l i s h e d c o r p u s o f i d e a s . I f i t i s a p o l i t i c a l o r r e l i g i o u s i d e a , i t m a y assist its o w n surv i v a l i f o n e o f its p h e n o t y p i c effects i s t o m a k e its b o d i e s v i o l e n t l y i n t o l e r a n t o f n e w a n d u n f a m i l i a r i d e a s . A m e m e h a s its o w n o p p o r t u n i t i e s for r e p l i c a t i o n , a n d its o w n p h e n o t y p i c effects, a n d t h e r e i s n o r e a s o n w h y s u c c e s s i n a m e m e should h a v e a n y c o n n e c t i o n w h a t e v e r with genetic success. T h i s is r e g a r d e d by m a n y of my biological correspondents as the weakest point in the w h o l e m e m e theory (Greene
1 9 7 8 ; A l e x a n d e r 1980, p . 7 8 ;
S t a d d o n i n p r e s s ) . I d o n ' t see t h e p r o b l e m ; o r , r a t h e r , I d o see t h e p r o b l e m b u t I d o n ' t t h i n k i t i s a n y g r e a t e r for m e m e s a s r e p l i c a t o r s t h a n i t i s for g e n e s . T i m e and again, my sociobiological colleagues have upbraided me as a t u r n c o a t , b e c a u s e I w i l l n o t a g r e e w i t h t h e m t h a t t h e ultimate c r i t e r i o n for the s u c c e s s o f a m e m e m u s t b e its c o n t r i b u t i o n t o D a r w i n i a n 'fitness'. A t b o t t o m , t h e y insist, a ' g o o d m e m e ' s p r e a d s b e c a u s e b r a i n s a r e r e c e p t i v e t o it, a n d the receptiveness of brains is ultimately shaped by (genetic) natural selection. T h e v e r y fact that a n i m a l s i m i t a t e other a n i m a l s a t all must u l t i m a t e l y b e explicable in terms of their D a r w i n i a n fitness. B u t t h e r e i s n o t h i n g m a g i c a b o u t D a r w i n i a n f i t n e s s i n t h e g e n e t i c sense. T h e r e is no l a w g i v i n g it priority as the f u n d a m e n t a l q u a n t i t y that is m a x i m i z e d . F i t n e s s i s j u s t a w a y o f t a l k i n g a b o u t the s u r v i v a l o f r e p l i c a t o r s , i n this c a s e g e n e t i c r e p l i c a t o r s . I f a n o t h e r k i n d o f e n t i t y arises, w h i c h a n s w e r s to
the definition of an
replicator that
active germ-line replicator,
w o r k for t h e i r o w n
survival
will
variants of the n e w
tend
to
become more
numerous. To be consistent, we could invent a new kind of 'individual f i t n e s s ' , w h i c h m e a s u r e d t h e s u c c e s s o f a n i n d i v i d u a l i n p r o p a g a t i n g his memes. I t is, o f c o u r s e , t r u e t h a t ' M e m e s a r e u t t e r l y d e p e n d e n t u p o n g e n e s , b u t g e n e s c a n exist a n d c h a n g e q u i t e i n d e p e n d e n t l y o f m e m e s ' ( B o n n e r 1980).
O r g a n i s m s , Groups and M e m e s : Replicators or Vehicles? 111
B u t this d o e s n o t m e a n
that the ultimate
c r i t e r i o n for s u c c e s s i n m e m e
selection is g e n e survival. It does not m e a n that success goes to those m e m e s t h a t f a v o u r t h e g e n e s o f t h e i n d i v i d u a l s b e a r i n g t h e m . T o b e s u r e , this w i l l s o m e t i m e s b e so. O b v i o u s l y a m e m e t h a t c a u s e s i n d i v i d u a l s b e a r i n g i t t o k i l l t h e m s e l v e s h a s a g r a v e d i s a d v a n t a g e , b u t n o t n e c e s s a r i l y a f a t a l o n e . J u s t as a g e n e for s u i c i d e s o m e t i m e s s p r e a d s i t s e l f b y a r o u n d a b o u t r o u t e ( e . g . i n s o c i a l insect workers, or p a r e n t a l sacrifice), so a suicidal m e m e c a n s p r e a d , as w h e n a d r a m a t i c a n d w e l l - p u b l i c i z e d m a r t y r d o m i n s p i r e s o t h e r s t o d i e for a d e e p l y l o v e d c a u s e , a n d this i n t u r n i n s p i r e s o t h e r s t o d i e , a n d s o o n ( V i d a l 1 9 5 5 ) . It is true that the relative survival success of a m e m e will d e p e n d critically o n t h e s o c i a l a n d b i o l o g i c a l c l i m a t e i n w h i c h i t f i n d s itself, a n d this c l i m a t e will certainly be influenced by the genetic m a k e - u p of the population. B u t it w i l l a l s o d e p e n d o n the m e m e s t h a t a r e a l r e a d y n u m e r o u s i n t h e m e m e - p o o l . Genetic
evolutionists
are
already
happy
with
the
idea
that
the
relative
success o f t w o a l l e l e s c a n d e p e n d u p o n w h i c h g e n e s a t o t h e r l o c i d o m i n a t e the g e n e - p o o l , a n d I h a v e a l r e a d y m e n t i o n e d this i n c o n n e c t i o n w i t h t h e evolution o f ' c o a d a p t e d g e n o m e s ' . T h e statistical structure o f the g e n e - p o o l sets u p a c l i m a t e o r e n v i r o n m e n t w h i c h affects t h e s u c c e s s o f a n y o n e g e n e r e l a t i v e t o its a l l e l e s . A g a i n s t o n e g e n e t i c b a c k g r o u n d o n e a l l e l e m a y b e f a v o u r e d ; a g a i n s t a n o t h e r g e n e t i c b a c k g r o u n d its a l l e l e m a y b e f a v o u r e d . For e x a m p l e , if the g e n e - p o o l is d o m i n a t e d by genes that m a k e a n i m a l s seek dry places,
this w i l l set u p s e l e c t i o n p r e s s u r e s i n f a v o u r o f g e n e s for a n
i m p e r m e a b l e s k i n . B u t a l l e l e s for a m o r e p e r m e a b l e s k i n w i l l b e f a v o u r e d i f the g e n e - p o o l h a p p e n s t o b e d o m i n a t e d b y g e n e s for s e e k i n g d a m p p l a c e s . The
point
is
the
obvious
one
that
selection
at
any
one
locus
is
not
independent of selection at other loci. O n c e a lineage begins e v o l v i n g in a p a r t i c u l a r d i r e c t i o n , m a n y l o c i w i l l fall i n t o s t e p , a n d t h e r e s u l t i n g p o s i t i v e feedbacks will tend to p r o p e l the lineage in the s a m e direction, in spite of pressures f r o m t h e o u t s i d e w o r l d . A n i m p o r t a n t a s p e c t o f t h e e n v i r o n m e n t w h i c h selects b e t w e e n a l l e l e s a t a n y o n e l o c u s w i l l b e t h e g e n e s t h a t a l r e a d y d o m i n a t e the g e n e - p o o l a t o t h e r l o c i . Similarly, an important aspect of selection on a n y one m e m e will be the other
memes
that
already
happen
to
dominate
the
meme-pool
(Wilson
1 9 7 5 ) . I f the society i s a l r e a d y d o m i n a t e d b y M a r x i s t , o r N a z i m e m e s , a n y n e w m e m e ' s r e p l i c a t i o n s u c c e s s w i l l b e i n f l u e n c e d b y its c o m p a t i b i l i t y w i t h this e x i s t i n g b a c k g r o u n d . P o s i t i v e f e e d b a c k s w i l l p r o v i d e a m o m e n t u m w h i c h can carry meme-based evolution in directions unconnected with, or even contradictory
to,
the
directions
that
would
be
favoured
by
gene-based
evolution. I agree w i t h P u l l i a m and D u n f o r d (1980) that cultural e v o l u t i o n ' o w e s its o r i g i n a n d its r u l e s t o g e n e t i c e v o l u t i o n , b u t i t h a s a m o m e n t u m a l l its o w n ' . There
are,
of course,
significant
gene-based selection processes
differences
(Cavalli-Sforza
between &
meme-based
Feldman
1973,
and
1981).
112
O r g a n i s m s , G r o u p s and M e m e s : R e p l i c a t o r s o r V e h i c l e s ?
M e m e s are not strung out a l o n g linear c h r o m o s o m e s , a n d it is not clear that t h e y o c c u p y a n d c o m p e t e for d i s c r e t e ' l o c i ' , o r t h a t t h e y h a v e i d e n t i f i a b l e 'alleles'. P r e s u m a b l y , as in the case of genes, we c a n strictly only talk a b o u t p h e n o t y p i c effects i n t e r m s o f d i f f e r e n c e s , e v e n i f w e j u s t m e a n t h e d i f f e r e n c e b e t w e e n the b e h a v i o u r p r o d u c e d by a brain c o n t a i n i n g the m e m e a n d that of a b r a i n n o t c o n t a i n i n g it. T h e c o p y i n g p r o c e s s i s p r o b a b l y m u c h less p r e c i s e than in the case of g e n e s : there m a y be a certain 'mutational' element in e v e r y c o p y i n g e v e n t , a n d this, b y t h e w a y , i s a l s o t r u e o f t h e ' s p e c i e s selection' discussed earlier in the c h a p t e r . M e m e s m a y partially blend with e a c h other in a w a y that genes do not. N e w 'mutations' m a y be 'directed' rather than r a n d o m w i t h respect to evolutionary trends. T h e equivalent of Weismannism
is
less
rigid
for
memes
than
for
genes:
there
may
be
' L a m a r c k i a n ' c a u s a l a r r o w s l e a d i n g from p h e n o t y p e to replicator, as well as t h e o t h e r w a y a r o u n d . T h e s e d i f f e r e n c e s m a y p r o v e sufficient t o r e n d e r the analogy
with
genetic
natural
selection
worthless
or
even
positively
m i s l e a d i n g . M y o w n f e e l i n g i s t h a t its m a i n v a l u e m a y lie n o t s o m u c h i n helping us to understand h u m a n culture as in sharpening our perception of genetic natural selection. T h i s is the only reason I am presumptuous enough t o d i s c u s s it, for I d o n o t k n o w n e n o u g h a b o u t t h e e x i s t i n g l i t e r a t u r e o n h u m a n c u l t u r e t o m a k e a n a u t h o r i t a t i v e c o n t r i b u t i o n t o it. W h a t e v e r t h e c l a i m s o f m e m e s t o b e r e g a r d e d a s r e p l i c a t o r s i n the s a m e sense a s g e n e s ,
t h e f i r s t p a r t o f this c h a p t e r e s t a b l i s h e d
that individual
organisms are not replicators. Nevertheless, they are obviously functional units of g r e a t i m p o r t a n c e , a n d it is n o w necessary to establish e x a c t l y w h a t t h e i r r o l e is. I f t h e o r g a n i s m i s n o t a r e p l i c a t o r , w h a t i s i t ? T h e a n s w e r i s t h a t it is a c o m m u n a l vehicle for r e p l i c a t o r s . A v e h i c l e is an e n t i t y in w h i c h replicators (genes a n d m e m e s ) travel a b o u t , an entity whose attributes are a f f e c t e d b y t h e r e p l i c a t o r s i n s i d e it, a n e n t i t y w h i c h m a y b e seen a s a c o m p o u n d tool of replicator p r o p a g a t i o n . B u t i n d i v i d u a l organisms are not t h e o n l y e n t i t i e s t h a t m i g h t b e r e g a r d e d a s v e h i c l e s i n this sense. T h e r e i s a h i e r a r c h y of entities e m b e d d e d in larger entities, a n d in theory the c o n c e p t of v e h i c l e m i g h t b e a p p l i e d t o a n y level o f the h i e r a r c h y . T h e concept of hierarchy is a generally important one. Chemists believe t h a t m a t t e r i s m a d e o f a b o u t a h u n d r e d different k i n d s o f a t o m s , i n t e r a c t i n g w i t h e a c h other by m e a n s of their electrons. A t o m s are gregarious, forming h u g e assemblages w h i c h are g o v e r n e d by laws at their o w n level. W i t h o u t c o n t r a d i c t i n g the laws of chemistry, therefore, we find it convenient to ignore atoms w h e n we are thinking about large lumps of matter. W h e n explaining t h e w o r k i n g s o f a m o t o r c a r w e f o r g e t a t o m s a n d v a n d e r W a a l ' s forces a s units of e x p l a n a t i o n , a n d prefer to talk of cylinders and sparking plugs. T h i s lesson a p p l i e s n o t j u s t t o t h e t w o l e v e l s o f a t o m s a n d c y l i n d e r h e a d s . T h e r e i s a h i e r a r c h y , r a n g i n g from f u n d a m e n t a l particles b e l o w the a t o m i c level up
O r g a n i s m s , G r o u p s and M e m e s : Replicators or V e h i c l e s ?
through
molecules
and
crystals
to
the
macroscopic
chunks
113
which
our
u n a i d e d sense o r g a n s a r e b u i l t t o a p p r e c i a t e . Living matter introduces complexity:
a w h o l e n e w set o f r u n g s
to
the
ladder of
m a c r o m o l e c u l e s folding themselves into their tertiary forms,
intracellular membranes and organelles, populations,
communities
and
cells,
ecosystems.
A
tissues, o r g a n s , o r g a n i s m s , similar
hierarchy
of units
e m b e d d e d in larger units e p i t o m i z e s the c o m p l e x artificial p r o d u c t s of l i v i n g things—semiconductor crystals,
transistors,
integrated
circuits,
computers
and e m b e d d e d units that c a n o n l y b e u n d e r s t o o d i n terms o f 'software'. A t every level the units interact w i t h e a c h other f o l l o w i n g laws a p p r o p r i a t e to that level, l a w s w h i c h are not c o n v e n i e n t l y r e d u c i b l e to l a w s at l o w e r levels. T h i s has all b e e n said m a n y times before, a n d is so o b v i o u s as to be a l m o s t platitudinous. B u t one sometimes has to repeat platitudes in o r d e r to p r o v e that one's heart is in the right p l a c e ! E s p e c i a l l y if o n e wishes to e m p h a s i z e a s l i g h t l y u n c o n v e n t i o n a l sort o f h i e r a r c h y , for this m a y b e m i s t a k e n for a ' r e d u c t i o n i s t ' a t t a c k o n t h e i d e a o f h i e r a r c h y itself. R e d u c t i o n i s m i s a d i r t y word,
and
a
fashionable.
kind I
of 'holistier than
enthusiastically
follow
thou'
self-righteousness
this
fashion
when
has
talking
become about
mechanisms within individual bodies, and have a d v o c a t e d 'neuro-economic' and
'software'
explanations
neurophysiological ones approach
of behaviour
(Dawkins
1976b).
to individual development.
in
preference
to
conventional
I w o u l d favour an analogous
B u t there
are
times
w h e n holistic
p r e a c h i n g b e c o m e s a n e a s y s u b s t i t u t e for t h o u g h t , a n d I b e l i e v e t h e d i s p u t e a b o u t u n i t s o f s e l e c t i o n p r o v i d e s e x a m p l e s o f this. T h e n e o - W e i s m a n n i s t v i e w o f life w h i c h this b o o k a d v o c a t e s l a y s stress o n the g e n e t i c r e p l i c a t o r a s a f u n d a m e n t a l u n i t o f e x p l a n a t i o n . I b e l i e v e i t h a s an atom-like role to p l a y in functional, t e l e o n o m i c e x p l a n a t i o n . If we wish to s p e a k o f a d a p t a t i o n s a s b e i n g 'for t h e g o o d o f s o m e t h i n g , t h a t s o m e t h i n g i s the a c t i v e , g e r m - l i n e r e p l i c a t o r . T h i s i s a s m a l l c h u n k o f D N A , a s i n g l e ' g e n e ' a c c o r d i n g to some definitions of the w o r d . B u t I am of course not s u g g e s t i n g that small genetic units w o r k in isolation from e a c h other, a n y m o r e than a chemist thinks that atoms d o . L i k e atoms, genes are h i g h l y g r e g a r i o u s . T h e y a r e often s t r u n g t o g e t h e r a l o n g c h r o m o s o m e s , c h r o m o s o m e s a r e w r a p p e d u p in groups in nuclear membranes, enveloped in cytoplasm and enclosed in cell m e m b r a n e s . C e l l s too are n o r m a l l y not isolated, b u t c l o n e d to form the h u g e conglomerates we k n o w as organisms. We are n o w p l u g g e d into the familiar e m b e d d e d hierarchy, and need go no further. F u n c t i o n a l l y s p e a k i n g , too, g e n e s a r e g r e g a r i o u s . T h e y h a v e p h e n o t y p i c effects o n b o d i e s , b u t t h e y d o n o t d o s o i n i s o l a t i o n . I stress this o v e r a n d o v e r a g a i n i n this b o o k . T h e r e a s o n I m a y s o u n d r e d u c t i o n i s t i c i s t h a t I insist o n a n a t o m i s t i c v i e w o f units o f s e l e c t i o n , i n t h e sense o f t h e u n i t s t h a t a c t u a l l y s u r v i v e o r fail t o
O r g a n i s m s , G r o u p s and M e m e s : Replicators or Vehicles?
114
s u r v i v e , w h i l e b e i n g w h o l e - h e a r t e d l y i n t e r a c t i o n i s t w h e n i t c o m e s t o the d e v e l o p m e n t o f t h e p h e n o t y p i c means b y w h i c h t h e y s u r v i v e : Of course
it
is
true
that
the
phenotypic
effect
of a
gene
is
a
m e a n i n g l e s s c o n c e p t o u t s i d e t h e c o n t e x t o f m a n y , o r e v e n a l l , o f the o t h e r g e n e s i n t h e g e n o m e . Y e t , h o w e v e r c o m p l e x a n d i n t r i c a t e the o r g a n i s m m a y be, h o w e v e r m u c h w e m a y a g r e e that the organism i s a u n i t of function, selection.
Genes
I still t h i n k it is m i s l e a d i n g to c a l l it a u n i t of may
interact,
even
"blend",
in
their
effects
on
e m b r y o n i c d e v e l o p m e n t , as m u c h as y o u please. But they do not b l e n d w h e n it c o m e s to b e i n g passed on to future generations. I am n o t t r y i n g to belittle the i m p o r t a n c e of the i n d i v i d u a l p h e n o t y p e in e v o l u t i o n . I a m m e r e l y t r y i n g t o sort o u t e x a c t l y w h a t its r o l e is. I t i s t h e a l l i m p o r t a n t i n s t r u m e n t of r e p l i c a t o r p r e s e r v a t i o n : it is not t h a t w h i c h is preserved [Dawkins 1978a, p. 69].
I n this b o o k I a m u s i n g t h e w o r d ' v e h i c l e ' for a n i n t e g r a t e d a n d c o h e r e n t 'instrument of replicator preservation'. A v e h i c l e is a n y unit, discrete e n o u g h to seem w o r t h n a m i n g , w h i c h houses a c o l l e c t i o n o f r e p l i c a t o r s a n d w h i c h w o r k s a s a u n i t for t h e p r e s e r v a t i o n a n d p r o p a g a t i o n of t h o s e r e p l i c a t o r s . I r e p e a t , a v e h i c l e is n o t a r e p l i c a t o r . A r e p l i c a t o r ' s s u c c e s s i s m e a s u r e d b y its c a p a c i t y t o s u r v i v e i n t h e f o r m o f c o p i e s . A v e h i c l e ' s s u c c e s s i s m e a s u r e d b y its c a p a c i t y t o p r o p a g a t e t h e r e p l i c a t o r s t h a t r i d e i n s i d e it. T h e o b v i o u s a n d a r c h e t y p a l v e h i c l e i s t h e i n d i v i d u a l o r g a n i s m , b u t this m a y n o t b e t h e o n l y l e v e l i n t h e h i e r a r c h y o f life a t w h i c h t h e title i s a p p l i c a b l e . W e c a n e x a m i n e a s c a n d i d a t e v e h i c l e s c h r o m o s o m e s a n d cells b e l o w the o r g a n i s m level, g r o u p s a n d c o m m u n i t i e s a b o v e it. A t a n y l e v e l , i f a v e h i c l e i s d e s t r o y e d , a l l t h e r e p l i c a t o r s inside i t w i l l b e d e s t r o y e d . N a t u r a l s e l e c t i o n w i l l t h e r e f o r e , a t least t o s o m e e x t e n t , f a v o u r r e p l i c a t o r s t h a t c a u s e t h e i r v e h i c l e s t o resist b e i n g d e s t r o y e d . p r i n c i p l e this c o u l d
In
a p p l y to g r o u p s of o r g a n i s m s as w e l l as to single
o r g a n i s m s , for i f a g r o u p i s d e s t r o y e d a l l t h e g e n e s i n s i d e i t a r e d e s t r o y e d t o o . V e h i c l e survival i s o n l y p a r t o f t h e s t o r y , h o w e v e r . R e p l i c a t o r s t h a t w o r k for t h e ' r e p r o d u c t i o n ' o f v e h i c l e s a t v a r i o u s l e v e l s m i g h t t e n d t o d o b e t t e r t h a n r i v a l r e p l i c a t o r s t h a t w o r k m e r e l y for v e h i c l e s u r v i v a l . R e p r o d u c t i o n a t the
organism
level
is
familiar
enough
to
need
no
further
discussion.
R e p r o d u c t i o n at the g r o u p level is more problematic. In principle a group m a y b e s a i d t o h a v e r e p r o d u c e d i f i t s e n d s off a ' p r o p a g u l e ' , s a y a b a n d o f y o u n g o r g a n i s m s w h o g o o u t a n d found a n e w g r o u p . T h e i d e a o f a nested h i e r a r c h y of levels at w h i c h selection m i g h t take p l a c e — v e h i c l e selection in my terms—is e m p h a s i z e d in W i l s o n ' s (1975) c h a p t e r on g r o u p selection (e.g. his f i g u r e 5 - 1 ) . I h a v e p r e v i o u s l y g i v e n r e a s o n s for s h a r i n g i n t h e g e n e r a l s c e p t i c i s m a b o u t
O r g a n i s m s , G r o u p s and M e m e s : R e p l i c a t o r s o r V e h i c l e s ?
115
' g r o u p selection' a n d selection at other h i g h levels, a n d n o t h i n g in the recent l i t e r a t u r e t e m p t s m e t o c h a n g e m y m i n d . B u t t h a t i s n o t t h e p o i n t a t issue here. T h e point here is that we must be clear a b o u t the difference b e t w e e n those t w o d i s t i n c t k i n d s o f c o n c e p t u a l u n i t s , r e p l i c a t o r s a n d v e h i c l e s . I h a v e s u g g e s t e d t h a t t h e best w a y o f u n d e r s t a n d i n g E l d r e d g e a n d G o u l d ' s t h e o r y o f ' s p e c i e s s e l e c t i o n ' i s i n t e r m s o f s p e c i e s a s replicators. B u t t h e m a j o r i t y o f models ordinarily called ' g r o u p selection', i n c l u d i n g all those r e v i e w e d by W i l s o n ( 1 9 7 5 ) , a n d most o f those r e v i e w e d b y W a d e ( 1 9 7 8 ) , are i m p l i c i t l y t r e a t i n g g r o u p s a s v e h i c l e s . T h e e n d result o f t h e s e l e c t i o n d i s c u s s e d i s a c h a n g e i n g e n e f r e q u e n c i e s , for e x a m p l e a n i n c r e a s e o f ' a l t r u i s t i c g e n e s ' a t t h e e x p e n s e o f 'selfish g e n e s ' .
I t i s still g e n e s t h a t a r e r e g a r d e d a s t h e
r e p l i c a t o r s w h i c h a c t u a l l y s u r v i v e (or fail t o s u r v i v e ) a s a c o n s e q u e n c e o f t h e (vehicle) selection process. A s for g r o u p s e l e c t i o n itself, m y p r e j u d i c e i s t h a t i t h a s s o a k e d u p m o r e t h e o r e t i c a l i n g e n u i t y t h a n its b i o l o g i c a l i n t e r e s t w a r r a n t s . I a m i n f o r m e d b y the e d i t o r o f a l e a d i n g m a t h e m a t i c s j o u r n a l t h a t h e i s c o n t i n u a l l y p l a g u e d b y ingenious papers p u r p o r t i n g to h a v e s q u a r e d the circle. S o m e t h i n g a b o u t the fact t h a t this h a s b e e n p r o v e d t o b e i m p o s s i b l e i s s e e n a s a n i r r e s i s t i b l e challenge
by
a
certain
type
of intellectual
dilettante.
Perpetual
motion
m a c h i n e s h a v e a s i m i l a r f a s c i n a t i o n for s o m e a m a t e u r i n v e n t o r s . T h e c a s e o f group
selection
is
hardly
analogous:
it
has
never
been
proved
to
be
i m p o s s i b l e , a n d n e v e r c o u l d b e . N e v e r t h e l e s s , I h o p e I m a y b e f o r g i v e n for w o n d e r i n g w h e t h e r part of g r o u p selection's e n d u r i n g r o m a n t i c a p p e a l stems from the a u t h o r i t a t i v e h a m m e r i n g t h e t h e o r y h a s r e c e i v e d e v e r s i n c e W y n n e E d w a r d s (1962) did us the v a l u a b l e service of b r i n g i n g it out into the open. Anti-group
selectionism
has
been
embraced
orthodox, and, as M a y n a r d Smith
(1976a)
by
notes,
the
establishment
as
'It is in the nature of
science that o n c e a position b e c o m e s o r t h o d o x it should be subjected to c r i t i c i s m . . . ' T h i s is, n o d o u b t , h e a l t h y , b u t M a y n a r d S m i t h d r i l y g o e s o n : 'It does not follow that, b e c a u s e a position is o r t h o d o x , it is w r o n g . . . ' M o r e generous recent treatments of g r o u p selection are g i v e n by G i l p i n ( 1 9 7 5 ) , E. O. Wilson (1975), W a d e (1978), Boorman and Levitt (1980), and D. S. W i l s o n ( 1 9 8 0 , b u t see c r i t i c i s m b y G r a f e n 1 9 8 0 , i n p r e s s ) . I am not g o i n g to go a g a i n into the d e b a t e o v e r g r o u p selection versus i n d i v i d u a l s e l e c t i o n . T h i s i s b e c a u s e t h e m a i n p u r p o s e o f this b o o k i s t o d r a w attention to the weaknesses of the w h o l e v e h i c l e c o n c e p t , w h e t h e r the v e h i c l e is an individual organism or a g r o u p .
S i n c e e v e n the staunchest g r o u p
s e l e c t i o n i s t w o u l d a g r e e t h a t t h e i n d i v i d u a l o r g a n i s m i s a far m o r e c o h e r e n t and
important
'unit of selection',
I
shall c o n c e n t r a t e my a t t a c k on
the
individual organism as my representative vehicle, rather than on the g r o u p . T h e case against the g r o u p should b e strengthened b y default. It m a y seem that I h a v e invented my o w n c o n c e p t , the v e h i c l e , as an A u n t S a l l y t o b e e a s i l y k n o c k e d d o w n . T h i s i s n o t so. I s i m p l y use t h e n a m e v e h i c l e
116
O r g a n i s m s , G r o u p s and M e m e s : Replicators or Vehicles?
to g i v e expression to a c o n c e p t w h i c h is f u n d a m e n t a l to the p r e d o m i n a n t orthodox
approach
to
natural
selection.
It
is
admitted
that,
in
some
f u n d a m e n t a l s e n s e , n a t u r a l s e l e c t i o n consists i n t h e d i f f e r e n t i a l s u r v i v a l o f g e n e s (or l a r g e r g e n e t i c r e p l i c a t o r s ) . B u t g e n e s a r e n o t n a k e d , t h e y w o r k t h r o u g h b o d i e s (or g r o u p s , e t c . ) . A l t h o u g h t h e u l t i m a t e u n i t o f s e l e c t i o n m a y i n d e e d be the genetic replicator, the p r o x i m a l unit of selection is usually regarded as something larger, usually an individual organism. T h u s M a y r (1963) d e v o t e s a w h o l e c h a p t e r to d e m o n s t r a t i n g the functional c o h e r e n c e of the w h o l e g e n o m e of an i n d i v i d u a l o r g a n i s m . I shall discuss M a y r ' s points in d e t a i l i n C h a p t e r 1 3 . F o r d ( 1 9 7 5 , p . 185) d i s d a i n f u l l y w r i t e s o f f t h e ' e r r o r ' that 'the unit of selection is the g e n e , w h e r e a s it is the i n d i v i d u a l ' . G o u l d (1977b) says:
S e l e c t i o n s i m p l y c a n n o t see g e n e s a n d p i c k a m o n g t h e m d i r e c t l y . I t must use bodies as an i n t e r m e d i a r y . A g e n e is a bit of D N A hidden w i t h i n a cell. S e l e c t i o n views bodies. It favors some bodies because they are stronger, better insulated, earlier in their sexual maturation, fiercer in c o m b a t , or m o r e b e a u t i f u l to b e h o l d . . . If, in f a v o r i n g a s t r o n g e r b o d y , s e l e c t i o n a c t e d d i r e c t l y u p o n a g e n e for s t r e n g t h , t h e n D a w k i n s might be vindicated. If bodies were u n a m b i g u o u s maps of t h e i r g e n e s , t h e n b a t t l i n g bits o f D N A w o u l d d i s p l a y t h e i r c o l o r s e x t e r n a l l y a n d selection m i g h t act u p o n t h e m directly. B u t bodies are no
such
t h i n g . . . Bodies
cannot
be
atomized
into
parts,
each
constructed by an individual gene. Hundreds of genes contribute to the b u i l d i n g of most b o d y parts and their action is channeled through a k a l e i d o s c o p i c series o f e n v i r o n m e n t a l i n f l u e n c e s :
embryonic and
postnatal, internal and external.
N o w i f this w e r e r e a l l y a g o o d a r g u m e n t , i t w o u l d b e a n a r g u m e n t a g a i n s t t h e w h o l e o f M e n d e l i a n g e n e t i c s , j u s t a s m u c h a s a g a i n s t t h e i d e a o f the g e n e as the unit of selection. T h e L a m a r c k i a n fanatic H. G. C a n n o n , indeed, e x p l i c i t l y uses i t a s s u c h : ' A l i v i n g b o d y i s n o t s o m e t h i n g i s o l a t e d , n e i t h e r i s i t a c o l l e c t i o n of p a r t s as D a r w i n e n v i s a g e d it, l i k e , as I h a v e s a i d b e f o r e , so m a n y m a r b l e s in a b o x . T h a t is the t r a g e d y of m o d e r n genetics. T h e devotees of the n e o - M e n d e l i a n hypothesis regard the o r g a n i s m as so m a n y characters c o n t r o l l e d b y s o m a n y g e n e s . S a y w h a t t h e y like a b o u t p o l y g e n e s — t h a t i s t h e essence of their fantastic hypothesis' ( C a n n o n 1959, p. 1 3 1 ) . Most
people
would
agree
that
this
is
not
a
good
argument
against
M e n d e l i a n g e n e t i c s , a n d n o m o r e i s i t a g o o d a r g u m e n t a g a i n s t t r e a t i n g the g e n e as the unit of selection. T h e mistake w h i c h both G o u l d and C a n n o n m a k e i s t h a t t h e y fail t o d i s t i n g u i s h g e n e t i c s f r o m e m b r y o l o g y . M e n d e l i s m i s a
theory
of
particulate
inheritance,
not
particulate
embryology.
The
a r g u m e n t of C a n n o n and G o u l d is a valid argument against particulate
O r g a n i s m s , G r o u p s and M e m e s : R e p l i c a t o r s o r V e h i c l e s ?
117
embryology and in favour of blending e m b r y o l o g y . I myself give similar a r g u m e n t s e l s e w h e r e i n this b o o k ( e . g . t h e c a k e a n a l o g y i n t h e s e c t i o n o f Chapter 9 called ' T h e poverty of preformationism'). Genes do indeed blend, a s far a s t h e i r effects o n d e v e l o p i n g p h e n o t y p e s a r e c o n c e r n e d . B u t , a s I h a v e already e m p h a s i z e d sufficiently,
t h e y d o not b l e n d a s t h e y r e p l i c a t e a n d
r e c o m b i n e d o w n t h e g e n e r a t i o n s . I t i s this t h a t m a t t e r s for t h e g e n e t i c i s t , a n d i t i s also this t h a t m a t t e r s for the s t u d e n t o f u n i t s o f s e l e c t i o n . G o u l d goes o n : So parts are not translated genes, and selection doesn't e v e n w o r k d i r e c t l y o n p a r t s . I t a c c e p t s o r rejects e n t i r e o r g a n i s m s b e c a u s e suites o f parts, interacting i n c o m p l e x w a y s , confer a d v a n t a g e s . T h e i m a g e o f i n d i v i d u a l g e n e s , p l o t t i n g the c o u r s e o f t h e i r o w n s u r v i v a l , b e a r s little r e l a t i o n s h i p Dawkins
will
t o d e v e l o p m e n t a l g e n e t i c s a s w e u n d e r s t a n d it.
need
another
metaphor:
genes
caucusing,
forming
a l l i a n c e s , s h o w i n g d e f e r e n c e for a c h a n c e t o j o i n a p a c t , g a u g i n g probable environments. But w h e n you a m a l g a m a t e so m a n y genes a n d tie t h e m t o g e t h e r i n h i e r a r c h i c a l c h a i n s o f a c t i o n m e d i a t e d b y environments, we call the resultant object a b o d y . G o u l d comes closer to the truth here, but the truth is subtler, as I h o p e to show in C h a p t e r
13. T h e point was alluded to in the previous chapter.
B r i e f l y , t h e sense i n w h i c h g e n e s m a y b e s a i d t o ' c a u c u s ' a n d f o r m ' a l l i a n c e s ' is the f o l l o w i n g . S e l e c t i o n f a v o u r s t h o s e g e n e s w h i c h s u c c e e d in the presence of other genes, which in turn succeed in the presence of them.
Therefore mutually
c o m p a t i b l e sets o f g e n e s a r i s e i n g e n e - p o o l s . T h i s i s m o r e s u b t l e a n d m o r e useful t h a n t o s a y t h a t ' w e c a l l t h e r e s u l t a n t o b j e c t a b o d y ' . Of course g e n e s a r e n o t d i r e c t l y v i s i b l e to s e l e c t i o n .
Obviously t h e y a r e
s e l e c t e d b y v i r t u e o f t h e i r p h e n o t y p i c effects, a n d c e r t a i n l y t h e y c a n o n l y b e said t o have p h e n o t y p i c effects i n c o n c e r t w i t h h u n d r e d s o f o t h e r g e n e s . B u t i t i s t h e thesis o f this b o o k t h a t w e s h o u l d n o t b e t r a p p e d i n t o a s s u m i n g t h a t those p h e n o t y p i c effects a r e best r e g a r d e d a s b e i n g n e a t l y w r a p p e d u p i n d i s c r e t e b o d i e s (or o t h e r d i s c r e t e v e h i c l e s ) . T h e d o c t r i n e o f t h e e x t e n d e d p h e n o t y p e is t h a t t h e p h e n o t y p i c effect of a g e n e ( g e n e t i c r e p l i c a t o r ) is b e s t seen a s a n effect u p o n t h e w o r l d a t l a r g e , a n d o n l y i n c i d e n t a l l y u p o n t h e i n d i v i d u a l o r g a n i s m — o r a n y o t h e r v e h i c l e — i n w h i c h i t h a p p e n s t o sit.
7 Selfish W a s p or Selfish Strategy?
T h i s is a chapter about practical research m e t h o d o l o g y . T h e r e will be t h o s e w h o a c c e p t t h e thesis o f this b o o k a t a t h e o r e t i c a l l e v e l b u t w h o w i l l o b j e c t t h a t , i n p r a c t i c e , f i e l d w o r k e r s f i n d i t useful t o focus t h e i r a t t e n t i o n o n individual a d v a n t a g e . In a t h e o r e t i c a l sense, t h e y w i l l s a y , it is r i g h t to see the natural w o r l d as a b a t t l e g r o u n d of replicators, but in real research we are obliged
to
measure
and
compare
the
D a r w i n i a n fitness of individual
o r g a n i s m s . I w a n t to discuss a p a r t i c u l a r piece of research in detail to show t h a t this i s n o t n e c e s s a r i l y t h e c a s e . I n s t e a d o f c o m p a r i n g t h e s u c c e s s o f i n d i v i d u a l o r g a n i s m s , i t i s often i n p r a c t i c e m o r e useful t o c o m p a r e t h e success of 'strategies' ( M a y n a r d S m i t h 1974) or ' p r o g r a m s ' or 'subroutines', averaged
across
the individuals
that
use
them.
O f the
many
pieces of
r e s e a r c h t h a t I c o u l d h a v e d i s c u s s e d , for i n s t a n c e t h e w o r k o n ' o p t i m a l foraging' (Pyke, Pulliam & C h a r n o v 1 9 7 7 ; K r e b s 1978), Parker's (1978a) d u n g f l i e s , o r a n y o f t h e e x a m p l e s r e v i e w e d b y D a v i e s (in p r e s s ) , I c h o o s e B r o c k m a n n ' s study of digger wasps purely because I am very familiar with it (Brockmann,
Grafen
&
Dawkins
1979;
Brockmann
&
Dawkins
1979;
D a w k i n s & B r o c k m a n n 1980). I s h a l l use t h e w o r d ' p r o g r a m ' i n e x a c t l y t h e s a m e sense a s M a y n a r d S m i t h uses ' s t r a t e g y ' .
I prefer ' p r o g r a m ' to 'strategy' because experience
w a r n s t h a t ' s t r a t e g y ' i s q u i t e l i k e l y t o b e m i s u n d e r s t o o d , i n a t least t w o different English
ways
Dictionary
(Dawkins and
1980).
standard
And
incidentally,
American
usage,
I
following prefer
the
Oxford
'program'
to
' p r o g r a m m e ' w h i c h a p p e a r s to be a nineteenth-century affectation imported f r o m t h e F r e n c h . A p r o g r a m (or s t r a t e g y ) is a r e c i p e for a c t i o n , a set of notional instructions that an a n i m a l seems to be ' o b e y i n g ' , just as a computer o b e y s its p r o g r a m . A c o m p u t e r p r o g r a m m e r w r i t e s o u t his p r o g r a m i n a l a n g u a g e s u c h a s A l g o l o r F o r t r a n , w h i c h m a y l o o k r a t h e r like i m p e r a t i v e E n g l i s h . T h e m a c h i n e r y o f t h e c o m p u t e r i s s o set u p t h a t i t b e h a v e s a s i f 118
Selfish W a s p or Selfish S t r a t e g y ?
119
o b e y i n g these q u a s i - E n g l i s h i n s t r u c t i o n s . B e f o r e i t c a n r u n , t h e p r o g r a m i s t r a n s l a t e d ( b y c o m p u t e r ) i n t o a set o f m o r e e l e m e n t a r y ' m a c h i n e l a n g u a g e ' instructions, closer to the h a r d w a r e a n d further from easy h u m a n c o m p r e h e n sion. I n a sense i t i s these m a c h i n e l a n g u a g e i n s t r u c t i o n s t h a t a r e ' a c t u a l l y ' o b e y e d r a t h e r t h a n t h e q u a s i - E n g l i s h p r o g r a m , a l t h o u g h i n a n o t h e r sense b o t h a r e o b e y e d , a n d i n y e t a n o t h e r sense n e i t h e r i s ! A person w a t c h i n g a n d a n a l y s i n g the b e h a v i o u r of a c o m p u t e r w h o s e program
had
been
lost m i g h t ,
in
principle,
be able
to reconstruct the
p r o g r a m o r its f u n c t i o n a l e q u i v a l e n t . T h e last f o u r w o r d s a r e c r u c i a l . F o r his o w n convenience he will write the reconstructed p r o g r a m in some particular l a n g u a g e — A l g o l , Fortran, a flow chart, some p a r t i c u l a r rigorous subset of English. B u t there is no w a y of k n o w i n g in w h i c h , if a n y , of these l a n g u a g e s the p r o g r a m w a s o r i g i n a l l y w r i t t e n . I t m a y h a v e b e e n d i r e c t l y w r i t t e n i n m a c h i n e l a n g u a g e , or ' h a r d - w i r e d ' into the m a c h i n e r y of the c o m p u t e r at m a n u f a c t u r e . T h e end result is the s a m e in a n y c a s e : the c o m p u t e r performs s o m e useful task s u c h a s c a l c u l a t i n g s q u a r e r o o t s , a n d a h u m a n c a n u s e f u l l y t r e a t t h e c o m p u t e r as if it w a s ' o b e y i n g ' a set of i m p e r a t i v e i n s t r u c t i o n s w r i t t e n o u t in a l a n g u a g e t h a t is c o n v e n i e n t for h u m a n s to u n d e r s t a n d . I t h i n k t h a t for m a n y p u r p o s e s s u c h
'software explanations'
of behaviour
m e c h a n i s m s a r e j u s t a s v a l i d a n d useful a s t h e m o r e o b v i o u s ' h a r d w a r e explanations' favoured by neurophysiologists. A biologist looking at an a n i m a l is in s o m e w h a t the s a m e position as an e n g i n e e r l o o k i n g a t a c o m p u t e r r u n n i n g a lost p r o g r a m . T h e a n i m a l i s behaving in w h a t appears to be an organized, purposeful w a y , as if it was obeying a program, an orderly sequence of imperative instructions. T h e a n i m a l ' s p r o g r a m h a s n o t a c t u a l l y b e e n lost, for i t n e v e r w a s w r i t t e n o u t . R a t h e r , natural selection c o b b l e d together the e q u i v a l e n t of a h a r d - w i r e d machine code
program,
by
favouring mutations
generations of nervous systems to b e h a v e
that
altered
successive
(and to learn to c h a n g e their
b e h a v i o u r ) i n a p p r o p r i a t e w a y s . A p p r o p r i a t e m e a n s , i n this c a s e , a p p r o p r i a t e for the s u r v i v a l
and
p r o p a g a t i o n of the genes
concerned.
Nevertheless,
although no p r o g r a m was ever written d o w n , just as in the case of the c o m p u t e r r u n n i n g a p r o g r a m w h i c h h a s b e e n lost, i t i s c o n v e n i e n t for u s t o think
of the
animal
as
'obeying'
a
program
'written'
in
some
easily
understood l a n g u a g e such as English. O n e of the things we c a n then do is to imagine alternative programs or subroutines w h i c h might 'compete' with e a c h o t h e r for ' c o m p u t e r t i m e ' i n the n e r v o u s s y s t e m s o f t h e p o p u l a t i o n . T h o u g h we must treat the a n a l o g y w i t h c i r c u m s p e c t i o n , as I shall s h o w , we can
usefully
alternative
imagine natural selection
programs
or
subroutines,
as
and
acting directly treat
individual
on
pool
of
organisms
a
as
t e m p o r a r y e x e c u t o r s a n d p r o p a g a t o r s o f these a l t e r n a t i v e p r o g r a m s . I n a p a r t i c u l a r m o d e l o f a n i m a l f i g h t i n g , for e x a m p l e , M a y n a r d S m i t h ( 1 9 7 2 , p . 19) p o s t u l a t e d five a l t e r n a t i v e ' s t r a t e g i e s ' ( p r o g r a m s ) :
1 2 0
Selfish W a s p o r Selfish S t r a t e g y ?
1 F i g h t c o n v e n t i o n a l l y ; retreat if o p p o n e n t proves to be stronger or if opponent escalates. 2 Fight at escalated level. Retreat only if injured. 3 Start c o n v e n t i o n a l l y . Escalate only if opponent escalates. 4 Start conventionally.
Escalate only if opponent continues to fight
conventionally. 5 F i g h t at escalated level. R e t r e a t before getting hurt if opponent does likewise. F o r t h e p u r p o s e o f c o m p u t e r s i m u l a t i o n i t w a s n e c e s s a r y t o d e f i n e these five 'strategies' imperative
more rigorously,
English
notation
is
b u t for h u m a n u n d e r s t a n d i n g the s i m p l e preferable.
T h e important
point
for this
c h a p t e r is that the five strategies w e r e t h o u g h t of as if they (rather than i n d i v i d u a l animals) w e r e c o m p e t i n g entities in their o w n right. R u l e s w e r e set
up
in
the
computer
simulation
for
the
'reproduction'
o f successful
s t r a t e g i e s ( p r e s u m a b l y i n d i v i d u a l s a d o p t i n g successful s t r a t e g i e s r e p r o d u c e d a n d p a s s e d o n g e n e t i c t e n d e n c i e s t o a d o p t t h o s e s a m e s t r a t e g i e s , b u t the d e t a i l s o f this w e r e i g n o r e d ) . T h e q u e s t i o n a s k e d w a s a b o u t s t r a t e g y s u c c e s s , not i n d i v i d u a l success. A further i m p o r t a n t point is that M a y n a r d S m i t h w a s seeking the 'best' s t r a t e g y i n o n l y a s p e c i a l s e n s e . I n fact h e w a s s e e k i n g a n ' e v o l u t i o n a r i l y stable s t r a t e g y ' o r E S S . T h e E S S has b e e n rigorously defined Smith
1974),
successful
b u t it c a n
be c r u d e l y encapsulated
(Maynard
as a strategy
that is
w h e n c o m p e t i n g w i t h c o p i e s o f itself. T h i s m a y s e e m a n o d d
p r o p e r t y to single out, but the rationale is really very powerful. If a p r o g r a m o r s t r a t e g y i s s u c c e s s f u l , this m e a n s t h a t c o p i e s o f i t w i l l t e n d t o b e c o m e m o r e n u m e r o u s in the p o p u l a t i o n of programs and will ultimately b e c o m e almost u n i v e r s a l . I t w i l l t h e r e f o r e c o m e t o b e s u r r o u n d e d b y c o p i e s o f itself. I f i t i s t o r e m a i n u n i v e r s a l , t h e r e f o r e , i t m u s t b e successful w h e n c o m p e t i n g a g a i n s t c o p i e s o f itself, s u c c e s s f u l c o m p a r e d w i t h r a r e different s t r a t e g i e s t h a t m i g h t arise by m u t a t i o n or invasion. A p r o g r a m that w a s not e v o l u t i o n a r i l y stable i n this s e n s e w o u l d n o t last l o n g i n t h e w o r l d , a n d w o u l d t h e r e f o r e n o t p r e s e n t i t s e l f for o u r e x p l a n a t i o n . I n t h e c a s e o f t h e f i v e s t r a t e g i e s listed a b o v e , M a y n a r d S m i t h w a n t e d t o know what
would
happen
in
a
p o p u l a t i o n c o n t a i n i n g c o p i e s o f all f i v e
p r o g r a m s . W a s there o n e of the five w h i c h , if it c a m e to p r e d o m i n a t e , w o u l d retain
its
numerical
superiority
against
all
comers?
He
concluded
that
p r o g r a m n u m b e r 3 i s a n E S S : w h e n i t h a p p e n s t o b e v e r y n u m e r o u s i n the p o p u l a t i o n n o o t h e r p r o g r a m f r o m t h e list d o e s b e t t e r t h a n p r o g r a m 3 itself ( a c t u a l l y t h e r e i s a p r o b l e m o v e r this p a r t i c u l a r e x a m p l e — D a w k i n s 1980, p . 7 — b u t I shall ignore it h e r e ) . W h e n we talk of a p r o g r a m as ' d o i n g better' or as b e i n g 'successful' we are notionally m e a s u r i n g success as c a p a c i t y to p r o p a g a t e c o p i e s o f t h e s a m e p r o g r a m i n t h e n e x t g e n e r a t i o n : i n r e a l i t y this
Selfish W a s p or Selfish S t r a t e g y ?
121
i s l i k e l y t o m e a n t h a t a successful p r o g r a m i s o n e w h i c h p r o m o t e s t h e s u r v i v a l a n d r e p r o d u c t i o n o f the a n i m a l a d o p t i n g it. W h a t M a y n a r d Smith, together with Price and Parker ( M a y n a r d Smith & Price
1973;
Maynard
Smith
&
Parker
1976),
has done is to take the
m a t h e m a t i c a l theory o f g a m e s a n d w o r k out the c r u c i a l respect i n w h i c h that t h e o r y m u s t b e m o d i f i e d t o suit t h e D a r w i n i s t ' s p u r p o s e . T h e c o n c e p t o f t h e E S S , a s t r a t e g y t h a t d o e s r e l a t i v e l y w e l l a g a i n s t c o p i e s of itself, is t h e r e s u l t . I h a v e a l r e a d y m a d e t w o attempts a t a d v o c a t i n g the i m p o r t a n c e o f the E S S c o n c e p t a n d e x p l a i n i n g its b r o a d a p p l i c a b i l i t y i n e t h o l o g y ( D a w k i n s 1 9 7 6 a , 1980), a n d I s h a l l n o t r e p e a t m y s e l f u n n e c e s s a r i l y h e r e . H e r e m y p u r p o s e i s t o d e v e l o p t h e r e l e v a n c e o f this w a y o f t h i n k i n g for t h e s u b j e c t o f t h e p r e s e n t b o o k , the d e b a t e a b o u t t h e l e v e l a t w h i c h n a t u r a l s e l e c t i o n a c t s . I s h a l l b e g i n by r e c o u n t i n g a specific piece of research that used the E S S c o n c e p t . A l l the facts I s h a l l g i v e a r e f r o m t h e field o b s e r v a t i o n s o f D r J a n e B r o c k m a n n , reported in detail elsewhere and briefly m e n t i o n e d in C h a p t e r 3. I shall h a v e to g i v e a brief a c c o u n t of the research itself before I c a n relate it to the m e s s a g e o f this c h a p t e r . Sphex ichneumcneus is a s o l i t a r y w a s p , s o l i t a r y in t h e sense t h a t t h e r e a r e no s o c i a l g r o u p s a n d n o sterile w o r k e r s , a l t h o u g h t h e f e m a l e s d o t e n d t o d i g t h e i r nests i n l o o s e a g g r e g a t i o n s . E a c h f e m a l e l a y s h e r o w n e g g s , a n d a l l l a b o u r on b e h a l f of the y o u n g is c o m p l e t e d before the e g g is l a i d — t h e w a s p s are
not
'progressive
underground
nest
provisioners'.
which
she has
The
female
previously
lays
provisioned
one with
egg
in
an
stung and
paralysed k a t y d i d s (long-horned grasshoppers). T h e n she closes up that nest, l e a v i n g t h e l a r v a t o feed o n t h e k a t y d i d s , w h i l e s h e h e r s e l f starts w o r k o n a n e w nest. T h e life o f a n a d u l t f e m a l e i s l i m i t e d t o a b o u t six s u m m e r w e e k s . I f o n e w i s h e d t o m e a s u r e it, t h e s u c c e s s o f a f e m a l e c o u l d b e a p p r o x i m a t e d a s t h e n u m b e r o f e g g s t h a t she s u c c e s s f u l l y l a y s o n a d e q u a t e p r o v i s i o n s d u r i n g this t i m e . T h e thing that especially interested us w a s that the wasps s e e m e d to h a v e t w o a l t e r n a t i v e w a y s o f a c q u i r i n g a nest. E i t h e r a f e m a l e w o u l d d i g h e r o w n nest i n t h e g r o u n d , o r s h e w o u l d a t t e m p t t o t a k e o v e r a n e x i s t i n g n e s t w h i c h a n o t h e r w a s p h a d d u g . W e c a l l e d t h e s e t w o b e h a v i o u r p a t t e r n s digging a n d entering, r e s p e c t i v e l y . N o w , h o w c a n t w o a l t e r n a t i v e w a y s o f a c h i e v i n g t h e s a m e e n d , i n this c a s e t w o a l t e r n a t i v e w a y s o f a c q u i r i n g a nest, c o e x i s t i n o n e p o p u l a t i o n ? S u r e l y o n e o r t h e o t h e r o u g h t t o b e m o r e s u c c e s s f u l , a n d t h e less successful o n e s h o u l d b e r e m o v e d f r o m t h e p o p u l a t i o n b y n a t u r a l s e l e c t i o n ? T h e r e a r e t w o g e n e r a l r e a s o n s w h y this m i g h t n o t h a p p e n , w h i c h I w i l l e x p r e s s i n t h e j a r g o n o f E S S t h e o r y : firstly, d i g g i n g a n d e n t e r i n g m i g h t b e two outcomes of one 'conditional strategy'; secondly, they might be equally successful a t s o m e c r i t i c a l f r e q u e n c y m a i n t a i n e d
by frequency-dependent
selection—part of a 'mixed E S S ' ( M a y n a r d Smith 1974,
1 9 7 9 ) . I f t h e first
possibility w e r e correct, all w a s p s w o u l d b e p r o g r a m m e d w i t h the s a m e
1 2 2
Selfish W a s p o r Selfish S t r a t e g y ?
c o n d i t i o n a l r u l e : ' I f X i s t r u e , d i g , o t h e r w i s e e n t e r ' ; for i n s t a n c e , ' I f y o u h a p p e n t o b e a s m a l l w a s p , d i g , o t h e r w i s e use y o u r s u p e r i o r s i z e t o t a k e o v e r a n o t h e r w a s p ' s b u r r o w ' . W e failed t o f i n d a n y e v i d e n c e for a c o n d i t i o n a l p r o g r a m o f this o r a n y o t h e r k i n d . I n s t e a d , w e c o n v i n c e d o u r s e l v e s t h a t the s e c o n d p o s s i b i l i t y , t h e ' m i x e d E S S ' , f i t t e d t h e facts. T h e r e are in theory two kinds of mixed E S S , or rather two extremes with a c o n t i n u u m b e t w e e n . T h e f i r s t e x t r e m e i s a b a l a n c e d p o l y m o r p h i s m . I n this c a s e , i f w e w a n t t o use t h e i n i t i a l s ' E S S ' , t h e f i n a l S s h o u l d b e t h o u g h t o f a s s t a n d i n g for state o f t h e p o p u l a t i o n r a t h e r t h a n s t r a t e g y o f t h e i n d i v i d u a l . I f this p o s s i b i l i t y o b t a i n e d , t h e r e w o u l d b e t w o d i s t i n c t k i n d s o f w a s p s , d i g g e r s a n d enterers, w h o w o u l d tend t o b e e q u a l l y successful. equally
successful,
natural
selection
would
tend
to
If they were not eliminate
the
less
successful o n e from the p o p u l a t i o n . It is too m u c h to h o p e that, by sheer c o i n c i d e n c e , t h e n e t costs a n d benefits o f d i g g i n g w o u l d e x a c t l y b a l a n c e the net
costs
and
dependent
benefits
selection.
of entering.
We
postulate
Rather, a
we
critical
are
invoking frequency-
equilibrium
proportion
of
d i g g e r s , p*, a t w h i c h t h e t w o k i n d s o f w a s p s a r e e q u a l l y s u c c e s s f u l . T h e n , i f t h e p r o p o r t i o n o f d i g g e r s i n t h e p o p u l a t i o n falls b e l o w t h e c r i t i c a l f r e q u e n c y , d i g g e r s w i l l b e f a v o u r e d b y s e l e c t i o n , w h i l e i f i t rises a b o v e t h e c r i t i c a l f r e q u e n c y e n t e r e r s w i l l b e f a v o u r e d . I n this w a y the p o p u l a t i o n w o u l d h o v e r a r o u n d the e q u i l i b r i u m frequency. I t i s e a s y t o t h i n k o f p l a u s i b l e r e a s o n s w h y benefit m i g h t b e f r e q u e n c y d e p e n d e n t i n this w a y . C l e a r l y , s i n c e n e w b u r r o w s c o m e i n t o e x i s t e n c e o n l y w h e n d i g g e r s d i g t h e m , t h e f e w e r d i g g e r s t h e r e a r e i n t h e p o p u l a t i o n the s t r o n g e r w i l l b e t h e c o m p e t i t i o n a m o n g e n t e r e r s for b u r r o w s , a n d the l o w e r the benefit to a t y p i c a l enterer. C o n v e r s e l y , w h e n diggers are v e r y numerous, a v a i l a b l e b u r r o w s a b o u n d and enterers tend to prosper.
But,
as
I
said,
frequency-dependent p o l y m o r p h i s m is only one end of a continuum. We now turn to the other end. At the other end of the c o n t i n u u m
there is no p o l y m o r p h i s m
among
i n d i v i d u a l s . I n t h e s t a b l e s t a t e a l l w a s p s o b e y the s a m e p r o g r a m , b u t t h a t p r o g r a m i s i t s e l f a m i x t u r e . E v e r y w a s p i s o b e y i n g the i n s t r u c t i o n , ' D i g w i t h p r o b a b i l i t y p, e n t e r w i t h p r o b a b i l i t y I — p'; for i n s t a n c e , ' D i g on 70 p e r c e n t of occasions, enter on 30 per cent of occasions'.
I f this i s r e g a r d e d a s a
' p r o g r a m ' , w e c o u l d p e r h a p s refer t o d i g g i n g a n d e n t e r i n g t h e m s e l v e s a s 'subroutines'.
Every
programmed
to
wasp
choose
is
one
equipped or
the
with
other
both on
subroutines.
each
occasion
She
is
with
a
c h a r a c t e r i s t i c p r o b a b i l i t y , p. Although
there
is
no
polymorphism
of diggers
and
enterers
here,
s o m e t h i n g m a t h e m a t i c a l l y e q u i v a l e n t to f r e q u e n c y - d e p e n d e n t selection can go on. H e r e is h o w it w o u l d w o r k . As before, there is a critical population f r e q u e n c y o f d i g g i n g , p*, a t w h i c h e n t e r i n g w o u l d y i e l d e x a c t l y the s a m e ' p a y - o f f ' a s d i g g i n g . p * is, t h e n , t h e e v o l u t i o n a r i l y s t a b l e d i g g i n g p r o b a b i l i t y .
Selfish W a s p o r Selfish S t r a t e g y ?
I f t h e s t a b l e p r o b a b i l i t y i s 0.7,
programs instructing wasps
123
to follow
a
different r u l e , s a y ' D i g w i t h p r o b a b i l i t y 0 . 7 5 ' , o r ' D i g w i t h p r o b a b i l i t y 0 . 6 5 ' , w o u l d d o less w e l l . T h e r e i s a w h o l e f a m i l y o f ' m i x e d s t r a t e g i e s ' o f t h e f o r m ' D i g w i t h p r o b a b i l i t y p, enter w i t h p r o b a b i l i t y 1 —p', a n d o n l y o n e of these is the E S S . I said t h a t the t w o e x t r e m e s w e r e j o i n e d b y a c o n t i n u u m . I m e a n t t h a t t h e s t a b l e p o p u l a t i o n f r e q u e n c y o f d i g g i n g , p * (70 p e r c e n t o r w h a t e v e r i t i s ) , could be achieved by any of a large n u m b e r of combinations of pure and mixed individual strategies. T h e r e might be a w i d e distribution of p values in individual nervous systems in the p o p u l a t i o n , i n c l u d i n g some p u r e diggers and
pure enterers.
But,
provided
the
total
frequency of d i g g i n g in
the
p o p u l a t i o n i s e q u a l t o t h e c r i t i c a l v a l u e p*, i t w o u l d still b e t r u e t h a t d i g g i n g and entering w e r e e q u a l l y successful, a n d n a t u r a l selection w o u l d not act to c h a n g e the r e l a t i v e f r e q u e n c y o f t h e t w o s u b r o u t i n e s i n t h e n e x t g e n e r a t i o n . T h e p o p u l a t i o n w o u l d b e i n a n e v o l u t i o n a r i l y stable state. T h e a n a l o g y w i t h F i s h e r ' s ( 1 9 3 0 a ) t h e o r y o f sex r a t i o e q u i l i b r i u m w i l l b e c l e a r . P r o c e e d i n g from the c o n c e i v a b l e t o the a c t u a l , B r o c k m a n n ' s d a t a s h o w conclusively that
these w a s p s a r e n o t i n a n y s i m p l e sense p o l y m o r p h i c .
Individuals sometimes d u g and sometimes entered. We c o u l d not e v e n detect a n y s t a t i s t i c a l t e n d e n c y for i n d i v i d u a l s t o s p e c i a l i z e i n d i g g i n g o r e n t e r i n g . E v i d e n t l y , if the w a s p p o p u l a t i o n is in a m i x e d e v o l u t i o n a r i l y stable state, it lies a w a y f r o m t h e p o l y m o r p h i s m e n d o f t h e c o n t i n u u m . W h e t h e r i t i s a t t h e other
extreme—all
individuals
running
the
same
stochastic
program—or
whether there is some m o r e c o m p l e x m i x t u r e of pure and m i x e d i n d i v i d u a l p r o g r a m s , w e d o n o t k n o w . I t i s o n e o f t h e c e n t r a l m e s s a g e s o f this c h a p t e r that, for o u r r e s e a r c h p u r p o s e , w e d i d n o t need t o k n o w . B e c a u s e w e r e f r a i n e d from t a l k i n g a b o u t i n d i v i d u a l s u c c e s s , b u t t h o u g h t i n s t e a d a b o u t s u b r o u t i n e success a v e r a g e d o v e r a l l i n d i v i d u a l s , w e w e r e a b l e t o d e v e l o p a n d test a successful m o d e l o f t h e m i x e d E S S w h i c h left o p e n t h e q u e s t i o n o f w h e r e a l o n g the c o n t i n u u m o u r w a s p s l a y . I s h a l l r e t u r n t o this p o i n t after g i v i n g s o m e p e r t i n e n t facts a n d after o u t l i n i n g t h e m o d e l itself. W h e n a w a s p d i g s a b u r r o w , she m a y e i t h e r s t a y w i t h i t a n d p r o v i s i o n it, o r she m a y a b a n d o n it.
R e a s o n s for a b a n d o n i n g nests w e r e n o t a l w a y s
obvious, but they i n c l u d e d invasion by ants and other undesirable aliens. A w a s p w h o m o v e s i n t o a b u r r o w t h a t a n o t h e r h a s d u g m a y find t h a t t h e o r i g i n a l o w n e r is still in r e s i d e n c e . In this c a s e s h e is s a i d to have joined t h e p r e v i o u s o w n e r , a n d t h e t w o w a s p s u s u a l l y w o r k o n t h e s a m e n e s t for a w h i l e , b o t h i n d e p e n d e n t l y b r i n g i n g k a t y d i d s t o it. A l t e r n a t i v e l y , t h e e n t e r i n g w a s p m a y b e f o r t u n a t e e n o u g h t o hit u p o n a nest t h a t h a s b e e n a b a n d o n e d b y its o r i g i n a l o w n e r , i n w h i c h c a s e she h a s i t t o herself. T h e e v i d e n c e i n d i c a t e s t h a t e n t e r i n g w a s p s c a n n o t d i s t i n g u i s h a nest t h a t h a s b e e n a b a n d o n e d f r o m o n e t h a t i s still o c c u p i e d b y its p r e v i o u s o w n e r . T h i s f a c t i s n o t s o s u r p r i s i n g as it m a y seem, since both wasps spend most of their time out hunting, so t w o
124
Selfish W a s p or Selfish S t r a t e g y ?
w a s p s ' s h a r i n g ' t h e s a m e nest s e l d o m m e e t . W h e n t h e y d o m e e t t h e y f i g h t , a n d i n a n y c a s e o n l y o n e o f t h e m s u c c e e d s i n l a y i n g a n e g g i n t h e nest u n d e r dispute. W h a t e v e r h a d p r e c i p i t a t e d t h e a b a n d o n i n g o f a nest b y t h e o r i g i n a l o w n e r s e e m e d u s u a l l y t o b e a t e m p o r a r y i n c o n v e n i e n c e , a n d a n a b a n d o n e d nest constituted a desirable resource w h i c h w a s soon used by a n o t h e r w a s p . A w a s p w h o e n t e r s a n a b a n d o n e d b u r r o w s a v e s h e r s e l f t h e costs a s s o c i a t e d w i t h d i g g i n g o n e . O n t h e o t h e r h a n d , s h e r u n s t h e risk t h a t t h e b u r r o w she enters h a s n o t b e e n a b a n d o n e d . I t m a y still c o n t a i n t h e o r i g i n a l o w n e r , o r i t m a y c o n t a i n a n o t h e r e n t e r i n g w a s p w h o g o t t h e r e f i r s t . I n e i t h e r o f these cases the e n t e r i n g w a s p lets h e r s e l f in for a h i g h risk of a c o s t l y fight, a n d a h i g h risk that she w i l l not be the o n e to l a y the e g g at the end of a costly period of p r o v i s i o n i n g t h e nest. We d e v e l o p e d a n d tested a m a t h e m a t i c a l m o d e l ( B r o c k m a n n , G r a f e n & D a w k i n s 1 9 7 9 ) w h i c h d i s t i n g u i s h e d f o u r different ' o u t c o m e s ' o r fates t h a t c o u l d befall a w a s p in a n y particular nesting episode. 1 S h e c o u l d b e f o r c e d t o a b a n d o n t h e nest, s a y b y a n a n t r a i d . 2 S h e c o u l d e n d u p a l o n e , i n sole c h a r g e o f t h e nest. 3 S h e c o u l d be j o i n e d by a second w a s p . 4 She could join an already incumbent wasp. O u t c o m e s 1 to 3 c o u l d r e s u l t f r o m an i n i t i a l d e c i s i o n to d i g a b u r r o w . O u t c o m e s 2 to 4 c o u l d result from an initial decision to enter. B r o c k m a n n ' s d a t a e n a b l e d us to m e a s u r e , in terms of p r o b a b i l i t y of l a y i n g an e g g per unit t i m e , t h e r e l a t i v e ' p a y o f f s ' a s s o c i a t e d w i t h e a c h o f these four o u t c o m e s . F o r instance, in one study population in Exeter, N e w Hampshire, O u t c o m e 4, ' j o i n i n g ' , h a d a p a y o f f s c o r e o f 0.35 e g g s p e r obtained
100 h o u r s . T h i s s c o r e w a s
by a v e r a g i n g o v e r all occasions w h e n w a s p s e n d e d up in that
o u t c o m e . T o c a l c u l a t e i t w e s i m p l y a d d e d u p t h e t o t a l n u m b e r o f e g g s laid by wasps w h o , on the occasion concerned, had j o i n e d an already incumbent w a s p , a n d d i v i d e d b y t h e t o t a l t i m e s p e n t b y w a s p s o n nests t h a t t h e y h a d joined.
The
corresponding
subsequently joined was
score
for
wasps
who
began
alone
but
were
1.06 e g g s p e r 100 h o u r s , a n d t h a t for w a s p s w h o
r e m a i n e d a l o n e w a s 1.93 e g g s p e r 100 h o u r s . I f a w a s p c o u l d c o n t r o l w h i c h o f t h e f o u r o u t c o m e s she e n d e d u p i n , she s h o u l d ' p r e f e r ' t o e n d u p a l o n e s i n c e this o u t c o m e c a r r i e d t h e h i g h e s t p a y o f f rate, b u t h o w m i g h t she a c h i e v e this? It w a s a k e y assumption of our m o d e l that the four o u t c o m e s did not correspond to decisions that were a v a i l a b l e to a w a s p . A w a s p c a n ' d e c i d e ' to d i g or to enter. She c a n n o t decide to be j o i n e d or to be alone a n y m o r e than a m a n can decide not to get cancer. T h e s e are o u t c o m e s that d e p e n d o n c i r c u m s t a n c e s b e y o n d the individual's c o n t r o l . I n this c a s e t h e y d e p e n d o n w h a t t h e o t h e r w a s p s i n t h e p o p u l a t i o n
Selfish W a s p or Selfish S t r a t e g y ?
125
d o . B u t j u s t a s a m a n m a y s t a t i s t i c a l l y r e d u c e his c h a n c e s o f g e t t i n g c a n c e r , by taking the decision to stop s m o k i n g , so a w a s p ' s 'task' is to m a k e the o n l y decision open to h e r — d i g or enter—in such a w a y as to m a x i m i z e her c h a n c e s o f e n d i n g u p i n a d e s i r a b l e o u t c o m e . M o r e s t r i c t l y , w e seek t h e stable v a l u e of p, p*, such that w h e n p* of the decisions in the p o p u l a t i o n are digging decisions, no m u t a n t gene l e a d i n g to the a d o p t i o n of some other value of p will be favoured by natural selection. T h e probability that an entering decision will lead to s o m e p a r t i c u l a r outcome, such as
the d e s i r a b l e
'alone' outcome,
frequency of entering decisions in
d e p e n d s on the overall
the p o p u l a t i o n .
If a
large
a m o u n t of
e n t e r i n g i s g o i n g o n i n the p o p u l a t i o n , t h e n u m b e r o f a v a i l a b l e a b a n d o n e d burrows goes d o w n , and the chances go up that a w a s p that decides to enter w i l l find h e r s e l f i n the u n d e s i r a b l e p o s i t i o n o f j o i n i n g a n i n c u m b e n t . O u r model enables us to take a n y given v a l u e of p, the overall frequency of d i g g i n g in the p o p u l a t i o n , a n d predict the p r o b a b i l i t y that an i n d i v i d u a l that decides to d i g , or an i n d i v i d u a l that d e c i d e s to enter, w i l l end that e p i s o d e i n e a c h o f t h e four o u t c o m e s . T h e a v e r a g e p a y o f f t o a w a s p t h a t decides to dig,
t h e r e f o r e , c a n b e p r e d i c t e d for a n y n a m e d f r e q u e n c y o f
d i g g i n g versus entering in the p o p u l a t i o n as a w h o l e . It is s i m p l y the sum, o v e r t h e four o u t c o m e s , o f t h e e x p e c t e d p a y o f f y i e l d e d b y e a c h o u t c o m e , multiplied by the p r o b a b i l i t y that a w a s p that digs will end up in that o u t c o m e . T h e e q u i v a l e n t s u m c a n b e w o r k e d o u t for a w a s p t h a t d e c i d e s t o enter, a g a i n
for a n y n a m e d
frequency of d i g g i n g versus entering in
the
population. Finally, making certain plausible additional assumptions which a r e listed i n t h e o r i g i n a l p a p e r , w e s o l v e a n e q u a t i o n t o find t h e p o p u l a t i o n d i g g i n g frequency at w h i c h the a v e r a g e e x p e c t e d benefit to a w a s p that digs is exactly e q u a l to the a v e r a g e e x p e c t e d benefit to a w a s p that enters. T h a t is our
predicted
equilibrium
frequency
which
we
can
compare
with
the
o b s e r v e d f r e q u e n c y i n the w i l d p o p u l a t i o n . O u r e x p e c t a t i o n i s t h a t t h e r e a l p o p u l a t i o n s h o u l d e i t h e r b e s i t t i n g a t t h e e q u i l i b r i u m f r e q u e n c y o r else i n t h e process o f e v o l v i n g t o w a r d s the e q u i l i b r i u m f r e q u e n c y .
T h e m o d e l also
predicts the proportion of wasps e n d i n g up in e a c h of the four o u t c o m e s at e q u i l i b r i u m , a n d these figures t o o c a n b e tested a g a i n s t t h e o b s e r v e d d a t a . The
model's
equilibrium
is
theoretically
stable
in
that
it
predicts
that
deviations from e q u i l i b r i u m will be corrected by n a t u r a l selection. Brockmann studied two populations of wasps, one in M i c h i g a n and one in New Hampshire.
The
results w e r e d i f f e r e n t
in
the
two
populations.
In
M i c h i g a n t h e m o d e l failed t o p r e d i c t t h e o b s e r v e d results, a n d w e c o n c l u d e d t h a t i t w a s q u i t e i n a p p l i c a b l e t o t h e M i c h i g a n p o p u l a t i o n , for u n k n o w n reasons as discussed population
has
now
in
the
gone
original extinct
paper is
(the
probably
fact
that
the
fortuitous!).
Michigan The
New
Hampshire population, on the other hand, g a v e a c o n v i n c i n g fit to the p r e d i c t i o n s o f the m o d e l . T h e p r e d i c t e d e q u i l i b r i u m f r e q u e n c y o f e n t e r i n g
126
Selfish W a s p or Selfish S t r a t e g y ?
w a s 0.44, a n d t h e o b s e r v e d f r e q u e n c y w a s 0 . 4 1 . T h e m o d e l also successfully p r e d i c t e d t h e f r e q u e n c y o f e a c h o f t h e four ' o u t c o m e s ' i n t h e N e w H a m p s h i r e population.
Perhaps most importantly,
t h e a v e r a g e p a y o f f r e s u l t i n g from
d i g g i n g d e c i s i o n s d i d n o t differ s i g n i f i c a n t l y f r o m t h e a v e r a g e p a y o f f r e s u l t i n g from entering decisions. T h e p o i n t o f m y t e l l i n g this s t o r y i n t h e p r e s e n t b o o k has n o w f i n a l l y a r r i v e d . I w a n t t o c l a i m t h a t w e w o u l d h a v e f o u n d i t difficult t o d o this r e s e a r c h i f w e h a d t h o u g h t i n t e r m s o f individual s u c c e s s , r a t h e r t h a n i n t e r m s o f strategy ( p r o g r a m ) success a v e r a g e d o v e r all i n d i v i d u a l s . I f the m i x e d E S S h a d h a p p e n e d t o lie a t t h e b a l a n c e d p o l y m o r p h i s m e n d o f t h e c o n t i n u u m , i t w o u l d , i n d e e d , h a v e m a d e sense t o ask s o m e t h i n g l i k e t h e f o l l o w i n g . I s the s u c c e s s o f w a s p s t h a t d i g e q u a l t o t h e success o f w a s p s t h a t e n t e r ? W e w o u l d h a v e classified w a s p s a s d i g g e r s o r e n t e r e r s , a n d c o m p a r e d t h e t o t a l l i f e t i m e ' s e g g - l a y i n g success of i n d i v i d u a l s of the t w o types, p r e d i c t i n g that the t w o s u c c e s s s c o r e s s h o u l d b e e q u a l . B u t a s w e h a v e seen these w a s p s a r e n o t p o l y m o r p h i c . E a c h i n d i v i d u a l sometimes digs and sometimes enters. I t m i g h t b e t h o u g h t t h a t i t w o u l d h a v e b e e n e a s y t o d o s o m e t h i n g like the f o l l o w i n g . C l a s s i f y a l l i n d i v i d u a l s i n t o those t h a t e n t e r e d w i t h a p r o b a b i l i t y less t h a n 0 . 1 , t h o s e t h a t e n t e r e d w i t h a p r o b a b i l i t y b e t w e e n 0.1
a n d 0.2,
t h o s e w i t h a p r o b a b i l i t y b e t w e e n 0.2 a n d 0.3, b e t w e e n 0.3 a n d 0.4, 0.4 a n d 0.5, e t c . T h e n c o m p a r e t h e l i f e t i m e r e p r o d u c t i v e successes o f w a s p s i n the d i f f e r e n t c l a s s e s . B u t s u p p o s i n g w e d i d this, e x a c t l y w h a t w o u l d the E S S t h e o r y p r e d i c t ? A h a s t y first t h o u g h t is t h a t t h o s e w a s p s w i t h a p v a l u e close to the e q u i l i b r i u m p* should enjoy a h i g h e r success score than wasps with s o m e o t h e r v a l u e o f p : t h e g r a p h o f success a g a i n s t p s h o u l d p e a k a t a n ' o p t i m u m ' at p*. B u t p* is n o t r e a l l y an o p t i m u m v a l u e , it is an e v o l u t i o n a r i l y stable v a l u e . T h e t h e o r y expects that, w h e n p* is a c h i e v e d in the p o p u l a t i o n as a w h o l e , d i g g i n g a n d e n t e r i n g should be e q u a l l y successful. At e q u i l i b r i u m , therefore, we e x p e c t no correlation b e t w e e n a wasp's d i g g i n g probability and her success. If the p o p u l a t i o n deviates from e q u i l i b r i u m in the direction of t o o m u c h e n t e r i n g , t h e ' o p t i m u m ' c h o i c e r u l e b e c o m e s ' a l w a y s d i g ' (not ' d i g w i t h p r o b a b i l i t y p * ' ) . I f t h e p o p u l a t i o n d e v i a t e s f r o m e q u i l i b r i u m i n the other direction, the ' o p t i m u m ' policy is ' a l w a y s enter'.
If the p o p u l a t i o n
f l u c t u a t e s a t r a n d o m a r o u n d t h e e q u i l i b r i u m v a l u e , a n a l o g y w i t h sex r a t i o t h e o r y s u g g e s t s t h a t i n t h e l o n g r u n g e n e t i c t e n d e n c i e s t o a d o p t e x a c t l y the e q u i l i b r i u m v a l u e , p*, w i l l b e f a v o u r e d o v e r t e n d e n c i e s t o a d o p t a n y o t h e r c o n s i s t e n t v a l u e o f p ( W i l l i a m s 1 9 7 9 ) . B u t i n a n y o n e y e a r this a d v a n t a g e i s n o t p a r t i c u l a r l y l i k e l y t o b e e v i d e n t . T h e s e n s i b l e e x p e c t a t i o n o f the t h e o r y i s t h a t t h e r e s h o u l d b e n o s i g n i f i c a n t d i f f e r e n c e i n s u c c e s s r a t e s a m o n g the classes o f w a s p s . I n a n y c a s e this m e t h o d o f d i v i d i n g w a s p s u p i n t o classes p r e s u p p o s e s t h a t there is some consistent variation a m o n g wasps in d i g g i n g tendency. T h e
Selfish W a s p or Selfish S t r a t e g y ?
127
theory gives us no particular reason to expect that there should be any such variation. positive
I n d e e d , the a n a l o g y w i t h sex ratio t h e o r y just m e n t i o n e d g i v e s grounds
probability.
for
expecting
that
wasps
I n a c c o r d a n c e w i t h this,
should
not
vary
in
digging
a s t a t i s t i c a l test o n t h e a c t u a l d a t a
revealed no evidence of inter-individual variation in digging tendency. E v e n if there w e r e some i n d i v i d u a l v a r i a t i o n , the m e t h o d of c o m p a r i n g the success o f i n d i v i d u a l s w i t h different p v a l u e s w o u l d h a v e b e e n a c r u d e a n d i n s e n s i t i v e o n e for c o m p a r i n g t h e s u c c e s s r a t e s o f d i g g i n g a n d e n t e r i n g . T h i s c a n b e s e e n by an analogy. An agriculturalist wishes to c o m p a r e the efficacy of t w o fertilizers, A a n d B . H e t a k e s ten fields a n d d i v i d e s e a c h o f t h e m i n t o a l a r g e n u m b e r o f s m a l l plots. E a c h plot is treated, at r a n d o m , w i t h either A or B, a n d w h e a t is s o w n i n a l l the p l o t s o f a l l t h e fields. N o w , h o w s h o u l d h e c o m p a r e t h e t w o fertilizers? T h e s e n s i t i v e w a y i s t o t a k e t h e y i e l d s o f a l l t h e p l o t s t r e a t e d w i t h A and c o m p a r e t h e m w i t h the yields of all the plots treated w i t h B, across all ten f i e l d s . B u t t h e r e i s a n o t h e r , m u c h c r u d e r w a y . I t h a p p e n s t h a t i n t h e r a n d o m a l l o c a t i o n o f fertilizers t o p l o t s , s o m e o f t h e t e n f i e l d s r e c e i v e d a relatively large a m o u n t of fertilizer A, w h i l e others h a p p e n e d to be g i v e n a relatively large a m o u n t of B. T h e agriculturalist c o u l d , then, plot the overall yield of each of the ten fields against the p r o p o r t i o n of the field that w a s treated
with
fertilizer A
rather
than
B.
If there
is
a
very
pronounced
d i f f e r e n c e i n q u a l i t y b e t w e e n t h e t w o f e r t i l i z e r s , this m e t h o d m i g h t j u s t s h o w i t u p , b u t far m o r e p r o b a b l y t h e d i f f e r e n c e w o u l d b e m a s k e d . T h e m e t h o d o f c o m p a r i n g the y i e l d s o f t h e t e n f i e l d s w o u l d b e efficient o n l y i f t h e r e i s v e r y h i g h b e t w e e n - f i e l d v a r i a n c e , a n d t h e r e i s n o p a r t i c u l a r r e a s o n t o e x p e c t this. I n the a n a l o g y , t h e t w o f e r t i l i z e r s s t a n d for d i g g i n g a n d e n t e r i n g . T h e fields a r e the w a s p s . T h e p l o t s a r e t h e e p i s o d e s o f t i m e t h a t i n d i v i d u a l w a s p s devote either to d i g g i n g or to entering. T h e crude m e t h o d of c o m p a r i n g d i g g i n g and entering is to plot the lifetime success of i n d i v i d u a l w a s p s against their p r o p o r t i o n a t e d i g g i n g t e n d e n c y .
The
sensitive
way
is
the
one
we
actually employed. We m a d e a detailed and exhaustive inventory of the time spent by e a c h w a s p o n e a c h b u r r o w w i t h w h i c h she w a s associated. individual duration,
female's each
adult
episode
lifetime
into
being designated
consecutive a digging
We divided each
episodes episode
of if the
known wasp
c o n c e r n e d b e g a n h e r a s s o c i a t i o n w i t h t h e b u r r o w b y d i g g i n g it. O t h e r w i s e , i t was designated an entering episode. T h e end of each episode was signalled b y t h e w a s p ' s l e a v i n g t h e nest for t h e last t i m e . T h i s i n s t a n t w a s a l s o t r e a t e d a s t h e start o f t h e n e x t b u r r o w e p i s o d e , e v e n t h o u g h t h e n e x t b u r r o w site had not, at the time, b e e n chosen. T h a t is to say, in o u r time a c c o u n t i n g , the t i m e s p e n t s e a r c h i n g for a n e w b u r r o w t o e n t e r , o r s e a r c h i n g for a p l a c e t o dig a new burrow, was designated retroactively as time 'spent' on that n e w
128
Selfish W a s p or Selfish S t r a t e g y ?
burrow.
It was
added
to
the
time
subsequently spent
p r o v i s i o n i n g the
b u r r o w w i t h k a t y d i d s , f i g h t i n g o t h e r w a s p s , f e e d i n g , s l e e p i n g , e t c . , u n t i l the w a s p left t h e n e w b u r r o w for t h e last t i m e . At the e n d of the season, therefore, we c o u l d a d d up the total n u m b e r of w a s p h o u r s s p e n t o n d u g - b u r r o w e p i s o d e s , a n d also the t o t a l n u m b e r o f w a s p h o u r s s p e n t o n e n t e r e d - b u r r o w e p i s o d e s . F o r t h e N e w H a m p s h i r e s t u d y these two
figures
were
8518.7
hours
and
6747.4
hours,
respectively.
This is
r e g a r d e d as t i m e s p e n t , or i n v e s t e d , for a r e t u r n , a n d t h e r e t u r n is m e a s u r e d i n n u m b e r s o f e g g s . T h e t o t a l n u m b e r o f e g g s l a i d a t t h e e n d o f the d u g b u r r o w e p i s o d e s (i.e. b y w a s p s t h a t h a d d u g t h e b u r r o w c o n c e r n e d ) i n t h e w h o l e N e w H a m p s h i r e p o p u l a t i o n d u r i n g t h e y e a r o f s t u d y w a s 82. T h e c o r r e s p o n d i n g n u m b e r for e n t e r e d - b u r r o w e p i s o d e s w a s 5 7 e g g s . T h e success r a t e o f t h e d i g g i n g s u b r o u t i n e w a s , t h e r e f o r e , 8 2 / 8 5 1 8 . 7 = 0.96 e g g s p e r 100 h o u r s . T h e s u c c e s s r a t e o f t h e e n t e r i n g s u b r o u t i n e w a s 5 7 / 6 7 4 7 . 4 = 0.84 e g g s p e r 100 h o u r s . T h e s e s u c c e s s scores a r e a v e r a g e d a c r o s s all t h e i n d i v i d u a l s w h o used the t w o subroutines. Instead of c o u n t i n g the n u m b e r of eggs laid in her lifetime b y a n i n d i v i d u a l w a s p — t h e e q u i v a l e n t o f m e a s u r i n g the w h e a t y i e l d o f e a c h o f t h e ten f i e l d s i n t h e a n a l o g y — w e c o u n t t h e n u m b e r o f e g g s l a i d ' b y ' t h e d i g g i n g (or e n t e r i n g ) s u b r o u t i n e p e r u n i t ' r u n n i n g t i m e ' o f the subroutine. T h e r e i s a n o t h e r r e s p e c t i n w h i c h i t w o u l d h a v e b e e n difficult for u s t o h a v e d o n e this a n a l y s i s i f w e h a d insisted o n t h i n k i n g i n t e r m s o f i n d i v i d u a l success. In o r d e r to solve the e q u a t i o n to predict the e q u i l i b r i u m entering f r e q u e n c y , w e h a d t o h a v e e m p i r i c a l e s t i m a t e s o f t h e e x p e c t e d payoffs o f e a c h of the
four
'outcomes'
(abandons,
remains
alone,
is joined, joins).
We
o b t a i n e d p a y o f f s c o r e s for t h e f o u r o u t c o m e s i n the s a m e w a y a s w e o b t a i n e d s u c c e s s s c o r e s for e a c h o f t h e t w o s t r a t e g i e s , d i g a n d e n t e r . W e a v e r a g e d o v e r a l l i n d i v i d u a l s , d i v i d i n g t h e t o t a l n u m b e r o f e g g s l a i d i n e a c h o u t c o m e b y the total time spent on episodes that ended up in that o u t c o m e . Since most i n d i v i d u a l s e x p e r i e n c e d a l l f o u r o u t c o m e s a t different t i m e s , i t i s n o t c l e a r h o w w e c o u l d h a v e o b t a i n e d t h e n e c e s s a r y e s t i m a t e s o f o u t c o m e payoffs i f w e h a d t h o u g h t in terms of i n d i v i d u a l success. N o t i c e t h e i m p o r t a n t r o l e o f time i n t h e c o m p u t a t i o n o f t h e ' s u c c e s s ' o f the d i g g i n g a n d e n t e r i n g subroutines (and o f the p a y o f f g i v e n b y e a c h o u t c o m e ) . T h e total n u m b e r of eggs laid ' b y ' the d i g g i n g subroutine is a poor measure of success until it has been d i v i d e d by the time spent on the subroutine. T h e n u m b e r of eggs laid by the t w o subroutines m i g h t be e q u a l , but if d i g g i n g episodes are on a v e r a g e t w i c e as l o n g as entering episodes, natural selection w i l l p r e s u m a b l y f a v o u r e n t e r i n g . I n fact r a t h e r m o r e e g g s w e r e l a i d ' b y ' the d i g g i n g s u b r o u t i n e t h a n by the entering one, but c o r r e s p o n d i n g l y m o r e time w a s spent on the d i g g i n g s u b r o u t i n e so the o v e r a l l success rates of the t w o w e r e a p p r o x i m a t e l y e q u a l . N o t i c e t o o t h a t w e d o n o t s p e c i f y w h e t h e r the e x t r a t i m e s p e n t o n d i g g i n g i s a c c o u n t e d for b y a g r e a t e r n u m b e r o f w a s p s
Selfish W a s p or Selfish S t r a t e g y ?
129
digging, or by each digging episode lasting longer. T h e distinction m a y be i m p o r t a n t for s o m e p u r p o s e s , b u t i t d o e s n ' t m a t t e r for t h e k i n d o f e c o n o m i c analysis we undertook. I t w a s c l e a r l y s t a t e d i n the o r i g i n a l p a p e r ( B r o c k m a n n , G r a f e n & D a w k i n s 1979), a n d must be repeated here, that the m e t h o d we used d e p e n d e d u p o n some
assumptions.
We
assumed,
for
instance,
that
a
wasp's
choice
of
s u b r o u t i n e o n a n y p a r t i c u l a r o c c a s i o n d i d n o t affect h e r s u r v i v a l o r s u c c e s s r a t e after t h e e n d o f t h e e p i s o d e c o n c e r n e d . T h u s t h e costs o f d i g g i n g w e r e assumed to be reflected totally in the time spent on d i g g i n g episodes, a n d the costs o f e n t e r i n g r e f l e c t e d i n t h e t i m e s p e n t o n e n t e r i n g e p i s o d e s . I f t h e a c t o f d i g g i n g h a d i m p o s e d s o m e e x t r a c o s t , s a y a risk o f w e a r a n d t e a r t o t h e l i m b s , s h o r t e n i n g life e x p e c t a t i o n , o u r s i m p l e t i m e - c o s t a c c o u n t i n g w o u l d n e e d t o be a m e n d e d . T h e success rates of the d i g g i n g a n d the e n t e r i n g subroutines would
have
to
be
expressed,
not
in
eggs
per
hour,
but
in
eggs
per
' o p p o r t u n i t y c o s t ' . O p p o r t u n i t y cost m i g h t still b e m e a s u r e d i n u n i t s o f t i m e , but d i g g i n g time w o u l d h a v e to be scaled up in a costlier c u r r e n c y than entering time, b e c a u s e e a c h h o u r spent in d i g g i n g shortens the e x p e c t a t i o n of effective
life
of the
individual.
Under
such
circumstances
it
might
be
n e c e s s a r y , i n spite o f a l l the difficulties, t o t h i n k i n t e r m s o f i n d i v i d u a l s u c c e s s rather than subroutine success. It is for this k i n d of r e a s o n t h a t C l u t t o n - B r o c k el al. (in press) a r e p r o b a b l y wise in their a m b i t i o n to m e a s u r e the total lifetime r e p r o d u c t i v e success rates o f t h e i r i n d i v i d u a l red d e e r s t a g s . I n t h e c a s e o f B r o c k m a n n ' s w a s p s , w e h a v e reason to think that our assumptions w e r e c o r r e c t , a n d that we w e r e justified in
ignoring individual
success
and
concentrating on
subroutine
success.
Therefore w h a t N. B. D a v i e s , in a lecture, j o c u l a r l y called the ' O x f o r d method'
(measuring
subroutine
(measuring i n d i v i d u a l success)
success)
and
the
'Cambridge
method'
m a y e a c h be justified in different c i r c u m -
stances. I am not s a y i n g that the O x f o r d m e t h o d should a l w a y s be used. T h e v e r y fact t h a t it is sometimes p r e f e r a b l e is sufficient to a n s w e r t h e c l a i m t h a t f i e l d w o r k e r s i n t e r e s t e d i n m e a s u r i n g costs a n d b e n e f i t s a l w a y s h a v e t o t h i n k in t e r m s of individual costs a n d b e n e f i t s . W h e n c o m p u t e r chess t o u r n a m e n t s a r e h e l d , a l a y m a n m i g h t i m a g i n e t h a t one c o m p u t e r plays against another. It is m o r e pertinent to describe the tournament as being between programs. A good p r o g r a m will consistently beat a poor p r o g r a m , and it doesn't m a k e a n y difference w h i c h physical computer cither program is running on.
Indeed the t w o p r o g r a m s could
swap physical computers every other g a m e , each one running alternately in a n I B M a n d a n I C L c o m p u t e r , a n d t h e result a t t h e e n d o f t h e t o u r n a m e n t will be the s a m e as if one p r o g r a m consistently ran in the I B M a n d the other consistently ran in the
ICL.
Similarly, to return to the a n a l o g y at the
b e g i n n i n g o f this c h a p t e r , the d i g g i n g s u b r o u t i n e ' r u n s ' i n a l a r g e n u m b e r o f different p h y s i c a l w a s p n e r v o u s s y s t e m s . E n t e r i n g i s t h e n a m e o f a r i v a l
130
Selfish W a s p or Selfish S t r a t e g y ?
subroutine
which
also
runs
in
many
different
wasp
nervous
systems,
i n c l u d i n g s o m e o f t h e s a m e p h y s i c a l n e r v o u s s y s t e m s as, a t o t h e r t i m e s , r u n the d i g g i n g s u b r o u t i n e . J u s t a s a p a r t i c u l a r I B M o r I C L c o m p u t e r f u n c t i o n s as the p h y s i c a l m e d i u m t h r o u g h w h i c h a n y of a v a r i e t y of chess p r o g r a m s c a n a c t o u t t h e i r skills, s o o n e i n d i v i d u a l w a s p i s t h e p h y s i c a l m e d i u m t h r o u g h w h i c h s o m e t i m e s the d i g g i n g subroutine, at other times the entering s u b r o u t i n e , a c t s o u t its c h a r a c t e r i s t i c b e h a v i o u r . As already explained, than programs,
I call d i g g i n g and entering 'subroutines', rather
b e c a u s e we h a v e a l r e a d y used
' p r o g r a m ' for the o v e r a l l
lifetime c h o o s i n g rules of an i n d i v i d u a l . An i n d i v i d u a l is r e g a r d e d as being p r o g r a m m e d w i t h a r u l e for c h o o s i n g t h e d i g g i n g o r t h e e n t e r i n g s u b r o u t i n e w i t h s o m e p r o b a b i l i t y p. In the special case of a p o l y m o r p h i s m , w h e r e each i n d i v i d u a l is e i t h e r a l i f e l o n g d i g g e r or a l i f e l o n g e n t e r e r , p b e c o m e s 1 or 0, and the categories p r o g r a m and subroutine b e c o m e synonymous. T h e beauty of c a l c u l a t i n g the e g g - l a y i n g success rates of subroutines rather than of i n d i v i d u a l s is that the p r o c e d u r e we a d o p t is the s a m e regardless of w h e r e on the
mixed
continuum
strategy we
continuum
still
predict
our
animals
that
the
are.
digging
Anywhere subroutine
along
the
should,
at
e q u i l i b r i u m , enjoy a success rate e q u a l to that of the entering subroutine. I t i s t e m p t i n g , t h o u g h r a t h e r m i s l e a d i n g , t o p u s h this l i n e o f t h o u g h t t o w h a t a p p e a r s t o b e its l o g i c a l c o n c l u s i o n , a n d t h i n k i n t e r m s o f s e l e c t i o n acting directly on subroutines in a subroutine pool. T h e population's nervous tissue, its d i s t r i b u t e d c o m p u t e r h a r d w a r e , i s i n h a b i t e d b y m a n y c o p i e s o f the d i g g i n g subroutine and m a n y copies of the entering subroutine. At any given time the p r o p o r t i o n of r u n n i n g copies of the d i g g i n g subroutine is p. T h e r e is a
critical
value
of p,
subroutines is equal. subroutine
pool,
c a l l e d p*,
at
which
the
success
rate
of the
two
I f e i t h e r o f t h e t w o b e c o m e s t o o n u m e r o u s i n the
natural
selection
penalizes
it
and
the
equilibrium
is
restored. The
reason
this
is
misleading
is
that
selection
really
works
on
the
d i f f e r e n t i a l s u r v i v a l o f a l l e l e s i n a g e n e p o o l . E v e n w i t h the m o s t l i b e r a l i m a g i n a b l e interpretation of w h a t we m e a n by g e n e control, there is no useful sense i n w h i c h t h e d i g g i n g s u b r o u t i n e a n d t h e e n t e r i n g s u b r o u t i n e c o u l d b e t h o u g h t o f a s b e i n g c o n t r o l l e d b y a l t e r n a t i v e a l l e l e s . I f for n o o t h e r r e a s o n , this i s b e c a u s e t h e w a s p s , a s w e h a v e s e e n , a r e n o t p o l y m o r p h i c , b u t a r e p r o g r a m m e d w i t h a s t o c h a s t i c r u l e for c h o o s i n g t o d i g o r e n t e r o n a n y g i v e n o c c a s i o n . N a t u r a l s e l e c t i o n m u s t f a v o u r g e n e s t h a t a c t o n the s t o c h a s t i c p r o g r a m o f i n d i v i d u a l s , i n p a r t i c u l a r c o n t r o l l i n g the v a l u e o f p , t h e d i g g i n g p r o b a b i l i t y . N e v e r t h e l e s s , a l t h o u g h i t i s m i s l e a d i n g i f t a k e n t o o l i t e r a l l y , the m o d e l o f s u b r o u t i n e s c o m p e t i n g d i r e c t l y for r u n n i n g t i m e i n n e r v o u s s y s t e m s p r o v i d e s s o m e useful s h o r t c u t s t o g e t t i n g t h e r i g h t a n s w e r . T h e i d e a of selection in a n o t i o n a l pool of subroutines also leads us to think about yet another time-scale on which an analogue of frequency-dependent
Selfish W a s p o r Selfish S t r a t e g y ?
131
selection m i g h t o c c u r . T h e present m o d e l a l l o w s that from d a y t o d a y the observed n u m b e r o f r u n n i n g copies o f the d i g g i n g s u b r o u t i n e m i g h t c h a n g e , as individual wasps o b e y i n g their stochastic p r o g r a m s switch their h a r d w a r e from o n e s u b r o u t i n e t o a n o t h e r . S o far I h a v e i m p l i e d t h a t a g i v e n w a s p i s born
with
a
built-in
predilection
to
dig
with
a
certain
characteristic
probability. But it is also theoretically possible that wasps m i g h t be e q u i p p e d t o m o n i t o r t h e p o p u l a t i o n a r o u n d t h e m w i t h t h e i r sense o r g a n s , a n d c h o o s e to dig or enter a c c o r d i n g l y . In E S S j a r g o n focusing on the i n d i v i d u a l l e v e l , this w o u l d b e r e g a r d e d a s a c o n d i t i o n a l s t r a t e g y , e a c h w a s p o b e y i n g a n ' i f c l a u s e ' o f t h e f o l l o w i n g f o r m : ' I f y o u see a l a r g e a m o u n t o f e n t e r i n g g o i n g on around you, dig, otherwise enter.' M o r e practically, each w a s p might be p r o g r a m m e d t o f o l l o w a r u l e o f t h u m b s u c h a s : ' S e a r c h for a b u r r o w t o e n t e r ; i f y o u h a v e n o t f o u n d o n e after a t i m e t , g i v e u p a n d d i g y o u r o w n . ' A s it
happens
our
evidence
goes
against
such
a
'conditional
strategy'
( B r o c k m a n n & D a w k i n s 1 9 7 9 ) , but the theoretical possibility is interesting. F r o m t h e p r e s e n t p o i n t o f v i e w w h a t i s p a r t i c u l a r l y i n t e r e s t i n g i s this. W e could
still
analyse
the
data
in
terms
of a
notional
selection
between
subroutines in a subroutine p o o l , even t h o u g h the selection process l e a d i n g to the r e s t o r a t i o n o f t h e e q u i l i b r i u m w h e n p e r t u r b e d w o u l d n o t b e n a t u r a l selection on a g e n e r a t i o n a l time-scale. It w o u l d be a d e v e l o p m e n t a l l y stable s t r a t e g y o r D S S ( D a w k i n s 1980) r a t h e r t h a n a n E S S , b u t t h e m a t h e m a t i c s c o u l d b e m u c h the s a m e ( H a r l e y 1 9 8 1 ) . I m u s t w a r n t h a t a n a l o g i c a l r e a s o n i n g o f this sort i s a l u x u r y t h a t w e d a r e not i n d u l g e unless we are c a p a b l e of c l e a r l y seeing the limitations of the analogy.
T h e r e are real
and
important distinctions
between
Darwinian
selection and b e h a v i o u r a l assessment, just as there w e r e real a n d i m p o r t a n t distinctions b e t w e e n a b a l a n c e d p o l y m o r p h i s m and
a
true m i x e d
evol-
utionarily stable strategy. Just as the v a l u e of p, the i n d i v i d u a l ' s d i g g i n g probability, w a s considered to be adjusted by n a t u r a l selection, so, in the b e h a v i o u r a l a s s e s s m e n t m o d e l , t , t h e i n d i v i d u a l ' s c r i t e r i o n for r e s p o n d i n g t o the frequency of d i g g i n g in the p o p u l a t i o n , is p r e s u m a b l y influenced by natural
selection.
The
concept
of selection
among
subroutines
in
a
subroutine pool blurs some important distinctions while p o i n t i n g up some i m p o r t a n t s i m i l a r i t i e s : t h e w e a k n e s s e s o f this w a y o f t h i n k i n g a r e l i n k e d t o its strengths. W h a t I do r e m e m b e r is that, w h e n we w e r e a c t u a l l y wrestling w i t h the difficulties o f t h e w a s p a n a l y s i s , o n e o f o u r m a i n l e a p s f o r w a r d occurred w h e n , u n d e r the influence o f A . G r a f e n , w e k i c k e d the h a b i t o f worrying imaginary
about world
individual where
reproductive
'digging'
success
competed
and
directly
switched with
to
an
'entering';
c o m p e t e d for ' r u n n i n g t i m e ' i n f u t u r e n e r v o u s s y s t e m s . T h i s chapter has been an interlude, a digression. I h a v e not been trying to a r g u e that 'subroutines', or 'strategies' are really true replicators, true units of natural selection. T h e y are not. G e n e s and fragments of g e n o m e s are true
132
Selfish W a s p or Selfish S t r a t e g y ?
r e p l i c a t o r s . S u b r o u t i n e s a n d s t r a t e g i e s c a n b e t h o u g h t o f for c e r t a i n p u r p o s e s as if they w e r e replicators, but w h e n those purposes h a v e been served we m u s t r e t u r n t o r e a l i t y . N a t u r a l s e l e c t i o n r e a l l y h a s t h e effect o f c h o o s i n g b e t w e e n alleles in w a s p gene-pools, alleles w h i c h influence the probability t h a t i n d i v i d u a l w a s p s w i l l e n t e r o r d i g . W e t e m p o r a r i l y l a i d this k n o w l e d g e a s i d e a n d e n t e r e d a n i m a g i n a r y w o r l d o f ' i n t e r - s u b r o u t i n e s e l e c t i o n ' for a s p e c i f i c m e t h o d o l o g i c a l p u r p o s e . W e w e r e j u s t i f i e d i n d o i n g this b e c a u s e w e w e r e a b l e to m a k e certain assumptions a b o u t the wasps, and because of the a l r e a d y d e m o n s t r a t e d m a t h e m a t i c a l e q u i v a l e n c e b e t w e e n the various w a y s in w h i c h a m i x e d evolutionarily stable strategy can be put together. As in the case of C h a p t e r 4,
t h e p u r p o s e o f this c h a p t e r h a s b e e n t o
u n d e r m i n e our c o n f i d e n c e in the i n d i v i d u a l - c e n t r e d v i e w of teleonomy, in this c a s e b y s h o w i n g t h a t i t i s n o t a l w a y s useful, i n p r a c t i c e , t o m e a s u r e i n d i v i d u a l s u c c e s s i f w e a r e t o s t u d y n a t u r a l s e l e c t i o n i n the f i e l d . T h e n e x t t w o chapters discuss a d a p t a t i o n s w h i c h , b y their v e r y nature, w e c a n n o t e v e n b e g i n t o u n d e r s t a n d i f w e insist o n t h i n k i n g i n t e r m s o f i n d i v i d u a l benefit.
8 O u t l a w s and Modifiers
N a t u r a l selection is the process w h e r e b y replicators o u t - p r o p a g a t e e a c h o t h e r . T h e y d o this b y e x e r t i n g p h e n o t y p i c effects o n t h e w o r l d , a n d i t i s often c o n v e n i e n t t o see t h o s e p h e n o t y p i c effects a s g r o u p e d t o g e t h e r i n discrete 'vehicles' such as i n d i v i d u a l organisms. T h i s gives s u b s t a n c e to the orthodox doctrine that each i n d i v i d u a l b o d y c a n be t h o u g h t of as a unitary agent m a x i m i z i n g one quantity—'fitness', various notions of w h i c h will be discussed i n C h a p t e r 1 0 . B u t the i d e a o f i n d i v i d u a l b o d i e s m a x i m i z i n g o n e q u a n t i t y relies o n t h e a s s u m p t i o n t h a t r e p l i c a t o r s a t d i f f e r e n t l o c i w i t h i n a b o d y can be e x p e c t e d to ' c o o p e r a t e ' . In other w o r d s we must assume that the a l l e l e t h a t s u r v i v e s best a t a n y g i v e n l o c u s t e n d s t o b e t h e o n e t h a t i s b e s t for the g e n o m e as a w h o l e . T h i s is i n d e e d o f t e n t h e c a s e . A r e p l i c a t o r t h a t e n s u r e s its o w n s u r v i v a l a n d p r o p a g a t i o n d o w n t h e g e n e r a t i o n s b y c o n f e r r i n g o n its s u c c e s s i v e b o d i e s r e s i s t a n c e t o a d a n g e r o u s d i s e a s e , s a y , w i l l t h e r e b y b e n e f i t all the o t h e r g e n e s i n t h e s u c c e s s i v e g e n o m e s o f w h i c h i t i s a m e m b e r . B u t i t i s a l s o e a s y t o i m a g i n e c a s e s w h e r e a g e n e m i g h t p r o m o t e its o w n survival while
h a r m i n g the s u r v i v a l c h a n c e s of most
of the
rest o f t h e
genome. Following A l e x a n d e r and Borgia (1978) I shall call such genes outlaws. I d i s t i n g u i s h t w o m a i n classes o f o u t l a w s . A n ' a l l e l i c o u t l a w ' i s d e f i n e d a s a r e p l i c a t o r t h a t h a s a p o s i t i v e s e l e c t i o n c o e f f i c i e n t a t its o w n l o c u s b u t for w h i c h , a t m o s t o t h e r l o c i , t h e r e i s s e l e c t i o n i n f a v o u r o f r e d u c i n g its effect a t its o w n l o c u s . A n e x a m p l e i s a ' s e g r e g a t i o n d i s t o r t e r ' o r ' m e i o t i c d r i v e ' g e n e . I t i s f a v o u r e d a t its o w n l o c u s t h r o u g h g e t t i n g i t s e l f i n t o m o r e t h a n 5 0 p e r c e n t o f the g a m e t e s p r o d u c e d . A t t h e s a m e t i m e , g e n e s a t o t h e r l o c i w h o s e effect i s t o r e d u c e t h e s e g r e g a t i o n d i s t o r t i o n w i l l b e f a v o u r e d b y s e l e c t i o n a t their respective loci. H e n c e the s e g r e g a t i o n distorter is an o u t l a w . T h e other m a i n class o f o u t l a w , t h e ' l a t e r a l l y s p r e a d i n g o u t l a w ' , i s less f a m i l i a r . I t w i l l b e discussed i n the n e x t c h a p t e r . F r o m t h e v i e w p o i n t o f this b o o k t h e r e i s a sense i n w h i c h w e e x p e c t a l l genes to be potential o u t l a w s , so m u c h so that the v e r y t e r m m i g h t seem 133
134
O u t l a w s and M o d i f i e r s
s u p e r f l u o u s . O n t h e o t h e r h a n d i t c a n b e a r g u e d , firstly, t h a t o u t l a w s a r e u n l i k e l y to be f o u n d in n a t u r e b e c a u s e at a n y g i v e n locus the allele that is best a t s u r v i v i n g w i l l n e a r l y a l w a y s t u r n o u t t o b e t h e a l l e l e t h a t i s best a t promoting
the
survival
and
reproduction
of the
organism
as
a
whole.
S e c o n d l y various authors, following L e i g h ( 1 9 7 1 ) , h a v e argued that, even if o u t l a w s did arise a n d w e r e t e m p o r a r i l y favoured by selection, they are likely, i n A l e x a n d e r a n d B o r g i a ' s w o r d s , ' t o h a v e t h e i r effects n u l l i f i e d , a t least t o t h e e x t e n t t h a t t h e y a r e o u t n u m b e r e d b y t h e o t h e r g e n e s i n the g e n o m e ' . I t d o e s , i n d e e d , f o l l o w f r o m t h e d e f i n i t i o n o f a n o u t l a w t h a t this s h o u l d t e n d t o h a p p e n . T h e s u g g e s t i o n b e i n g m a d e i s t h a t , w h e n e v e r a n o u t l a w arises, s e l e c t i o n w i l l f a v o u r m o d i f i e r g e n e s a t s o m a n y o t h e r loci t h a t n o t r a c e w i l l r e m a i n o f t h e p h e n o t y p i c effects o f t h e o u t l a w . O u t l a w s w i l l t h e r e f o r e , t h e suggestion goes, be transient p h e n o m e n a . T h i s w o u l d not, h o w e v e r , make t h e m n e g l i g i b l e : i f g e n o m e s a r e r i d d l e d w i t h o u t l a w - s u p p r e s s i n g g e n e s , this, i n itself, i s a n i m p o r t a n t effect o f o u t l a w g e n e s , e v e n i f n o t r a c e r e m a i n s o f t h e i r o r i g i n a l p h e n o t y p i c effects. I s h a l l d i s c u s s t h e r e l e v a n c e o f m o d i f i e r g e n e s in a l a t e r s e c t i o n . T h e r e is a sense in w h i c h a ' v e h i c l e ' is w o r t h y of the n a m e in inverse proportion to the n u m b e r of o u t l a w replicators that it contains. T h e idea of a discrete v e h i c l e m a x i m i z i n g a u n i t a r y q u a n t i t y — f i t n e s s — d e p e n d s on the a s s u m p t i o n t h a t t h e r e p l i c a t o r s t h a t i t s e r v e s a l l s t a n d t o g a i n f r o m the s a m e properties a n d b e h a v i o u r of their shared vehicle. If some replicators w o u l d b e n e f i t f r o m t h e v e h i c l e ' s d o i n g a c t X , w h i l e o t h e r r e p l i c a t o r s w o u l d benefit f r o m its d o i n g a c t Y , t h a t v e h i c l e i s c o r r e s p o n d i n g l y less l i k e l y t o b e h a v e a s a coherent unit. governed
by
It will h a v e the attributes of a h u m a n o r g a n i z a t i o n that is a
quarrelsome
committee—pulled
this
way
and
that,
and
unable to show decisiveness and consistency of purpose. T h e r e is a superficial a n a l o g y here with g r o u p selection.
O n e o f the
p r o b l e m s of the t h e o r y that g r o u p s of o r g a n i s m s function as effective g e n e v e h i c l e s i s t h a t o u t l a w s (from t h e g r o u p ' s p o i n t o f v i e w ) a r e v e r y l i k e l y t o a r i s e a n d b e f a v o u r e d b y s e l e c t i o n . I f w e a r e h y p o t h e s i z i n g the e v o l u t i o n o f individual restraint through g r o u p selection, a gene that makes individuals b e h a v e selfishly i n a n o t h e r w i s e a l t r u i s t i c g r o u p i s a n a l o g o u s t o a n o u t l a w . I t is the n e a r i n e v i t a b i l i t y of such ' o u t l a w s ' arising that has d a s h e d the hopes of m a n y a g r o u p selection modeller. T h e i n d i v i d u a l b o d y i s a m u c h m o r e p e r s u a s i v e g e n e v e h i c l e t h a n the g r o u p b e c a u s e , a m o n g o t h e r r e a s o n s , o u t l a w r e p l i c a t o r s w i t h i n the b o d y a r e not v e r y likely to be strongly favoured over their alleles. T h e fundamental r e a s o n for
this
is
the drilled
formality of the
mechanisms of individual
r e p r o d u c t i o n , t h e ' g a v o t t e o f c h r o m o s o m e s ' a s H a m i l t o n ( 1 9 7 5 b ) c a l l e d it. I f all replicators ' k n o w ' that their o n l y h o p e of g e t t i n g into the next generation is v i a the o r t h o d o x b o t t l e n e c k of i n d i v i d u a l r e p r o d u c t i o n , all will h a v e the s a m e 'interests at h e a r t ' ; s u r v i v a l of the shared b o d y to r e p r o d u c t i v e age,
O u t l a w s and M o d i f i e r s
135
successful c o u r t s h i p a n d r e p r o d u c t i o n o f t h e s h a r e d b o d y , a n d a successful o u t c o m e to the parental enterprise of the shared b o d y .
E n l i g h t e n e d self-
interest d i s c o u r a g e s o u t l a w r y w h e n all r e p l i c a t o r s h a v e a n e q u a l s t a k e i n t h e normal r e p r o d u c t i o n of the same shared b o d y . Where
reproduction
is
asexual
the
stake
is
equal
and
total,
for
all
r e p l i c a t o r s h a v e t h e s a m e 100 p e r c e n t c h a n c e o f f i n d i n g t h e m s e l v e s i n e v e r y child
produced
by
their joint
c o r r e s p o n d i n g c h a n c e for
efforts.
Where
reproduction
is sexual
each replicator is only half as great,
but
the the
ritualized courtliness of meiosis, H a m i l t o n ' s ' g a v o t t e ' , l a r g e l y succeeds in g u a r a n t e e i n g to e a c h allele an equal c h a n c e of r e a p i n g the benefits of the success o f t h e j o i n t r e p r o d u c t i v e e n t e r p r i s e . I t is, o f c o u r s e , a n o t h e r q u e s t i o n why t h e g a v o t t e
of t h e c h r o m o s o m e s
is so c o u r t l y .
It
is
an
immensely
important question w h i c h I shall e v a d e on a simple p l e a of c o w a r d i c e . It is one o f a set o f q u e s t i o n s a b o u t t h e e v o l u t i o n o f g e n e t i c s y s t e m s w i t h w h i c h b e t t e r m i n d s t h a n m i n e h a v e w r e s t l e d m o r e o r less u n s u c c e s s f u l l y ( W i l l i a m s 1 9 7 5 , 1 9 8 0 ; M a y n a r d S m i t h 1 9 7 8 a ) , a set o f q u e s t i o n s w h i c h m o v e d W i l l i a m s t o r e m a r k t h a t ' t h e r e i s a k i n d o f crisis a t h a n d i n e v o l u t i o n a r y b i o l o g y ' . I d o n ' t u n d e r s t a n d w h y m e i o s i s i s t h e w a y i t is, b u t g i v e n t h a t i t i s m u c h f o l l o w s . I n particular the o r g a n i z e d
f a i r - d e a l i n g o f m e i o s i s h e l p s t o a c c o u n t for t h e
c o h e r e n c e a n d h a r m o n y w h i c h u n i t e s t h e p a r t s o f a n i n d i v i d u a l o r g a n i s m . If, a t t h e l e v e l o f t h e group o f i n d i v i d u a l s a s p o t e n t i a l v e h i c l e , t h e p r i v i l e g e o f reproduction was g r a n t e d w i t h the same scrupulous p r o b i t y in a similarly well-disciplined 'gavotte of the organisms', g r o u p selection m i g h t b e c o m e a more plausible theory of e v o l u t i o n . But, w i t h the possible e x c e p t i o n of the v e r y s p e c i a l c a s e o f t h e s o c i a l insects, g r o u p ' r e p r o d u c t i o n ' i s a n a r c h i c a l a n d favourable to individual o u t l a w r y . E v e n social insect colonies will never s e e m fully h a r m o n i o u s a g a i n after T r i v e r s a n d H a r e ' s i n g e n i o u s a n a l y s i s o f sex r a t i o c o n f l i c t s (see C h a p t e r 4 ) . T h i s c o n s i d e r a t i o n tells u s w h e r e w e s h o u l d l o o k first i f w e w a n t t o d i s c o v e r o u t l a w s w i t h i n the i n d i v i d u a l b o d y a s v e h i c l e . A n y r e p l i c a t o r t h a t m a n a g e d t o s u b v e r t t h e rules o f m e i o s i s s o t h a t i t e n j o y e d m o r e t h a n t h e o r d a i n e d 5 0 per cent c h a n c e of e n d i n g up in a g a m e t e w o u l d , other things b e i n g e q u a l , tend t o b e f a v o u r e d o v e r its a l l e l e s i n n a t u r a l s e l e c t i o n . S u c h g e n e s a r e k n o w n t o g e n e t i c i s t s u n d e r the n a m e o f m e i o t i c d r i v e g e n e s o r s e g r e g a t i o n d i s t o r t e r s . I h a v e already used
them
as an e x a m p l e to illustrate my definition of an
outlaw.
'Genes that beat the system' T h e a c c o u n t of segregation distorters that I shall m a i n l y follow is that of C r o w ( 1 9 7 9 ) , w h o uses l a n g u a g e c o n g e n i a l t o t h e s p i r i t o f this b o o k . H i s paper is called ' G e n e s that violate M e n d e l ' s rules', and it ends as follows: 'The
Mendelian
system
works
with
maximum
efficiency
only
if it
is
s c r u p u l o u s l y fair t o all g e n e s . I t i s i n c o n s t a n t d a n g e r , h o w e v e r , o f b e i n g
136
O u t l a w s and M o d i f i e r s
upset
by
genes
that
subvert
the
meiotic
process
to
their
own
a d v a n t a g e . . . T h e r e are m a n y refinements of meiosis a n d sperm formation whose purpose is a p p a r e n t l y to render such cheating unlikely. A n d yet some genes h a v e m a n a g e d to beat the system.' C r o w suggests that segregation distorters m a y b e m u c h m o r e c o m m o n t h a n w e o r d i n a r i l y r e a l i z e , for t h e m e t h o d s o f g e n e t i c i s t s a r e n o t w e l l g e a r e d t o d e t e c t i n g t h e m , e s p e c i a l l y i f t h e y p r o d u c e o n l y s l i g h t , q u a n t i t a t i v e effects. T h e S D g e n e s i n Drosophila a r e p a r t i c u l a r l y w e l l s t u d i e d , a n d h e r e t h e r e i s some
indication
homologous
as
to
the
chromosomes
actual are
still
mechanism paired
up
of distortion. during
'While
meiosis,
c h r o m o s o m e m i g h t do something to its n o r m a l p a r t n e r ( a n d r i v a l )
the
the SD
that later
causes a dysfunction of the sperm r e c e i v i n g the n o r m a l c h r o m o s o m e . . . SD might
actually break
the other c h r o m o s o m e '
(Crow
1979,
my macabre
emphasis). T h e r e is e v i d e n c e that, in S D - h e t e r o z y g o u s individuals, sperms not c o n t a i n i n g the S D c h r o m o s o m e h a v e a b n o r m a l , a n d p r e s u m a b l y faulty, tails.
It
might
be
thought,
then,
that
the faulty
tail
results f r o m s o m e
s a b o t a g e t o t h e n o n - S D c h r o m o s o m e i n t h e s p e r m s c o n t a i n i n g it. T h i s c a n n o t be the w h o l e story, as C r o w points out, because sperms h a v e been shown to b e c a p a b l e o f d e v e l o p i n g n o r m a l tails w i t h o u t a n y c h r o m o s o m e s a t a l l . I n d e e d , the w h o l e sperm p h e n o t y p e seems usually to be u n d e r the control of t h e d i p l o i d g e n o t y p e o f t h e f a t h e r , n o t its o w n h a p l o i d g e n o t y p e ( B e a t t y & G l u e c k s o h n - W a e l s c h 1 9 7 2 ; see b e l o w ) . ' T h e effect o f t h e S D c h r o m o s o m e o n its h o m o l o g u e c a n n o t , t h e n , b e s i m p l y t o i n a c t i v a t e s o m e f u n c t i o n , b e c a u s e n o f u n c t i o n i s r e q u i r e d . S D m u s t s o m e h o w i n d u c e its p a r t n e r t o c o m m i t a positive act of sabotage.' S e g r e g a t i o n distorters prosper w h e n rare, because the chances are then g o o d that their v i c t i m s are alleles, not copies. W h e n c o m m o n , the distorter t e n d s t o o c c u r h o m o z y g o u s l y , a n d t h e r e f o r e s a b o t a g e s c o p i e s o f itself, m a k i n g t h e o r g a n i s m v i r t u a l l y s t e r i l e . T h e s t o r y i s m o r e c o m p l i c a t e d t h a n this, b u t c o m p u t e r simulations described by C r o w suggest that a stable proportion of segregation distorter genes will be maintained
at
a frequency somewhat
g r e a t e r t h a n w o u l d b e a c c o u n t e d for b y r e c u r r e n t m u t a t i o n a l o n e . T h e r e i s s o m e e v i d e n c e t h a t this i s s o i n r e a l life. In order to qualify as an o u t l a w , a segregation distorter must do harm to m o s t o f t h e rest o f t h e g e n o m e , n o t j u s t t o its a l l e l e s . S e g r e g a t i o n distorters c o u l d h a v e this effect b y r e d u c i n g t h e t o t a l g a m e t e c o u n t o f t h e i n d i v i d u a l . E v e n i f t h e y d i d n o t d o this, t h e r e i s a m o r e g e n e r a l r e a s o n for e x p e c t i n g there to be selection at other loci in favour of suppressing them ( C r o w 1979). T h e a r g u m e n t needs to be d e v e l o p e d stage by stage. Firstly m a n y genes, w h e n c o m p a r e d w i t h t h e i r a l l e l e s , h a v e s e v e r a l p l e i o t r o p i c effects. L e w o n t i n ( 1 9 7 4 ) g o e s s o far a s t o s p e a k o f ' . . . t h e u n d o u b t e d t r u t h t h a t e v e r y g e n e affects e v e r y c h a r a c t e r . . .'. W h i l e t o c a l l this a n ' u n d o u b t e d t r u t h ' m a y b e ,
O u t l a w s and M o d i f i e r s
137
t o p u t i t m i l d l y , a n e n t h u s i a s t i c e x a g g e r a t i o n , for m y p u r p o s e s I n e e d o n l y a s s u m e t h a t m o s t n e w m u t a t i o n s h a v e s e v e r a l p l e i o t r o p i c effects. N o w i t i s r e a s o n a b l e t o e x p e c t t h a t m o s t s u c h p l e i o t r o p i c effects w i l l b e d e l e t e r i o u s — m u t a t i o n a l effects u s u a l l y a r e . I f a g e n e i s f a v o u r e d b y s e l e c t i o n r e s u l t i n g f r o m o n e b e n e f i c i a l effect, this w i l l b e b e c a u s e t h e a d v a n t a g e s o f its b e n e f i c i a l effect q u a n t i t a t i v e l y o u t w e i g h t h e d i s a d v a n t a g e s o f its o t h e r effects. Normally,
by
'beneficial'
and
'deleterious',
deleterious to the w h o l e o r g a n i s m .
we
mean
beneficial
and
In the case of a segregation distorter,
h o w e v e r , t h e b e n e f i c i a l effect w e a r e t a l k i n g a b o u t i s b e n e f i c i a l t o t h e g e n e a l o n e . A n y p l e i o t r o p i c effects t h a t i t m a y h a v e o n t h e b o d y a r e p r e t t y l i k e l y to be deleterious to the w h o l e b o d y ' s s u r v i v a l a n d r e p r o d u c t i o n . S e g r e g a t i o n distorters a r e t h e r e f o r e , o n t h e w h o l e , l i k e l y t o b e o u t l a w s : w e e x p e c t t h a t s e l e c t i o n w i l l f a v o u r g e n e s a t o t h e r l o c i w h o s e p h e n o t y p i c effect i s t o r e d u c e the s e g r e g a t i o n d i s t o r t i o n . T h i s b r i n g s u s t o t h e t o p i c o f m o d i f i e r s .
Modifiers T h e classic p r o v i n g g r o u n d for t h e t h e o r y o f m o d i f i e r g e n e s w a s R . A . F i s h e r ' s e x p l a n a t i o n o f t h e e v o l u t i o n o f d o m i n a n c e . F i s h e r ( 1 9 3 0 a , b u t see C h a r l e s w o r t h 1 9 7 9 ) s u g g e s t e d t h a t t h e b e n e f i c i a l effects o f a g i v e n g e n e t e n d t o b e c o m e d o m i n a n t t h r o u g h t h e s e l e c t i o n o f m o d i f i e r s , w h i l e its d e l e t e r i o u s effects t e n d t o b e c o m e r e c e s s i v e . H e n o t e d t h a t d o m i n a n c e a n d r e c e s s i v e n e s s are not properties of genes themselves, b u t properties of their p h e n o t y p i c effects. I n d e e d a g i v e n g e n e c a n b e d o m i n a n t i n o n e o f its p l e i o t r o p i c effects a n d r e c e s s i v e i n a n o t h e r . A p h e n o t y p i c effect o f a g e n e i s t h e j o i n t p r o d u c t o f itself a n d its e n v i r o n m e n t , a n e n v i r o n m e n t w h i c h i n c l u d e s t h e rest o f t h e g e n o m e . T h i s i n t e r a c t i v e v i e w o f g e n e a c t i o n , w h i c h F i s h e r h a d t o a r g u e for at length in 1930, h a d b e c o m e so well a c c e p t e d by 1958 that he w a s a b l e to t a k e i t for g r a n t e d i n t h e s e c o n d e d i t i o n o f his g r e a t b o o k . I t f o l l o w s f r o m i t t h a t d o m i n a n c e o r r e c e s s i v e n e s s , l i k e a n y o t h e r p h e n o t y p i c effect, m a y i t s e l f e v o l v e , t h r o u g h t h e s e l e c t i o n o f o t h e r g e n e s e l s e w h e r e i n t h e g e n o m e , a n d this w a s the basis o f F i s h e r ' s t h e o r y o f d o m i n a n c e . A l t h o u g h t h e s e o t h e r g e n e s a r e k n o w n as modifiers, it is n o w realized that there is no separate c a t e g o r y of modifier genes as distinct from major genes. R a t h e r , a n y g e n e m a y serve as m o d i f i e r o f t h e p h e n o t y p i c effects o f a n y o t h e r g e n e . I n d e e d , a n y g i v e n g e n e ' s p h e n o t y p i c effects a r e s u s c e p t i b l e t o m o d i f i c a t i o n b y m a n y o t h e r g e n e s i n t h e genome, genes w h i c h themselves m a y h a v e m a n y other major and minor effects
(Mayr
theoretical
1963).
purposes,
Modifiers for
have
instance
in
been the
invoked
for
various
other
Medawar/Williams/Hamilton
progression of theories of the e v o l u t i o n of senescence ( K i r k w o o d & H o l l i d a y 1979)T h e r e l e v a n c e o f modifiers t o the subject o f o u t l a w genes has a l r e a d y b e e n alluded
to.
Since
any
gene's
phenotypic
effects
may
be
subject
to
138
O u t l a w s and M o d i f i e r s
modification by genes at other loci, and since outlaws, by definition, work to t h e d e t r i m e n t o f t h e rest o f t h e g e n o m e , w e s h o u l d e x p e c t s e l e c t i o n t o f a v o u r g e n e s t h a t h a p p e n t o h a v e t h e effect o f n e u t r a l i z i n g the o u t l a w ' s d e l e t e r i o u s effects o n t h e b o d y a s a w h o l e . S u c h m o d i f i e r s w o u l d b e f a v o u r e d o v e r alleles t h a t d i d n o t i n f l u e n c e t h e o u t l a w ' s effects. H i c k e y a n d C r a i g ( 1 9 6 6 ) , s t u d y i n g a s e x - r a t i o d i s t o r t i n g g e n e (see b e l o w ) in t h e y e l l o w - f e v e r m o s q u i t o Aedes aegypti, f o u n d e v i d e n c e for e v o l u t i o n a r y d i m i n u t i o n o f t h e d i s t o r t i n g effect which
could
be
interpreted
as
r e s u l t i n g from
the selection of modifiers
(though their o w n interpretation was slightly different). If outlaws do, in general,
call
forth
the
selection
of suppressing
modifiers,
there
will
p r e s u m a b l y b e a n a r m s r a c e b e t w e e n e a c h o u t l a w a n d its m o d i f i e r s . A s i n a n y o t h e r a r m s r a c e ( C h a p t e r 4 ) , w e n o w ask w h e t h e r t h e r e i s a n y g e n e r a l r e a s o n t o e x p e c t o n e side t o p r e v a i l o v e r t h e o t h e r . L e i g h ( 1 9 7 1 , 1 9 7 7 ) , A l e x a n d e r a n d B o r g i a ( 1 9 7 8 ) , K u r l a n d ( 1 9 7 9 , 1 9 8 0 ) , H a r t u n g (in p r e s s ) , a n d o t h e r s s u g g e s t t h a t t h e r e i s j u s t s u c h a g e n e r a l r e a s o n . S i n c e , for a n y single o u t l a w , suppressing modifiers m a y arise a n y w h e r e in the g e n o m e , t h e o u t l a w w i l l b e o u t n u m b e r e d . A s L e i g h ( 1 9 7 1 ) p u t s it, ' I t i s a s i f w e h a d t o d o w i t h a p a r l i a m e n t o f g e n e s : e a c h a c t s i n its o w n self-interest, b u t i f its acts h u r t t h e o t h e r s , t h e y w i l l c o m b i n e t o g e t h e r t o s u p p r e s s i t . . . H o w e v e r , a t loci s o c l o s e l y l i n k e d t o a d i s t o r t e r t h a t t h e benefits o f " r i d i n g its c o a t t a i l s " o u t w e i g h t h e d a m a g e o f its d i s e a s e , s e l e c t i o n t e n d s t o e n h a n c e the d i s t o r t i o n effect. T h u s a s p e c i e s m u s t h a v e m a n y c h r o m o s o m e s if, w h e n a d i s t o r t e r arises, s e l e c t i o n at m o s t l o c i is to f a v o r its s u p p r e s s i o n . J u s t as t o o s m a l l a p a r l i a m e n t m a y be p e r v e r t e d by the C a b a l s of a few, a species w i t h only one, slightly linked c h r o m o s o m e is an easy prey to distorters' ( L e i g h 1971, p. 249). I am not sure w h a t I think a b o u t L e i g h ' s point a b o u t chromosome numbers,
b u t his m o r e g e n e r a l p o i n t t h a t t h e r e i s s o m e sense i n w h i c h
o u t l a w s m a y b e ' o u t n u m b e r e d ' ( A l e x a n d e r & B o r g i a 1 9 7 8 , p . 4 5 8 ) b y their modifiers seems to me to h a v e promise. I suppose ' o u t n u m b e r i n g ' could, in practice, work in two main ways. F i r s t l y , i f d i f f e r e n t m o d i f i e r s e a c h c a u s e a q u a n t i t a t i v e d i m i n u t i o n o f the o u t l a w ' s effect, s e v e r a l m o d i f i e r s m i g h t c o m b i n e a d d i t i v e l y . S e c o n d l y , i f a n y o n e o f s e v e r a l m o d i f i e r s w o u l d suffice t o n e u t r a l i z e t h e o u t l a w , t h e c h a n c e o f effective n e u t r a l i z a t i o n goes up w i t h the n u m b e r of a v a i l a b l e modifier loci. Alexander and Borgia's metaphor of 'outnumbering', and Leigh's metaphor of the p o w e r of the c o l l e c t i v e in a ' p a r l i a m e n t ' of the m a n y , c o u l d be given m e a n i n g i n e i t h e r o r b o t h o f these t w o w a y s . I t i s i m p o r t a n t for t h e a r g u m e n t t h a t s e g r e g a t i o n d i s t o r t e r s a t different l o c i c o u l d n o t , i n a n y o b v i o u s sense, ' p o o l t h e i r efforts'. T h e y a r e n o t w o r k i n g for s o m e c o m m o n e n d o f ' g e n e r a l segregation distortion'. R a t h e r , e a c h one is w o r k i n g to distort segregation in f a v o u r o f itself, a n d this w i l l h u r t o t h e r s e g r e g a t i o n d i s t o r t e r s j u s t a s m u c h a s it hurts non-distorters.
Suppressors of segregation distorters, on the other
h a n d , c o u l d , in a sense, p o o l t h e i r efforts.
O u t l a w s and M o d i f i e r s
139
T h e p a r l i a m e n t o f genes i s o n e o f those m e t a p h o r s w h i c h , i f w e are not c a r e f u l , tricks u s i n t o t h i n k i n g t h a t i t e x p l a i n s m o r e t h a n i t d o e s . L i k e all humans,
but
unlike
genes,
human
Members
of Parliament
are
highly
sophisticated c o m p u t e r s c a p a b l e of using foresight a n d l a n g u a g e to conspire and reach agreements. O u t l a w s m a y seem to be suppressed by a g r e e m e n t of a collective in the p a r l i a m e n t of genes, but w h a t is really g o i n g on is the selection of modifier genes in preference to n o n - m o d i f y i n g alleles at their respective
loci.
Needless
to say,
Leigh
and
the
other
a d v o c a t e s of the
' p a r l i a m e n t o f g e n e s ' h y p o t h e s i s a r e w e l l a w a r e o f this. I n o w w a n t t o e x t e n d the list o f o u t l a w s .
Sex-linked outlaws If a segregation distorter occurs on a sex c h r o m o s o m e , it is not o n l y an outlaw in conflict with suppression
by
population
with
t h e rest o f t h e g e n o m e a n d
modifiers:
it
extinction.
also,
This
incidentally,
is
because,
therefore subject threatens
in
addition
the to
to
whole
ordinary
d e t r i m e n t a l side effects, i t a l s o distorts t h e sex r a t i o , a n d m a y e v e n e l i m i n a t e one
sex
from
the
population
altogether.
In
one
of Hamilton's
(1967)
c o m p u t e r simulations, a single m u t a n t m a l e w i t h a ' d r i v i n g Y' c h r o m o s o m e c a u s i n g m a l e s t o h a v e o n l y sons a n d n o d a u g h t e r s , w a s i n t r o d u c e d i n t o a p o p u l a t i o n o f 1000 m a l e s a n d 1000 f e m a l e s . I t t o o k o n l y f i f t e e n g e n e r a t i o n s t o d r i v e t h e m o d e l p o p u l a t i o n e x t i n c t for l a c k o f f e m a l e s . S o m e t h i n g l i k e this effect h a s b e e n d e m o n s t r a t e d i n t h e l a b o r a t o r y ( L y t t l e 1 9 7 7 ) . T h e p o s s i b i l i t y o f u s i n g a d r i v i n g Y g e n e i n t h e c o n t r o l o f s e r i o u s pests l i k e t h e y e l l o w - f e v e r mosquito did not escape H i c k e y a n d C r a i g ( 1 9 6 6 ) . It is a m e t h o d w i t h sinister e l e g a n c e b e c a u s e i t i s s o c h e a p : a l l t h e w o r k o f s p r e a d i n g t h e p e s t c o n t r o l a g e n t i s d o n e b y t h e pests t h e m s e l v e s t o g e t h e r w i t h n a t u r a l s e l e c t i o n . It is like ' g e r m w a r f a r e ' e x c e p t that the lethal ' g e r m ' is not an e x t r a n e o u s virus but a g e n e in the species's o w n g e n e - p o o l . P e r h a p s the distinction is not a fundamental one a n y w a y (Chapter 9). X - l i n k e d d r i v e i s l i k e l y t o h a v e t h e s a m e sort o f d e t r i m e n t a l effect o n populations
as
Y-linked
extinguish the population
drive,
but
(Hamilton
tends 1967).
to
take
more
generations
T h e driving gene on
c h r o m o s o m e c a u s e s m a l e s t o h a v e d a u g h t e r s r a t h e r t h a n sons birds,
Lepidoptera,
etc.).
As
we
saw
in
Chapter
4,
an
to X
(except in
if haploid
male
H y m e n o p t e r a c o u l d influence the a m o u n t of care d e v o t e d to their spouses' offspring, t h e y w o u l d f a v o u r d a u g h t e r s r a t h e r t h a n sons, s i n c e m a l e s pass n o g e n e s o n t o sons. T h e m a t h e m a t i c s o f this s i t u a t i o n a r e a n a l o g o u s t o t h e c a s e o f X - l i n k e d drive, the w h o l e g e n o m e o f the m a l e h y m e n o p t e r a n f u n c t i o n i n g like a n X c h r o m o s o m e ( H a m i l t o n 1 9 6 7 , p . 481 a n d f o o t n o t e 1 8 ) . I t i s often t h e c a s e t h a t X c h r o m o s o m e s cross o v e r w i t h e a c h o t h e r b u t n o t w i t h Y c h r o m o s o m e s . It follows that all genes on X c h r o m o s o m e s c o u l d stand t o g a i n from t h e p r e s e n c e i n t h e g e n e - p o o l o f a d r i v i n g X g e n e w h i c h d i s t o r t s
140
O u t l a w s and Modifiers
g a m e t o g e n e s i s i n t h e h e t e r o g a m e t i c sex i n f a v o u r o f X g a m e t e s a n d a g a i n s t Y g a m e t e s . G e n e s on X c h r o m o s o m e s a r e , in a sense, u n i t e d a g a i n s t Y g e n e s , in a kind of 'anti linkage g r o u p ' , simply because they h a v e no c h a n c e of finding themselves on a Y c h r o m o s o m e . Modifiers to suppress X - l i n k e d meiotic drive i n t h e h e t e r o g a m e t i c s e x m i g h t w e l l n o t b e f a v o u r e d i f t h e y a r o s e a t o t h e r loci on X c h r o m o s o m e s . T h e y w o u l d be favoured if they arose on autosomes. T h i s is different from the case of segregation distorters on a u t o s o m e s : here there m i g h t w e l l be selection in favour of suppressing them by modifiers at other
loci
even
on
the same
chromosome.
X-linked
distorters
affecting
g a m e t e p r o d u c t i o n i n t h e h e t e r o g a m e t i c s e x a r e , t h e n , o u t l a w s from the p o i n t o f v i e w o f t h e a u t o s o m a l p a r t o f t h e g e n e - p o o l , b u t n o t from the p o i n t o f v i e w o f t h e rest o f t h e X - c h r o m o s o m a l p a r t o f t h e g e n e - p o o l . T h i s p o t e n t i a l ' s o l i d a r i t y ' a m o n g t h e g e n e s o n sex c h r o m o s o m e s s u g g e s t s t h a t the c o n c e p t o f the o u t l a w g e n e m a y be too simple. It c o n v e y s the i m a g e of a single rebel s t a n d i n g o u t a g a i n s t t h e rest o f t h e g e n o m e . A t t i m e s w e m i g h t , i n s t e a d , d o b e t t e r t o t h i n k i n t e r m s o f w a r s b e t w e e n r i v a l g a n g s o f g e n e s , for i n s t a n c e the X - c h r o m o s o m e g e n e s a g a i n s t t h e rest. C o s m i d e s a n d T o o b y ( 1 9 8 1 ) c o i n the useful t e r m ' c o r e p l i c o n ' for s u c h a g a n g o f g e n e s t h a t r e p l i c a t e t o g e t h e r a n d therefore tend
t o w o r k for t h e s a m e e n d s .
I n m a n y cases n e i g h b o u r i n g
coreplicons will blur into each other. G a n g i n g up by Y - c h r o m o s o m e genes is even more to be expected. As long as Y c h r o m o s o m e s do n o t cross o v e r , it is c l e a r t h a t all g e n e s on a Y c h r o m o s o m e s t a n d t o g a i n from t h e p r e s e n c e o f a Y - l i n k e d d i s t o r t e r e v e r y bit a s m u c h a s t h e d i s t o r t e r g e n e itself. H a m i l t o n ( 1 9 6 7 ) m a d e t h e i n t e r e s t i n g s u g g e s t i o n t h a t t h e r e a s o n for t h e w e l l - k n o w n i n e r t n e s s o f Y c h r o m o s o m e s (hairy ears seems to be the o n l y c o n s p i c u o u s Y - l i n k e d trait in m a n ) is that Ys u p p r e s s i n g m o d i f i e r s h a v e b e e n p o s i t i v e l y s e l e c t e d e l s e w h e r e i n the g e n o m e . I t i s n o t o b v i o u s h o w a m o d i f i e r m i g h t g o a b o u t s u p p r e s s i n g the p h e n o t y p i c a c t i v i t y o f a n e n t i r e c h r o m o s o m e , s i n c e t h e v a r i o u s p h e n o t y p i c effects o f a single c h r o m o s o m e are usually so heterogeneous. ( W h y w o u l d selection not s u p p r e s s o n l y t h e effects o f t h e d r i v i n g g e n e s , l e a v i n g o t h e r Y - l i n k e d effects intact?) I suppose it m i g h t do it by p h y s i c a l l y d e l e t i n g large chunks of Y c h r o m o s o m e , o r b y c o n t r i v i n g t o q u a r a n t i n e t h e Y c h r o m o s o m e from the cell's transcription machinery. A w e i r d e x a m p l e of a d r i v i n g r e p l i c a t o r w h i c h is p r o b a b l y n o t a g e n e in t h e o r d i n a r y sense o f t h e w o r d i s g i v e n b y W e r r e n , S k i n n e r a n d C h a r n o v (in p r e p a r a t i o n ) . T h e y s t u d i e d t h e p a r a s i t o i d w a s p Nasonia vitripennis, i n w h i c h there
is
a
variety
of males
called
Dl,
or
'daughterless'.
Wasps
being
h a p l o d i p l o i d , m a l e s pass t h e i r g e n e s o n l y t o d a u g h t e r s : a m a l e ' s m a t e m a y h a v e sons, b u t t h o s e sons a r e h a p l o i d a n d fatherless. W h e n D l m a l e s m a t e w i t h f e m a l e s , t h e y c a u s e t h e m t o p r o d u c e all m a l e b r o o d s . M o s t o f t h e sons o f females m a t e d to Dl males are themselves Dl males. A l t h o u g h no nuclear g e n e s pass from f a t h e r t o s o n , t h e r e f o r e , t h e D l f a c t o r s o m e h o w d o e s pass
O u t l a w s and Modifiers
141
f r o m father t o 'son'. T h e D l factor r a p i d l y spreads, i n e x a c t l y the s a m e w a y as a driving Y c h r o m o s o m e w o u l d .
It is not k n o w n w h a t the Dl factor
p h y s i c a l l y consists of. I t i s c e r t a i n l y n o t n u c l e a r g e n e t i c m a t e r i a l , a n d i t i s theoretically possible that it is not e v e n c o m p o s e d of nucleic acid, a l t h o u g h W e r r e n e t al. s u s p e c t t h a t i t p r o b a b l y i s c y t o p l a s m i c a l l y b o r n e n u c l e i c a c i d . T h e o r e t i c a l l y , any k i n d o f p h y s i c a l o r c h e m i c a l i n f l u e n c e o f a D l m a l e o n his m a t e , w h i c h c a u s e s h e r t o h a v e D l sons, w o u l d s p r e a d l i k e a d r i v i n g Y c h r o m o s o m e , a n d w o u l d q u a l i f y a s a n a c t i v e g e r m - l i n e r e p l i c a t o r i n t h e sense of C h a p t e r 5. It is a l s o an o u t l a w par excellence, for it s p r e a d s i t s e l f at t h e t o t a l e x p e n s e o f a l l t h e n u c l e a r g e n e s i n t h e m a l e s t h a t b e a r it.
Selfish sperm W i t h some e x c e p t i o n s , all the d i p l o i d cells of an o r g a n i s m are g e n e t i c a l l y i d e n t i c a l , b u t the h a p l o i d g a m e t e s i t p r o d u c e s a r e a l l d i f f e r e n t . O n l y o n e o u t of m a n y sperms in an ejaculate c a n fertilize an e g g , a n d there is therefore potential
for c o m p e t i t i o n a m o n g t h e m .
A n y gene that found
phenotypic
e x p r e s s i o n w h e n i n the h a p l o i d s t a t e i n a s p e r m c e l l c o u l d b e f a v o u r e d o v e r its alleles i f i t i m p r o v e d the c o m p e t i t i v e a b i l i t y o f t h e s p e r m . S u c h a g e n e w o u l d not necessarily be sex-linked: it could be found on any c h r o m o s o m e . I f i t w a s s e x - l i n k e d i t w o u l d h a v e t h e effect o f b i a s i n g t h e s e x r a t i o , a n d w o u l d b e a n o u t l a w . I f i t w a s o n a n a u t o s o m e i t w o u l d still q u a l i f y a s a n o u t l a w for t h e g e n e r a l k i n d o f r e a s o n a l r e a d y g i v e n for a n y s e g r e g a t i o n distorter: ' . . . if there were genes affecting sperm-cell function there w o u l d be competition a m o n g sperm cells, a n d a g e n e that i m p r o v e d the ability to fertilize w o u l d i n c r e a s e i n t h e p o p u l a t i o n . I f s u c h a g e n e h a p p e n e d t o c a u s e , say, m a l f u n c t i o n o f the liver, that w o u l d b e j u s t too b a d ; the g e n e w o u l d i n c r e a s e a n y w a y , s i n c e s e l e c t i o n for g o o d h e a l t h i s m u c h less e f f e c t i v e t h a n selection by c o m p e t i t i o n a m o n g sperm cells'
(Crow
1 9 7 9 ) . T h e r e is, o f
course, no particular reason w h y a sperm competition g e n e should h a p p e n to cause malfunction of the liver but, as a l r e a d y p o i n t e d out, most m u t a t i o n s are d e l e t e r i o u s , s o s o m e u n d e s i r a b l e side effect i s p r e t t y l i k e l y . W h y d o e s C r o w assert t h a t s e l e c t i o n for g o o d h e a l t h i s m u c h less e f f e c t i v e than selection by competition a m o n g sperm cells? T h e r e must inevitably be a q u a n t i t a t i v e t r a d e - o f f i n v o l v i n g the m a g n i t u d e o f t h e effect o n h e a l t h . B u t , t h a t a s i d e , a n d e v e n a l l o w i n g for t h e c o n t r o v e r s i a l p o s s i b i l i t y t h a t o n l y a minority of sperms are v i a b l e ( C o h e n 1 9 7 7 ) , the a r g u m e n t a p p e a r s to h a v e force b e c a u s e t h e c o m p e t i t i o n b e t w e e n s p e r m c e l l s i n a n e j a c u l a t e w o u l d s e e m to be so f i e r c e .
A million million spermatozoa, All of them alive: O u t of their c a t a c l y s m but one poor N o a h Dare hope to survive.
142
O u t l a w s and M o d i f i e r s
A n d of that billion minus one Might have chanced to be Shakespeare, another Newton, a new D o n n e — But the O n e w a s M e . S h a m e to h a v e ousted y o u r betters thus. T a k i n g ark while the others remained outside! B e t t e r for a l l o f us, f r o w a r d H o m u n c u l u s , If you'd quietly died! Aldous
Huxley
O n e m i g h t i m a g i n e t h a t a m u t a n t g e n e t h a t e x p r e s s e d itself w h e n i n the haploid g e n o t y p e of a spermatozoon, causing increased competitive ability, s a y a n i m p r o v e d s w i m m i n g t a i l o r t h e s e c r e t i o n o f a s p e r m i c i d e t o w h i c h the sperm itself w a s i m m u n e , w o u l d be i m m e d i a t e l y favoured by a selection pressure
gigantic
enough
to
outweigh
all
but
the
most
catastrophic
of
d e l e t e r i o u s s i d e effects o n the d i p l o i d b o d y . B u t a l t h o u g h i t m a y b e t r u e t h a t only one in
hundreds of millions of sperms
'dare hope to survive',
the
c a l c u l a t i o n l o o k s v e r y different f r o m t h e p o i n t o f v i e w o f a s i n g l e g e n e . I f w e f o r g e t l i n k a g e g r o u p s a n d b r a n d - n e w m u t a t i o n s for a m o m e n t , h o w e v e r r a r e a g e n e m a y b e i n t h e g e n e - p o o l , i f a g i v e n m a l e h a s i t i n his d i p l o i d g e n o t y p e , a t least 5 0 p e r c e n t o f his s p e r m s m u s t h a v e it. I f o n e s p e r m h a s r e c e i v e d a g e n e g i v i n g i t c o m p e t i t i v e a d v a n t a g e , 5 0 p e r c e n t o f its r i v a l s i n t h e s a m e e j a c u l a t e w i l l h a v e r e c e i v e d t h e s a m e g e n e . O n l y i f t h e m u t a t i o n h a s arisen d e novo d u r i n g astronomical
the genesis of a single sperm will in
magnitude.
the selection pressure be
U s u a l l y it will be a m o r e modest selection
p r e s s u r e , n o t o f m i l l i o n s t o o n e b u t o n l y t w o t o o n e . I f w e t a k e l i n k a g e effects into c o n s i d e r a t i o n the c a l c u l a t i o n is m o r e c o m p l i c a t e d , and the selection pressure in favour of c o m p e t i t i v e sperms will increase s o m e w h a t . In a n y c a s e , it is a s t r o n g e n o u g h p r e s s u r e for us to e x p e c t t h a t , if g e n e s expressed themselves w h e n in the h a p l o i d g e n o t y p e of the sperm, outlaws w o u l d b e f a v o u r e d , t o t h e d e t r i m e n t o f t h e rest o f t h e g e n e s i n t h e d i p l o i d f a t h e r ' s g e n o m e . I t s e e m s , t o s a y t h e least, f o r t u n a t e t h a t s p e r m p h e n o t y p e s are, as a m a t t e r of fact, usually not u n d e r the control of their o w n haploid genotypes (Beatty & Gluecksohn-Waelsch types
must
be
under
some
genetic
1972). Of course sperm pheno-
control,
and
natural
selection
has
doubtless w o r k e d on the genes c o n t r o l l i n g sperm p h e n o t y p e s to perfect sperm a d a p t a t i o n . B u t t h o s e g e n e s s e e m t o e x p r e s s t h e m s e l v e s w h e n i n the d i p l o i d g e n o t y p e of the father, not w h e n in the h a p l o i d g e n o t y p e of the sperm. W h e n in the sperm they are passively carried. T h e p a s s i v i t y o f t h e i r g e n o t y p e s m a y b e a n i m m e d i a t e c o n s e q u e n c e o f the lack
of cytoplasm
in
spermatozoa:
a
gene
cannot
achieve
phenotypic
O u t l a w s and M o d i f i e r s
143
expression e x c e p t v i a c y t o p l a s m . T h i s is a p r o x i m a l e x p l a n a t i o n . B u t it is at least w o r t h t o y i n g w i t h r e v e r s i n g t h e p r o p o s i t i o n
to obtain an ultimate
functional e x p l a n a t i o n : sperms are m a d e small, as an a d a p t a t i o n to p r e v e n t the p h e n o t y p i c e x p r e s s i o n o f t h e h a p l o i d g e n o t y p e . O n this h y p o t h e s i s w e a r e proposing an arms race between competitive
ability
among
(haploid-expressed)
spermatozoa
on
the
g e n e s for i n c r e a s e d
one
hand,
and
genes
e x p r e s s i n g t h e m s e l v e s w h e n i n the d i p l o i d g e n o t y p e o f t h e f a t h e r o n t h e o t h e r hand,
causing sperms
to
b e c o m e smaller and
therefore
unable
to
give
phenotypic expression to their o w n haploid g e n o t y p e s . T h i s hypothesis does not e x p l a i n w h y eggs are larger than s p e r m s ; it assumes the basic fact of anisogamy, and therefore does not aspire to be an alternative to theories of the o r i g i n s o f a n i s o g a m y ( P a r k e r 1 9 7 8 b ; M a y n a r d S m i t h 1 9 7 8 a ; A l e x a n d e r & Borgia
1 9 7 9 ) . M o r e o v e r not all sperms are small, as S i v i n s k i
(1980)
r e m i n d s u s i n a m o s t i n t r i g u i n g r e v i e w . B u t t h e p r e s e n t e x p l a n a t i o n still deserves consideration as an ancillary to others. It is a n a l o g o u s to H a m i l t o n ' s ( 1 9 6 7 ) e x p l a n a t i o n for t h e i n e r t n e s s o f Y c h r o m o s o m e s , t o w h i c h I h a v e already alluded.
Green beards and armpits S o m e of the outlaws I h a v e been considering h a v e been realistic, a n d are a c t u a l l y k n o w n t o g e n e t i c i s t s . S o m e o f the s u g g e s t e d o u t l a w s t h a t I s h a l l n o w c o m e t o a r e , f r a n k l y , p r e t t y i m p r o b a b l e . I m a k e n o a p o l o g y for this. I see them as t h o u g h t e x p e r i m e n t s . T h e y p l a y the s a m e role in h e l p i n g me to think straight a b o u t reality as i m a g i n a r y trains t r a v e l l i n g at n e a r l y the speed of l i g h t d o for p h y s i c i s t s . So,
in
this
spirit
of t h o u g h t
experiment,
imagine
a
gene
on
a
Y
c h r o m o s o m e w h i c h m a k e s its possessor kill his d a u g h t e r s a n d f e e d t h e m t o his sons. T h i s i s c l e a r l y a b e h a v i o u r a l v e r s i o n o f a d r i v i n g Y - c h r o m o s o m e effect. I f i t a r o s e i t w o u l d t e n d t o s p r e a d for t h e s a m e r e a s o n , a n d i t w o u l d b e a n o u t l a w i n t h e s a m e sense t h a t its p h e n o t y p i c effect w o u l d b e d e t r i m e n t a l t o the rest o f t h e m a l e ' s g e n e s . M o d i f i e r s , o n a n y c h r o m o s o m e o t h e r t h a n t h e Y c h r o m o s o m e , w h i c h t e n d e d t o r e d u c e t h e p h e n o t y p i c effect o f t h e d a u g h t e r killing g e n e w o u l d be favoured over their alleles. In a sense the o u t l a w g e n e is u s i n g t h e sex of t h e m a l e ' s c h i l d r e n as a c o n v e n i e n t label for t h e p r e s e n c e or a b s e n c e o f itself: a l l sons a r e l a b e l l e d a s d e f i n i t e possessors o f t h e g e n e , a l l d a u g h t e r s a s d e f i n i t e n o n - p o s s e s s o r s o f it. A s i m i l a r a r g u m e n t c a n b e m a d e for X c h r o m o s o m e s . H a m i l t o n ( 1 9 7 2 , p . 201) p o i n t e d o u t t h a t i n n o r m a l d i p l o i d s p e c i e s a g e n e o n a n X c h r o m o s o m e i n the h o m o g a m e t i c sex h a s t h r e e - q u a r t e r s o f a c h a n c e o f b e i n g i d e n t i c a l b y descent with a g e n e in a sibling of the h o m o g a m e t i c sex. T h u s the ' X c h r o m o s o m e r e l a t e d n e s s ' o f h u m a n sisters i s a s h i g h a s t h e o v e r a l l r e l a t e d n e s s o f h y m e n o p t e r a n sisters, a n d h i g h e r t h a n t h e o v e r a l l r e l a t e d n e s s o f h u m a n sisters. H a m i l t o n w e n t s o far a s t o w o n d e r w h e t h e r a n X - c h r o m o s o m e effect
144
O u t l a w s and Modifiers
m i g h t a c c o u n t for t h e f a c t t h a t h e l p e r s a t the nest i n b i r d s s e e m , u s u a l l y , t o be elder brothers,
r a t h e r t h a n sisters,
o f the n e s t l i n g s
(the m a l e sex i s
h o m o g a m e t i c in birds). He noted that the X c h r o m o s o m e in birds accounts for s o m e 1 0 p e r c e n t o f t h e w h o l e g e n o m e , a n d t h a t i t i s t h e r e f o r e n o t too i m p r o b a b l e t h a t t h e g e n e t i c basis for b r o t h e r l y c a r e m i g h t lie o n t h e X c h r o m o s o m e . I f so, b r o t h e r l y c a r e m i g h t b e f a v o u r e d b y t h e s a m e k i n d o f s e l e c t i o n p r e s s u r e a s H a m i l t o n h a d e a r l i e r s u g g e s t e d for sisterly c a r e i n H y m e n o p t e r a . Perhaps significantly, S y r e n and L u y c k x (1977) point out t h a t i n s o m e t e r m i t e s , t h e o n l y n o n - h a p l o d i p l o i d g r o u p t o h a v e a c h i e v e d full eusociality, ' a p p r o x i m a t e l y h a l f the g e n o m e is m a i n t a i n e d as a linkage g r o u p w i t h t h e sex c h r o m o s o m e ' ( L a c y 1 9 8 0 ) . Wickler
(1977),
commenting
on
Hamilton's X - c h r o m o s o m e idea, potentially
even
more
Whitney's
(1976)
rediscovery
of
s u g g e s t s t h a t Y - c h r o m o s o m e effects are
powerful
than
X-chromosome
effects,
but
Y
c h r o m o s o m e s a s a r u l e d o n ' t m a k e u p s u c h a h i g h p r o p o r t i o n o f the g e n o m e . I n a n y c a s e ' s e x - l i n k e d a l t r u i s m ' m u s t b e discriminating: i n d i v i d u a l s a c t i n g under
the
influence
of
their
sex
chromosomes
should
tend
to
show
f a v o u r i t i s m t o w a r d s c l o s e r e l a t i v e s o f t h e s a m e sex r a t h e r t h a n o f the o p p o s i t e s e x . G e n e s for s e x - b l i n d s i b l i n g c a r e w o u l d n o t b e o u t l a w s . T h e v a l u e o f the o u t l a w e d s e x - c h r o m o s o m e t h o u g h t e x p e r i m e n t does not lie i n its p l a u s i b i l i t y — w h i c h , l i k e H a m i l t o n , I d o n o t r a t e h i g h l y — b u t i n the fact t h a t i t f o c u s e s o u r a t t e n t i o n o n t h e i m p o r t a n c e o f this d i s c r i m i n a t i o n . T h e sex of a n o t h e r i n d i v i d u a l is u s e d as a label to i d e n t i f y it as a m e m b e r of a class
of individuals
ordinary
theory
about
of kin
whose genetics
selection,
something
relatedness
(or
is
known.
rather some
In
the
proximate
c o r r e l a t e o f r e l a t e d n e s s s u c h a s p r e s e n c e i n o n e ' s o w n nest) i s used a s a l a b e l i n d i c a t i n g h i g h e r t h a n a v e r a g e p r o b a b i l i t y o f s h a r i n g a g e n e . F r o m the p o i n t of v i e w of a g e n e on a Y c h r o m o s o m e , t h e sex of a s i b l i n g is a l a b e l w h i c h signifies t h e d i f f e r e n c e b e t w e e n c e r t a i n t y o f s h a r i n g t h e g e n e a n d c e r t a i n t y o f n o t s h a r i n g it. N o t e , by the w a y , the ineptness of notions of individual fitness, or even i n c l u s i v e f i t n e s s a s o r d i n a r i l y u n d e r s t o o d , a t d e a l i n g w i t h s i t u a t i o n s like this. T h e n o r m a l c a l c u l a t i o n o f i n c l u s i v e f i t n e s s m a k e s use o f a c o e f f i c i e n t o f relationship w h i c h is s o m e m e a s u r e of the p r o b a b i l i t y that a pair of relatives will
share
a
approximation
particular provided
gene, the
identical
genes
by
concerned
descent. have
This no
is
better
a
good
way
of
' r e c o g n i z i n g ' c o p i e s o f t h e m s e l v e s i n o t h e r i n d i v i d u a l s . I f a g e n e i s o n a sex c h r o m o s o m e a n d c a n u s e t h e sex o f r e l a t i v e s a s a l a b e l , h o w e v e r , its best ' e s t i m a t e ' of the p r o b a b i l i t y that a relative shares a c o p y of itself will be a b e t t e r e s t i m a t e t h a n t h a t p r o v i d e d b y t h e c o e f f i c i e n t o f r e l a t i o n s h i p . I n its most general form, the principle of genes a p p e a r i n g to 'recognize' copies of t h e m s e l v e s i n o t h e r i n d i v i d u a l s h a s b e e n d u b b e d t h e ' g r e e n - b e a r d effect' ( D a w k i n s 1976a, p. 96, following H a m i l t o n 1964b, p. 25). G r e e n - b e a r d or
O u t l a w s and M o d i f i e r s
'recognition
alleles'
have
been
described
in
the
literature
as
145
outlaws
( A l e x a n d e r & B o r g i a 1 9 7 8 ; A l e x a n d e r 1980), a n d they should therefore be discussed i n this c h a p t e r , e v e n t h o u g h , a s w e s h a l l s e e , t h e i r s t a t u s a s o u t l a w s needs careful e x a m i n a t i o n ( R i d l e y & G r a f e n in press). T h e g r e e n - b e a r d effect r e d u c e s t h e p r i n c i p l e o f ' g e n e s e l f - r e c o g n i t i o n ' t o its b a r e essentials i n a n u n r e a l i s t i c a l l y h y p o t h e t i c a l , b u t n e v e r t h e l e s s i n s t r u c t i v e , w a y . A g e n e i s p o s t u l a t e d w h i c h h a s t w o p l e i o t r o p i c effects. O n e effect i s t o c o n f e r a c o n s p i c u o u s l a b e l , t h e ' g r e e n b e a r d ' . T h e o t h e r effect i s t o c o n f e r a tendency to b e h a v e altruistically t o w a r d s bearers of the l a b e l . S u c h a g e n e , if it ever arose, could easily be favoured by natural selection, a l t h o u g h it w o u l d be vulnerable to a m u t a n t arising w h i c h conferred the label w i t h o u t the altruism. G e n e s a r e n o t c o n s c i o u s little d e v i l s , a b l e t o r e c o g n i z e c o p i e s o f t h e m s e l v e s i n o t h e r i n d i v i d u a l s a n d t o a c t a c c o r d i n g l y . T h e o n l y w a y for t h e g r e e n b e a r d effect t o arise i s b y i n c i d e n t a l p l e i o t r o p y . A m u t a t i o n m u s t a r i s e w h i c h j u s t h a p p e n s t o h a v e t w o c o m p l e m e n t a r y effects: t h e l a b e l o r ' g r e e n b e a r d ' , a n d the t e n d e n c y t o b e h a v e a l t r u i s t i c a l l y t o w a r d s l a b e l l e d i n d i v i d u a l s . I h a v e a l w a y s t h o u g h t s u c h a f o r t u i t o u s c o n j u n c t i o n o f p l e i o t r o p i c effects t o o g o o d to be true. H a m i l t o n also noted the idea's i n h e r e n t i m p l a u s i b i l i t y , b u t h e w e n t o n ' . . . e x a c t l y t h e s a m e a priori o b j e c t i o n s m i g h t b e m a d e t o t h e evolution of assortative m a t i n g w h i c h manifestly has e v o l v e d , p r o b a b l y m a n y t i m e s i n d e p e n d e n t l y a n d d e s p i t e its o b s c u r e a d v a n t a g e s ' ( H a m i l t o n 1 9 6 4 b , p . 2 5 ) . I t i s w o r t h b r i e f l y e x a m i n i n g this c o m p a r i s o n w i t h a s s o r t a t i v e m a t i n g , w h i c h for p r e s e n t p u r p o s e s I s h a l l t a k e t o m e a n t h e t e n d e n c y o f i n d i v i d u a l s t o prefer t o m a t e w i t h i n d i v i d u a l s t h a t g e n e t i c a l l y r e s e m b l e t h e m . W h y i s i t t h a t t h e g r e e n - b e a r d effect s e e m s s o m u c h m o r e f a r - f e t c h e d t h a n assortative m a t i n g ? It is not just that assortative m a t i n g is positively k n o w n to occur. I suggest another reason. T h i s is that w h e n we think of assortative m a t i n g w e i m p l i c i t l y a s s u m e self-inspection a s a m e a n s o f f a c i l i t a t i n g t h e effect. If black individuals prefer to m a t e with b l a c k individuals, and w h i t e w i t h w h i t e , w e d o n o t find this h a r d t o b e l i e v e b e c a u s e w e t a c i t l y a s s u m e t h a t i n d i v i d u a l s p e r c e i v e t h e i r own c o l o u r . E a c h i n d i v i d u a l , w h a t e v e r his c o l o u r , i s a s s u m e d t o b e o b e y i n g t h e same r u l e : i n s p e c t y o u r s e l f (or m e m b e r s o f y o u r o w n family) and choose a m a t e of the same colour. T h i s p r i n c i p l e does not stretch our credulity by d e m a n d i n g that t w o specific effects—colour a n d behavioural preference—are controlled pleiotropically by the s a m e gene. If there
is
a
general
advantage
in
mating
with
similar
partners,
natural
selection will favour the self-inspection rule regardless of the e x a c t n a t u r e of the r e c o g n i t i o n c h a r a c t e r u s e d . I t d o e s n o t h a v e t o b e s k i n c o l o u r . A n y conspicuous
and
variable
character
would
work
with
the
identical
behavioural rule. No far-fetched pleiotropism need be postulated. W e l l t h e n , w i l l t h e s a m e k i n d o f m e c h a n i s m w o r k for t h e g r e e n - b e a r d effect? M i g h t a n i m a l s o b e y a b e h a v i o u r a l r u l e o f t h e f o r m : ' I n s p e c t y o u r s e l f
146
O u t l a w s and Modifiers
and b e h a v e altruistically towards other individuals that resemble y o u ' ? T h e a n s w e r i s t h a t t h e y m i g h t , b u t this w o u l d n o t b e a t r u e e x a m p l e o f t h e g r e e n beard
effect.
Instead,
I
call
it
the
'armpit
effect'.
In
the
paradigm
h y p o t h e t i c a l e x a m p l e , t h e a n i m a l i s s u p p o s e d t o s m e l l its o w n a r m p i t s , a n d b e h a v e altruistically towards other individuals with a similar smell.
(The
r e a s o n for c h o o s i n g a n o l f a c t o r y n a m e i s t h a t p o l i c e d o g trials h a v e s h o w n that
dogs
presented
with
handkerchiefs
held
under
human
armpits can
distinguish the sweats of a n y t w o i n d i v i d u a l h u m a n s e x c e p t identical twins ( K a l m u s 1 9 5 5 ) . T h i s suggests that there is an e n o r m o u s l y v a r i a b l e richness of g e n e t i c l a b e l l i n g i n m o l e c u l e s o f s w e a t . I n t h e l i g h t o f t h e result w i t h i d e n t i c a l t w i n s , o n e feels i n c l i n e d t o b e t t h a t p o l i c e d o g s c o u l d b e t r a i n e d t o sniff o u t t h e c o e f f i c i e n t o f r e l a t i o n s h i p b e t w e e n p a i r s o f h u m a n s a n d t h a t , for i n s t a n c e , t h e y c o u l d b e t r a i n e d t o t r a c k d o w n a c r i m i n a l i f g i v e n a sniff o f his b r o t h e r . B e t h a t a s i t m a y , ' a r m p i t effect' i s h e r e b e i n g used a s a g e n e r a l n a m e for a n y case
of an
animal
inspecting
himself,
or
a
known
close
relative,
and
discriminating in favour of other individuals with a similar smell or with some other perceived similarity.) T h e e s s e n t i a l d i f f e r e n c e b e t w e e n t h e g r e e n - b e a r d effect a n d t h e a r m p i t s e l f - i n s p e c t i o n effect i s a s f o l l o w s . T h e a r m p i t s e l f - i n s p e c t i o n b e h a v i o u r a l r u l e will lead
to the detection of other individuals that are similar in some
r e s p e c t , p e r h a p s i n m a n y r e s p e c t s , b u t i t w i l l n o t s p e c i f i c a l l y l e a d t o the detection
of individuals
that
possess
copies
of the
gene
mediating
the
b e h a v i o u r a l r u l e itself. T h e a r m p i t r u l e m i g h t p r o v i d e a n a d m i r a b l e m e a n s o f d e t e c t i n g t r u e k i n f r o m n o n - k i n , o r o f d e t e c t i n g w h e t h e r a b r o t h e r w a s a full brother or only a half brother. T h i s could be very important, and it might p r o v i d e t h e basis for s e l e c t i o n i n f a v o u r o f s e l f - i n s p e c t i n g b e h a v i o u r , b u t the selection w o u l d b e c o n v e n t i o n a l , familiar kin selection. T h e self-inspection rule w o u l d be functioning simply as a kin-recognition d e v i c e , a n a l o g o u s to a rule like: ' B e h a v e altruistically towards individuals that g r e w up in y o u r o w n nest.' T h e g r e e n - b e a r d effect i s q u i t e d i f f e r e n t . H e r e t h e i m p o r t a n t t h i n g i s t h a t a g e n e (or c l o s e l i n k a g e g r o u p ) p r o g r a m s t h e r e c o g n i t i o n s p e c i f i c a l l y o f c o p i e s o f itself. T h e g r e e n - b e a r d effect i s n o t a m e c h a n i s m for t h e r e c o g n i t i o n o f k i n . R a t h e r , kin recognition and ' g r e e n - b e a r d ' recognition are alternative w a y s in w h i c h genes could b e h a v e as if discriminating in favour of copies of themselves. T o r e t u r n t o H a m i l t o n ' s c o m p a r i s o n w i t h a s s o r t a t i v e m a t i n g , w e c a n see that
it
does
not
really
provide
good
grounds
for
optimism
over
the
p l a u s i b i l i t y o f t h e g r e e n - b e a r d effect. A s s o r t a t i v e m a t i n g i s m u c h m o r e l i k e l y to i n v o l v e s e l f - i n s p e c t i o n . If, for w h a t e v e r r e a s o n , it is an a d v a n t a g e in g e n e r a l for l i k e t o m a t e w i t h l i k e , s e l e c t i o n w o u l d f a v o u r a n a r m p i t t y p e o f b e h a v i o u r a l r u l e : Inspect yourself, a n d choose a m a t e that resembles y o u . T h i s will a c h i e v e the desired result—an optimal b a l a n c e between outbreed-
O u t l a w s and M o d i f i e r s
147
ing and inbreeding (Bateson 1978a) or w h a t e v e r the a d v a n t a g e m a y b e — r e g a r d l e s s o f the e x a c t n a t u r e o f t h e c h a r a c t e r i s t i c s b y w h i c h i n d i v i d u a l s differ. Assortative m a t i n g is not the o n l y a n a l o g y H a m i l t o n m i g h t h a v e chosen. A n o t h e r o n e i s t h e c a s e o f c r y p t i c m o t h s c h o o s i n g t o sit o n a b a c k g r o u n d t h a t m a t c h e s t h e i r o w n c o l o u r . K e t t l e w e l l ( 1 9 5 5 ) g a v e d a r k - c o l o u r e d carbonaria a n d l i g h t - c o l o u r e d t y p i c a l m o r p h s o f t h e p e p p e r e d m o t h Biston betularia t h e o p p o r t u n i t y t o sit o n d a r k - o r l i g h t - c o l o u r e d b a c k g r o u n d s . T h e r e w a s a s t a t i s t i c a l l y s i g n i f i c a n t t e n d e n c y for m o t h s t o c h o o s e a b a c k g r o u n d m a t c h i n g t h e i r o w n b o d y c o l o u r . T h i s c o u l d b e d u e t o p l e i o t r o p i s m (or g e n e s for c o l o u r b e i n g c l o s e l y l i n k e d t o g e n e s for b a c k g r o u n d c h o i c e ) . I f this w e r e so, a s Sargent (1969a) believes, it might, by analogy, reduce our scepticism about the
inherent
plausibility of the
green-beard
effect.
Kettlewell
believed,
h o w e v e r , that the moths a c h i e v e d the m a t c h i n g b y the simpler m e c h a n i s m o f ' c o n t r a s t c o n f l i c t ' . H e s u g g e s t e d t h a t a m o t h c o u l d see a s m a l l p o r t i o n o f its o w n b o d y , a n d t h a t i t m o v e d a r o u n d u n t i l t h e o b s e r v e d c o n t r a s t b e t w e e n its o w n b o d y and the b a c k g r o u n d r e a c h e d a m i n i m u m . It is easy to b e l i e v e that natural
selection
minimizing
might
favour
behavioural
rule,
the
genetic
because
it
basis
would
for
such
work
a
contrast-
automatically
conjunction with any colour, including a newly mutated colour.
in
It is of
c o u r s e a n a l o g o u s t o t h e ' a r m p i t s e l f - i n s p e c t i o n ' effect, a n d i s p l a u s i b l e for t h e same reason. S a r g e n t ' s ( 1 9 6 9 a ) i n t u i t i o n differs f r o m K e t t l e w e l l ' s . H e d o u b t s t h e selfinspection
theory,
and
thinks
that
the
two
morphs
of B.
betularia differ
genetically in their b a c k g r o u n d preference. He has no e v i d e n c e a b o u t B. betularia itself, b u t h a s d o n e s o m e i n g e n i o u s e x p e r i m e n t s o n o t h e r s p e c i e s . F o r e x a m p l e , he took m e m b e r s of a d a r k species and of a light species, and painted
the
c i r c u m - o c u l a r hairs
in an
attempt
to
'fool'
the moths into
choosing a b a c k g r o u n d that m a t c h e d the p a i n t e d hairs. T h e y obstinately persisted
in
choosing
a
background
that
matched
their
genetically
d e t e r m i n e d c o l o u r ( S a r g e n t 1 9 6 8 ) . U n f o r t u n a t e l y , h o w e v e r , this i n t e r e s t i n g result w a s o b t a i n e d
w i t h t w o different species,
not with dark and
light
morphs of one species. I n a n o t h e r e x p e r i m e n t w h i c h w a s d o n e w i t h a d i m o r p h i c s p e c i e s , Phigalia titea, S a r g e n t ( 1 9 6 9 a ) s i m p l y failed t o g e t t h e r e s u l t K e t t l e w e l l h a d w i t h B . betularia. T h e P . titea i n d i v i d u a l s , w h e t h e r t h e d a r k o r t h e l i g h t m o r p h , c h o s e t o sit o n l i g h t b a c k g r o u n d s , p r e s u m a b l y t h e a p p r o p r i a t e b a c k g r o u n d for t h e l i g h t a n c e s t r a l f o r m o f t h e s p e c i e s . W h a t i s n e e d e d i s for s o m e b o d y t o r e p e a t S a r g e n t ' s k e y e x p e r i m e n t o f p a i n t i n g the p a r t s o f a m o t h ' s b o d y t h a t i t c a n see, b u t u s i n g a d i m o r p h i c s p e c i e s like B. betularia w h i c h is k n o w n to s h o w morph-specific b a c k g r o u n d choice. K e t t l e w e l l ' s theory w o u l d predict that moths p a i n t e d b l a c k will select b l a c k b a c k g r o u n d s , a n d m o t h s p a i n t e d light will select light b a c k g r o u n d s , regardless of w h e t h e r t h e y are g e n e t i c a l l y
148
O u t l a w s and M o d i f i e r s
carbonaria or typica. A p u r e l y g e n e t i c t h e o r y w o u l d p r e d i c t t h a t carbonaria w i l l c h o o s e d a r k b a c k g r o u n d s a n d typica l i g h t b a c k g r o u n d s ,
regardless of h o w
they are painted. I f t h e l a t t e r t h e o r y t u r n e d o u t t o b e r i g h t , w o u l d this result g i v e a i d a n d c o m f o r t t o t h e g r e e n - b e a r d t h e o r y ? A little, p e r h a p s , s i n c e i t w o u l d s u g g e s t that a m o r p h o l o g i c a l character and behavioural recognition of something resembling that morphological character can be, or can rapidly become, closely linked g e n e t i c a l l y . It must be r e m e m b e r e d , here, that in the m o t h crypsis e x a m p l e there is no suggestion that we are dealing with an outlaw effect.
If there
are
two
genes,
one
controlling
colour
and
the
other
b a c k g r o u n d c h o i c e b e h a v i o u r , b o t h s t a n d t o g a i n f r o m t h e p r e s e n c e o f the a p p r o p r i a t e o t h e r o n e , a n d n e i t h e r o f t h e t w o i s i n a n y sense a n o u t l a w . I f the t w o genes started out distantly linked, selection w o u l d favour closer and c l o s e r l i n k a g e . I t i s n o t c l e a r t h a t s e l e c t i o n w o u l d s i m i l a r l y f a v o u r t h e close l i n k a g e o f a ' g r e e n - b e a r d g e n e ' a n d a g e n e for g r e e n - b e a r d r e c o g n i t i o n . I t s e e m s t h a t t h e a s s o c i a t i o n b e t w e e n t h e effects w o u l d h a v e t o b e t h e r e b y l u c k r i g h t f r o m t h e start. T h e g r e e n - b e a r d effect i s a l l a b o u t o n e selfish g e n e l o o k i n g after c o p i e s o f i t s e l f i n o t h e r i n d i v i d u a l s , r e g a r d l e s s of, i n d e e d i n spite of, the p r o b a b i l i t y that those i n d i v i d u a l s will share genes in g e n e r a l . T h e g r e e n - b e a r d g e n e ' s p o t s ' c o p i e s o f itself, a n d i t t h e r e b y s e e m s t o w o r k a g a i n s t the interests o f the rest o f t h e g e n o m e . I t a p p e a r s t o b e a n o u t l a w i n t h e sense t h a t i t m a k e s i n d i v i d u a l s w o r k a n d p a y costs, for t h e b e n e f i t o f o t h e r i n d i v i d u a l s w h o a r e n o t p a r t i c u l a r l y l i k e l y t o s h a r e g e n e s o t h e r t h a n t h e o u t l a w itself. T h i s i s the r e a s o n A l e x a n d e r a n d B o r g i a ( 1 9 7 8 ) c a l l i t a n o u t l a w , a n d i t i s o n e o f the r e a s o n s for t h e i r s c e p t i c i s m a b o u t t h e e x i s t e n c e o f g r e e n - b e a r d g e n e s . But it is actually not obvious that green-beard genes w o u l d , if they ever arose, be outlaws. T h e following caution is urged by R i d l e y and Grafen (in p r e s s ) . O u r d e f i n i t i o n o f a n o u t l a w m a k e s r e f e r e n c e t o its p r o v o k i n g o f m o d i f i e r s a t o t h e r l o c i w h i c h t e n d t o s u p p r e s s its p h e n o t y p i c effects. A t first sight it seems clear that g r e e n - b e a r d genes w o u l d indeed p r o v o k e suppressing modifiers, b e c a u s e the modifiers w o u l d not tend to h a v e copies in the bodies of the
(unrelated)
g r e e n - b e a r d e d i n d i v i d u a l s c a r e d for.
But we must not
f o r g e t t h a t a m o d i f i e r , i f i t i s t o h a v e a n y effect o n t h e p h e n o t y p i c e x p r e s s i o n of a g r e e n - b e a r d g e n e , is l i k e l y itself to be in a g r e e n - b e a r d e d b o d y , a n d is t h e r e f o r e in a p o s i t i o n to b e n e f i t f r o m receiving a l t r u i s m f r o m o t h e r g r e e n b e a r d e d i n d i v i d u a l s . M o r e o v e r , s i n c e those o t h e r g r e e n - b e a r d e d d o n o r s a r e n o t p a r t i c u l a r l y l i k e l y t o b e r e l a t i v e s , t h e costs o f t h e i r a l t r u i s m w i l l not b e felt b y c o p i e s o f t h e w o u l d - b e m o d i f i e r s . A c a s e c o u l d t h e r e f o r e b e m a d e t h a t w o u l d - b e m o d i f i e r s a t o t h e r l o c i w i l l g a i n r a t h e r t h a n lose f r o m s h a r i n g a b o d y w i t h a g r e e n - b e a r d g e n e . T o this i t c a n n o t b e o b j e c t e d t h a t t h e costs o f p a y i n g o u t a l t r u i s m t o o t h e r g r e e n - b e a r d e d i n d i v i d u a l s m a y o u t w e i g h the b e n e f i t s o f r e c e i v i n g a l t r u i s m f r o m o t h e r g r e e n - b e a r d e d i n d i v i d u a l s : i f this
O u t l a w s and Modifiers
149
w e r e true there w o u l d be no question of the g r e e n - b e a r d g e n e s p r e a d i n g in the first p l a c e . T h e e s s e n c e o f R i d l e y a n d G r a f e n ' s p o i n t i s t h a t i f ( w h i c h i s unlikely)
the g r e e n - b e a r d g e n e has w h a t it takes to spread
through the
p o p u l a t i o n a t all, t h e costs a n d b e n e f i t s o f t h e s i t u a t i o n w i l l b e s u c h a s t o f a v o u r m o d i f i e r s t h a t e n h a n c e r a t h e r t h a n r e d u c e t h e effect. I n e v a l u a t i n g this p o i n t , e v e r y t h i n g d e p e n d s o n t h e e x a c t n a t u r e o f w h a t w e are c a l l i n g the g r e e n - b e a r d p h e n o t y p e .
If the entire p l e i o t r o p i c d u a l
p h e n o t y p e — g r e e n beard plus altruism towards g r e e n - b e a r d e d i n d i v i d u a l s — is regarded as a p a c k a g e deal, w h i c h modifiers c a n suppress or e n h a n c e only as a unit, then R i d l e y and G r a f e n are surely right that g r e e n - b e a r d genes are n o t o u t l a w s . B u t , o f c o u r s e , a s t h e y t h e m s e l v e s stress, a m o d i f i e r t h a t c o u l d d e t a c h t h e t w o p h e n o t y p i c effects f r o m e a c h o t h e r , s u p p r e s s i n g t h e a l t r u i s t i c p h e n o t y p e of the g r e e n - b e a r d g e n e w h i l e not suppressing the g r e e n b e a r d itself w o u l d c e r t a i n l y b e f a v o u r e d . A t h i r d p o s s i b i l i t y i s t h e s p e c i a l c a s e o f a green-beard g e n e that caused parents to discriminate in f a v o u r of those of their c h i l d r e n that h a p p e n e d to share the r e c o g n i t i o n c h a r a c t e r . S u c h a g e n e w o u l d be analogous to a meiotic-drive gene, a n d w o u l d be a true o u t l a w . W h a t e v e r w e m a y feel a b o u t R i d l e y a n d G r a f e n ' s p o i n t a b o u t t h e g r e e n b e a r d effect, i t i s c l e a r t h a t g e n e s m e d i a t i n g a l t r u i s m t o w a r d s c l o s e k i n , a n d favoured by c o n v e n t i o n a l kin-selection pressure, are definitely not o u t l a w s . A l l the g e n e s i n t h e g e n o m e h a v e t h e s a m e s t a t i s t i c a l o d d s o f g a i n i n g f r o m t h e kin a l t r u i s m b e h a v i o u r , for a l l h a v e t h e s a m e s t a t i s t i c a l o d d s o f b e i n g p o s s e s s e d b y t h e i n d i v i d u a l b e n e f i t e d . A ' k i n - s e l e c t i o n g e n e ' is, i n a s e n s e , w o r k i n g for itself a l o n e , b u t i t b e n e f i t s t h e o t h e r g e n e s i n its g e n o m e a s w e l l . T h e r e w i l l t h e r e f o r e n o t b e s e l e c t i o n i n f a v o u r o f m o d i f i e r s t h a t s u p p r e s s it. A r m p i t selfinspection genes w o u l d be a special case of kin-recognition genes, and are likewise not o u t l a w s . I h a v e b e e n n e g a t i v e a b o u t t h e p l a u s i b i l i t y o f t h e g r e e n - b e a r d effect. T h e postulated favouritism based on sex c h r o m o s o m e s , w h i c h
I have already
m e n t i o n e d , i s a s p e c i a l c a s e o f t h e g r e e n - b e a r d effect, a n d i s p e r h a p s t h e l e a s t implausible one. I discussed it in the context of w i t h i n - f a m i l y favouritism: elder siblings w e r e supposed to discriminate a m o n g their y o u n g e r siblings on the basis o f p r o b a b i l i t y o f s h a r i n g sex c h r o m o s o m e s , s e x i t s e l f b e i n g u s e d a s the l a b e l ( ' g r e e n b e a r d ' ) . T h i s i s n o t t o o w i l d l y i m p r o b a b l e b e c a u s e , i f Y chromosomes do not pleiotropic
cross o v e r ,
green-beard
chromosome'.
'gene'
instead of h a v i n g to postulate a single
we
can
postulate
a
whole
'green-beard
I t i s sufficient t h a t t h e g e n e t i c b a s i s for s e x u a l f a v o u r i t i s m
s h o u l d o c c u r a n y w h e r e o n t h e sex c h r o m o s o m e c o n c e r n e d . O n e m i g h t m a k e a s i m i l a r a r g u m e n t for a n y s u b s t a n t i a l p o r t i o n o f a c h r o m o s o m e w h i c h , s a y b e c a u s e o f i n v e r s i o n , d i d n o t cross o v e r . I t i s c o n c e i v a b l e , t h e r e f o r e , t h a t a true g r e e n - b e a r d effect o f s o m e k i n d m i g h t o n e d a y b e d i s c o v e r e d . I suspect that all present e x a m p l e s of w h a t m i g h t a p p e a r to be g r e e n - b e a r d effects a r e , i n f a c t , v e r s i o n s o f t h e a r m p i t s e l f - i n s p e c t i o n effect. T h u s W u e t al.
150
O u t l a w s and M o d i f i e r s
( 1 9 8 0 ) p l a c e d i n d i v i d u a l m o n k e y s , Macaca nemestrina, in a c h o i c e a p p a r a t u s w h e r e t h e y h a d t o c h o o s e t o sit n e x t t o o n e o f t w o offered c o m p a n i o n s . I n e a c h c a s e o n e o f t h e t w o c o m p a n i o n s offered w a s a h a l f s i b l i n g , r e l a t e d t h r o u g h the father b u t not the m o t h e r ; the other w a s an unrelated control. T h e r e s u l t w a s a s t a t i s t i c a l l y s i g n i f i c a n t t e n d e n c y for i n d i v i d u a l s t o c h o o s e t o sit n e x t t o h a l f s i b l i n g s r a t h e r t h a n u n r e l a t e d c o n t r o l s . N o t e t h a t the h a l f s i b l i n g s c o n c e r n e d w e r e n o t r e l a t e d i n t h e m a t e r n a l l i n e : this m e a n s t h a t there is no possibility of their r e c o g n i z i n g an o d o u r a c q u i r e d from
the
mother, say.
the
W h a t e v e r the m o n k e y s are recognizing,
i t c o m e s from
s h a r e d f a t h e r , a n d this s u g g e s t s , i n s o m e sense, r e c o g n i t i o n o f s h a r e d g e n e s . My bet is that the m o n k e y s recognize resemblances of relatives to perceived f e a t u r e s o f t h e m s e l v e s . W u e t al. a r e o f t h e s a m e o p i n i o n . Greenberg zephyrum.
(1979)
(Seger,
studied
t h e p r i m i t i v e l y s o c i a l s w e a t b e e Lasioglossum
1 9 8 0 , refers t o this w o r k u n d e r t h e p i c t u r e s q u e h e a d i n g ,
' D o b e e s h a v e g r e e n s e t a e ? ' . ) W h e r e W u e t al. u s e d c h o i c e o f s i t t i n g p a r t n e r as a b e h a v i o u r a l assay, G r e e n b e r g used the decision of a g u a r d w o r k e r w h e t h e r t o a d m i t o r e x c l u d e a n o t h e r w o r k e r s e e k i n g e n t r a n c e t o t h e nest. He
plotted
the
probability
of a
worker's
being
admitted
against
her
coefficient of relationship w i t h the sentinel. N o t o n l y w a s there an excellent p o s i t i v e c o r r e l a t i o n : t h e s l o p e o f t h e l i n e w a s a l m o s t e x a c t l y o n e , s o the p r o b a b i l i t y of a s e n t i n e l a d m i t t i n g a s t r a n g e r w a s a p p r o x i m a t e l y equal to the coefficient o f r e l a t i o n s h i p ! G r e e n b e r g ' s e v i d e n c e c o n v i n c e d him that ' T h e g e n e t i c c o m p o n e n t i s t h e r e f o r e i n o d o r p r o d u c t i o n a n d a p p a r e n t l y n o t i n the p e r c e p t u a l s y s t e m ' (p. 1096). I n m y t e r m i n o l o g y , G r e e n b e r g ' s w o r d s a m o u n t t o t h e s t a t e m e n t t h a t h e i s d e a l i n g w i t h t h e a r m p i t effect, n o t w i t h t h e g r e e n b e a r d effect. O f c o u r s e t h e b e e s m a y , a s G r e e n b e r g b e l i e v e s , h a v e i n s p e c t e d relatives
with
whom
they
were
already
familiar
rather
than
their
own
' a r m p i t s ' ( H o l l d o b l e r & M i c h e n e r 1 9 8 0 ) . I t i s still e s s e n t i a l l y a n e x a m p l e o f t h e a r m p i t r a t h e r t h a n t h e g r e e n - b e a r d effect, i n w h i c h c a s e t h e r e i s n o question of the genes responsible being outlaws. A particularly elegant study w h i c h c o m e s t o a s i m i l a r c o n c l u s i o n i s t h a t o f L i n s e n m a i r ( 1 9 7 2 ) o n the f a m i l y - s p e c i f i c c h e m i c a l ' b a d g e ' o f t h e s o c i a l d e s e r t w o o d l o u s e Hemilepistus reaumuri.
Similarly, Bateson
(in p r e p a r a t i o n )
provides intriguing evidence
that J a p a n e s e q u a i l d i s c r i m i n a t e their first cousins from their siblings and from m o r e distant relatives, using learned visual cues. W a l d m a n and A d l e r (1979) h a v e investigated w h e t h e r tadpoles preferentially
associate
with
siblings.
Colour-marked
tadpoles
taken
from
two
c l u t c h e s w e r e a l l o w e d t o s w i m freely a r o u n d a t a n k ; t h e n a g r i d w a s l o w e r e d into the tank, t r a p p i n g e a c h tadpole in one of sixteen compartments. T h e r e was a statistically significant
t e n d e n c y for t a d p o l e s
to end
up closer to
siblings than to non-siblings. P e r h a p s unfortunately, the e x p e r i m e n t a l design d o e s n o t r u l e o u t a p o s s i b l e c o n f o u n d i n g effect o f g e n e t i c a l l y d e t e r m i n e d 'habitat selection'.
I f t h e r e w a s a g e n e t i c a l l y d e t e r m i n e d t e n d e n c y to, s a y ,
O u t l a w s and M o d i f i e r s
151
h u g the e d g e s o f t h e t a n k r a t h e r t h a n t h e m i d d l e , g e n e t i c r e l a t i v e s m i g h t a s a consequence be e x p e c t e d to end up in the same parts of the tank. T h e experiment does not, therefore, u n e q u i v o c a l l y d e m o n s t r a t e recognition of r e l a t i v e s o r a p r e f e r e n c e for a s s o c i a t i n g w i t h r e l a t i v e s a s s u c h , b u t for m a n y theoretical
purposes
this d o e s
not
matter.
The
authors
introduced
their
paper with reference to Fisher's (1930a) kin selection theory of the e v o l u t i o n o f a p o s e m a t i s m , a n d for p u r p o s e s o f t h a t t h e o r y r e l a t i v e s s i m p l y h a v e t o e n d up together. It doesn't matter whether they are together because of shared habitat preference or b e c a u s e of true relative-recognition. F o r o u r present purpose, h o w e v e r , it is w o r t h n o t i n g that, if further e x p e r i m e n t s confirm the r u l e o f ' i n c i d e n t a l h a b i t a t s e l e c t i o n ' for t h e t a d p o l e s , this w o u l d r u l e o u t t h e 'armpit' theory but w o u l d not rule out the g r e e n - b e a r d theory. S h e r m a n (1979) invokes the i d e a of genetic favouritism in an ingenious theory a b o u t c h r o m o s o m e n u m b e r s in social insects. He presents e v i d e n c e t h a t e u s o c i a l insects t e n d t o h a v e h i g h e r c h r o m o s o m e n u m b e r s t h a n t h e i r nearest
non-social
phylogenetic
relatives.
Seger
(1980)
independently
d i s c o v e r e d t h e effect, a n d h a s his o w n t h e o r y t o a c c o u n t for it. T h e e v i d e n c e for the effect i s s o m e w h a t e q u i v o c a l a n d w o u l d p e r h a p s b e n e f i t f r o m a demanding
analysis
using
the
statistical
methods
developed
by
modern
students of the c o m p a r a t i v e m e t h o d (e.g. H a r v e y & M a c e in press). B u t what I
a m c o n c e r n e d w i t h h e r e i s n o t t h e t r u t h o f t h e effect i t s e l f b u t
S h e r m a n ' s t h e o r y t o a c c o u n t for it. H e c o r r e c t l y n o t e s t h a t h i g h c h r o m o s o m e numbers tend to r e d u c e the v a r i a n c e in fraction of shared genes a m o n g siblings. To take an e x t r e m e case, if a species has o n l y one c h r o m o s o m e pair w i t h n o c r o s s i n g - o v e r , a n y p a i r o f full s i b l i n g s w i l l s h a r e ( i d e n t i c a l b y d e s c e n t ) either all, none, or h a l f of their genes w i t h a m e a n of 50 per cent. If there are hundreds of chromosomes, on the other hand, the n u m b e r of genes shared (identical by descent) a m o n g siblings will be n a r r o w l y distributed a b o u t the same m e a n of 50 per cent. C r o s s i n g - o v e r c o m p l i c a t e s the issue, b u t it r e m a i n s true that a high c h r o m o s o m e n u m b e r in a species tends to go w i t h l o w genetic variance a m o n g siblings in that species. It follows that if social insect workers wished to discriminate in favour of those o f t h e i r s i b l i n g s w i t h w h o m t h e y h a p p e n e d t o s h a r e t h e m o s t g e n e s , i t w o u l d b e e a s i e r for t h e m t o d o s o i f t h e s p e c i e s ' s c h r o m o s o m e n u m b e r w e r e low than if it were high. S u c h preferential discrimination by workers w o u l d b e d e t r i m e n t a l t o t h e f i t n e s s o f the q u e e n , w h o w o u l d ' p r e f e r ' a m o r e e v e n h a n d e d t r e a t m e n t o f h e r o f f s p r i n g . S h e r m a n t h e r e f o r e s u g g e s t s , i n effect, t h a t the h i g h c h r o m o s o m e c o u n t i n e u s o c i a l i n s e c t s i s a n a d a p t a t i o n t o c a u s e "offsprings' r e p r o d u c t i v e interests to m o r e closely c o i n c i d e w i t h those of their m o t h e r " . W e should not forget, b y the w a y , that w o r k e r s w i l l not b e unanimous. E a c h worker might show favouritism towards y o u n g e r siblings t h a t r e s e m b l e h e r , b u t o t h e r w o r k e r s w i l l t e n d t o resist h e r f a v o u r i t i s m , for the s a m e r e a s o n a s t h e q u e e n w i l l resist it. T h e w o r k e r s c a n n o t b e t r e a t e d a s
152
O u t l a w s and M o d i f i e r s
a m o n o l i t h i c p a r t y in opposition to the q u e e n , in the same w a y as T r i v e r s a n d H a r e ( 1 9 7 6 ) w e r e a b l e to treat t h e m in their theory of conflict o v e r the sex r a t i o . S h e r m a n v e r y f a i r l y lists t h r e e w e a k n e s s e s o f his h y p o t h e s i s , b u t t h e r e a r e t w o m o r e s e r i o u s p r o b l e m s w i t h it, F i r s t l y , u n l e s s w e a r e c a r e f u l t o q u a l i f y i t further, the hypothesis a p p e a r s to c o m e d a n g e r o u s l y close to a fallacy w h i c h I h a v e d u b b e d ' M i s u n d e r s t a n d i n g N u m b e r II' ( D a w k i n s 1979a) or the ' A c e of Spades
Fallacy'
(Chapter
10).
Sherman
assumes
that
the
extent of
c o o p e r a t i o n a m o n g c o n s p e c i f i c s i s r e l a t e d t o t h e ' m e a n fraction o f a l l e l e s t h e y s h a r e ' ( m y e m p h a s i s ) w h e r e a s h e s h o u l d t h i n k i n t e r m s o f the probability t h a t a g e n e ' f o r ' c o o p e r a t i o n i s s h a r e d (see a l s o P a r t r i d g e & N u n n e y 1 9 7 7 ) . O n t h e l a t t e r a s s u m p t i o n his h y p o t h e s i s , a s a t p r e s e n t e x p r e s s e d , w o u l d n o t w o r k (Seger
1980).
Sherman
could
r e s c u e his h y p o t h e s i s f r o m
this p a r t i c u l a r
c r i t i c i s m b y i n v o k i n g t h e ' a r m p i t s e l f - r e c o g n i t i o n ' effect. I s h a l l n o t spell t h e a r g u m e n t o u t i n d e t a i l , b e c a u s e I s u s p e c t t h a t S h e r m a n a c c e p t s it.
(The
e s s e n t i a l p o i n t i s t h a t t h e a r m p i t effect c a n use w e a k l i n k a g e w i t h i n a f a m i l y , w h i l e t h e g r e e n - b e a r d effect r e q u i r e s p l e i o t r o p y o r l i n k a g e d i s e q u i l i b r i u m . I f workers
inspect
themselves,
and
show
favouritism
to
those
of
their
r e p r o d u c t i v e siblings that share features that they p e r c e i v e themselves to possess,
ordinary
hypothesis
linkage
could
escape
effects the
become
'Ace
all-important
of Spades
Fallacy'.
and It
Sherman's would
also,
i n c i d e n t a l l y , e s c a p e t h e first o f S h e r m a n ' s o w n o b j e c t i o n s , n a m e l y t h a t the hypothesis ' d e p e n d s on the existence of alleles that e n a b l e their bearers to recognize
their
covered ...',
alleles'.
'Such
recognition
alleles
have
never
been dis-
and, by implication, are pretty implausible. S h e r m a n could
m a k e t h i n g s e a s i e r for h i m s e l f b y t y i n g his h y p o t h e s i s t o t h e a r m p i t r a t h e r t h a n t h e g r e e n - b e a r d effect.) My
second
attention
difficulty
by J.
with
Maynard
Sherman's
Smith
hypothesis
(personal
was
brought
communication).
to
my
Taking
the
' a r m p i t ' version of the theory, it is indeed c o n c e i v a b l e that workers might be s e l e c t e d t o i n s p e c t t h e m s e l v e s , a n d s h o w f a v o u r i t i s m t o w a r d s those o f t h e i r r e p r o d u c t i v e s i b l i n g s t h a t s h a r e t h e i r o w n i n d i v i d u a l c h a r a c t e r i s t i c s . I t i s also t r u e t h a t q u e e n s w o u l d t h e n b e s e l e c t e d t o s u p p r e s s this f a v o u r i t i s m i f t h e y c o u l d , for i n s t a n c e b y p h e r o m o n a l m a n i p u l a t i o n . B u t , i n o r d e r t o b e s e l e c t e d , a n y s u c h m o v e o n t h e p a r t o f a q u e e n w o u l d h a v e t o h a v e a n effect a s soon a s it a r o s e as a m u t a t i o n . W o u l d this be t r u e of a m u t a t i o n t h a t i n c r e a s e d a queen's c h r o m o s o m e n u m b e r ? No it w o u l d not. An increase in chromosome n u m b e r w o u l d c h a n g e the selection pressures b e a r i n g o n w o r k e r favouritism, and m a n y generations later it might produce an evolutionary change which w o u l d b e t o t h e a d v a n t a g e o f q u e e n s i n g e n e r a l . B u t this w o u l d n o t h e l p the original
mutant
queen,
programming and
would
whose
workers
be oblivious
would
follow
their
own
genetic
t o c h a n g e s i n s e l e c t i o n pressures.
C h a n g e s i n s e l e c t i o n p r e s s u r e s e x e r t t h e i r effects o v e r t h e l o n g e r t i m e - s c a l e o f
O u t l a w s and Modifiers
153
generations. A q u e e n c a n n o t be e x p e c t e d to initiate a p r o g r a m of artificial s e l e c t i o n for t h e l o n g - t e r m b e n e f i t o f f u t u r e q u e e n s ! T h e h y p o t h e s i s m a y b e r e s c u e d from this o b j e c t i o n b y s u g g e s t i n g t h a t h i g h c h r o m o s o m e n u m b e r s a r e not an a d a p t a t i o n to facilitate q u e e n m a n i p u l a t i o n of w o r k e r s , b u t rather are a p r e a d a p t a t i o n . T h o s e g r o u p s t h a t h a p p e n e d , for o t h e r r e a s o n s , t o h a v e high chromosome
numbers,
were the most likely
to evolve eusociality.
S h e r m a n m e n t i o n s this v e r s i o n o f his h y p o t h e s i s , b u t sees n o r e a s o n t o f a v o u r i t o v e r the m o r e p o s i t i v e , m a t e r n a l - m a n i p u l a t i o n v e r s i o n .
In conclusion,
Sherman's hypothesis can be m a d e theoretically sound, if it is phrased in terms of p r e a d a p t a t i o n rather t h a n a d a p t a t i o n , a n d in terms of the a r m p i t effect r a t h e r t h a n t h e g r e e n - b e a r d effect. T h e g r e e n - b e a r d effect m a y b e i m p l a u s i b l e , b u t i t i s i n s t r u c t i v e . T h e s t u d e n t o f k i n s e l e c t i o n w h o first u n d e r s t a n d s t h e h y p o t h e t i c a l g r e e n - b e a r d effect, a n d t h e n a p p r o a c h e s k i n s e l e c t i o n t h e o r y i n t e r m s o f its s i m i l a r i t i e s t o a n d d i f f e r e n c e s f r o m ' g r e e n - b e a r d t h e o r y ' , i s u n l i k e l y t o fall p r e y t o t h e m a n y t e m p t i n g o p p o r t u n i t i e s for e r r o r t h a t k i n s e l e c t i o n t h e o r y offers
(Dawkins
1 9 7 9 a ) . M a s t e r y o f the g r e e n - b e a r d m o d e l will c o n v i n c e h i m that altruism t o w a r d s k i n i s n o t a n e n d i n itself, s o m e t h i n g t h a t a n i m a l s a r e m y s t e r i o u s l y e x p e c t e d t o p r a c t i s e i n a c c o r d a n c e w i t h s o m e c l e v e r m a t h e m a t i c s t h a t field workers don't understand. Rather, kinship provides just one w a y in w h i c h genes can b e h a v e as if they recognized and favoured copies of themselves in o t h e r i n d i v i d u a l s . H a m i l t o n h i m s e l f i s e m p h a t i c o n this p o i n t : ' . . . k i n s h i p should be considered just one w a y of getting positive regression of g e n o t y p e i n t h e r e c i p i e n t , a n d . . . i t i s this p o s i t i v e r e g r e s s i o n t h a t i s v i t a l l y n e c e s s a r y for a l t r u i s m . T h u s the i n c l u s i v e fitness c o n c e p t i s m o r e g e n e r a l t h a n " k i n selection"' (Hamilton 1975a, p. 140-141). H a m i l t o n is here using w h a t he earlier described as 'the extended m e a n i n g o f i n c l u s i v e fitness' ( H a m i l t o n 1 9 6 4 b , p . 2 5 ) . T h e c o n v e n t i o n a l m e a n i n g o f inclusive
fitness,
the
meaning
upon
which
Hamilton
himself based
his
d e t a i l e d m a t h e m a t i c s , i s i n c a p a b l e o f h a n d l i n g t h e g r e e n - b e a r d effect a n d , indeed, o u t l a w s such as meiotic-drive genes. T h i s is b e c a u s e it is firmly tied to t h e i d e a of t h e
individual organism
as
'vehicle'
or
' m a x i m i z i n g entity'.
O u t l a w g e n e s d e m a n d t o b e t r e a t e d a s selfish m a x i m i z i n g e n t i t i e s i n t h e i r o w n r i g h t , a n d t h e y c o n s t i t u t e a s t r o n g w e a p o n i n t h e c a s e a g a i n s t t h e 'selfish o r g a n i s m ' p a r a d i g m . N o w h e r e i s this b e t t e r e x e m p l i f i e d t h a n i n H a m i l t o n ' s o w n i n g e n i o u s e x t e n s i o n s o f F i s h e r ' s sex r a t i o t h e o r y ( H a m i l t o n 1 9 6 7 ) . T h e green-beard t h o u g h t e x p e r i m e n t is instructive in further w a y s . A n y o n e w h o thinks a b o u t genes literally as m o l e c u l a r entities is in d a n g e r of b e i n g m i s l e d b y p a s s a g e s l i k e ' W h a t i s t h e selfish g e n e ? I t i s n o t j u s t o n e s i n g l e p h y s i c a l bit o f D N A . . . I t i s all replicas o f a p a r t i c u l a r b i t o f D N A , d i s t r i b u t e d throughout the w o r l d . . . a distributed a g e n c y , existing in m a n y different i n d i v i d u a l s a t o n c e . . . a g e n e m i g h t b e a b l e t o assist replicas o f i t s e l f w h i c h a r e s i t t i n g i n o t h e r b o d i e s . ' T h e w h o l e o f k i n s e l e c t i o n t h e o r y rests o n this g e n e r a l
154
O u t l a w s and Modifiers
p r e m i s e , y e t i t w o u l d b e m y s t i c a l a n d w r o n g t o t h i n k t h a t g e n e s assist c o p i e s o f e a c h o t h e r because t h o s e c o p i e s a r e i d e n t i c a l m o l e c u l e s t o t h e m s e l v e s . A g r e e n b e a r d t h o u g h t e x p e r i m e n t h e l p s t o e x p l a i n this. C h i m p a n z e e s a n d g o r i l l a s a r e s o s i m i l a r t h a t a g e n e i n o n e s p e c i e s m i g h t b e p h y s i c a l l y i d e n t i c a l i n its m o l e c u l a r d e t a i l s to a g e n e in t h e o t h e r . Is this m o l e c u l a r i d e n t i t y a sufficient reason to e x p e c t selection to favour genes in one species ' r e c o g n i z i n g ' copies of themselves in the other species, a n d extending them a helping h a n d ? T h e a n s w e r i s n o , a l t h o u g h a n a i v e a p p l i c a t i o n o f 'selfish g e n e ' r e a s o n i n g a t the m o l e c u l a r level m i g h t lead us to think otherwise. N a t u r a l selection at the g e n e level is c o n c e r n e d w i t h c o m p e t i t i o n a m o n g a l l e l e s for a p a r t i c u l a r c h r o m o s o m a l slot in a s h a r e d g e n e - p o o l . A g r e e n b e a r d g e n e i n t h e c h i m p a n z e e g e n e p o o l i s n o t a c a n d i d a t e for a slot o n a n y g o r i l l a c h r o m o s o m e , a n d n o r i s a n y o f its a l l e l e s . I t i s t h e r e f o r e indifferent t o t h e fate o f its s t r u c t u r a l l y i d e n t i c a l c o u n t e r p a r t i n t h e g o r i l l a g e n e - p o o l . (It not
be
counterpart
might
in
indifferent the
to
gorilla
molecular identity.)
the
fate
gene-pool,
of
but
its that
phenotypically
identical
has
do with
nothing
to
A s far a s t h e p r e s e n t a r g u m e n t i s c o n c e r n e d , c h i m p
g e n e s a n d g o r i l l a g e n e s a r e n o t c o p i e s o f e a c h o t h e r i n a n i m p o r t a n t sense. T h e y a r e c o p i e s o f e a c h o t h e r o n l y i n t h e t r i v i a l sense t h a t t h e y h a p p e n t o h a v e the i d e n t i c a l m o l e c u l a r structure. T h e unconscious, m e c h a n i c a l laws o f n a t u r a l s e l e c t i o n g i v e u s n o g r o u n d s for e x p e c t i n g t h e m t o assist m o l e c u l a r c o p i e s , j u s t b e c a u s e t h e y are m o l e c u l a r c o p i e s . Conversely,
we m i g h t be justified
i n e x p e c t i n g t o see g e n e s assisting
m o l e c u l a r l y different alleles at their o w n locus w i t h i n a species g e n e - p o o l , p r o v i d e d t h e y h a d t h e s a m e p h e n o t y p i c effects. A p h e n o t y p i c a l l y n e u t r a l mutation at a locus changes molecular identity but does nothing to weaken a n y selection there m a y be in favour of m u t u a l assistance.
Green-beard
a l t r u i s m c o u l d still i n c r e a s e t h e i n c i d e n c e o f g r e e n - b e a r d p h e n o t y p e s i n the population,
even
t h o u g h g e n e s w e r e assisting o t h e r g e n e s t h a t w e r e not
s t r i c t c o p i e s o f t h e m s e l v e s i n t h e m o l e c u l a r sense.
It is the incidence of
phenotypes
not
that
we
are
interested
in
explaining,
the
incidence
of
m o l e c u l a r c o n f i g u r a t i o n s o f D N A . A n d i f a n y r e a d e r t h i n k s t h a t last r e m a r k c o n t r a d i c t s m y b a s i c thesis, I m u s t h a v e failed t o m a k e m y b a s i c thesis c l e a r ! L e t m e use t h e g r e e n b e a r d i n o n e m o r e i n s t r u c t i v e t h o u g h t e x p e r i m e n t , t o c l a r i f y t h e t h e o r y o f r e c i p r o c a l a l t r u i s m . I h a v e c a l l e d t h e g r e e n - b e a r d effect i m p l a u s i b l e , w i t h t h e p o s s i b l e e x c e p t i o n o f t h e sex c h r o m o s o m e s p e c i a l cases. But
there
is
another
special
case
which
could
conceivably
have some
c o u n t e r p a r t in reality. I m a g i n e a g e n e p r o g r a m m i n g the b e h a v i o u r a l rule: ' I f y o u see a n o t h e r i n d i v i d u a l p e r f o r m i n g a n a l t r u i s t i c a c t , r e m e m b e r t h e incident,
and
individual in
i f t h e o p p o r t u n i t y arises b e h a v e a l t r u i s t i c a l l y t o w a r d s future'
'altruism-recognition
(Dawkins effect.'
1976a,
Using
the
p.
96).
This m a y be called
legendary
example
that the
of Haldane's
(1955) j u m p i n g into the river to save a d r o w n i n g person, the g e n e that I am
O u t l a w s and M o d i f i e r s
155
p o s t u l a t i n g m i g h t s p r e a d b e c a u s e i t w a s , i n effect, r e c o g n i z i n g c o p i e s o f itself. I t is, i n fact, a k i n d o f g r e e n - b e a r d g e n e . I n s t e a d o f u s i n g a n i n c i d e n t a l p l e i o t r o p i c r e c o g n i t i o n c h a r a c t e r s u c h as a g r e e n b e a r d , it uses a n o n i n c i d e n t a l o n e : t h e b e h a v i o u r p a t t e r n o f a l t r u i s t i c r e s c u i n g itself. R e s c u e r s tend t o s a v e o n l y o t h e r s w h o h a v e r e s c u e d s o m e b o d y i n t h e i r t i m e , s o t h e gene tends to save copies of itself (setting aside p r o b l e m s of h o w the system c o u l d g e t s t a r t e d , e t c . ) . M y p o i n t i n b r i n g i n g this h y p o t h e t i c a l e x a m p l e u p h e r e i s t o e m p h a s i z e its d i s t i n c t n e s s f r o m t w o o t h e r , s u p e r f i c i a l l y s i m i l a r cases. T h e f i r s t i s t h e o n e H a l d a n e h i m s e l f w a s i l l u s t r a t i n g , t h e s a v i n g o f c l o s e kin;
thanks
to
Hamilton
we
now
understand
this
well.
T h e second
is
reciprocal altruism (Trivers 1 9 7 1 ) . A n y resemblance b e t w e e n true reciprocal a l t r u i s m a n d the h y p o t h e t i c a l a l t r u i s m - r e c o g n i t i o n c a s e I a m n o w d i s c u s s i n g is purely accidental (Rothstein 1981). T h e resemblance, h o w e v e r , sometimes muddles students of the t h e o r y of r e c i p r o c a l altruism, w h i c h is w h y I am m a k i n g use o f g r e e n - b e a r d t h e o r y t o d i s p e l t h e m u d d l e . I n true r e c i p r o c a l a l t r u i s m , t h e ' a l t r u i s t ' s t a n d s t o g a i n i n t h e f u t u r e f r o m the p r e s e n c e o f the individual b e n e f i c i a r y o f his a l t r u i s m . T h e effect w o r k s e v e n i f t h e t w o s h a r e n o g e n e s , a n d e v e n (contra R o t h s t e i n
1981) if they
b e l o n g t o different s p e c i e s , a s i n T r i v e r s ' s e x a m p l e o f t h e m u t u a l i s m b e t w e e n cleaner fish and
their clients.
Genes mediating such reciprocal
altruism
benefit t h e rest o f t h e g e n o m e n o less t h a n t h e y b e n e f i t t h e m s e l v e s , a n d a r e clearly
not
outlaws.
They
are
favoured
by
ordinary,
familiar
natural
selection, albeit some p e o p l e (e.g. Sahlins 1 9 7 7 , p p . 8 5 - 8 7 ) seem to h a v e difficulty i n u n d e r s t a n d i n g t h e p r i n c i p l e , a p p a r e n t l y b e c a u s e t h e y o v e r l o o k the f r e q u e n c y - d e p e n d e n t n a t u r e o f t h e s e l e c t i o n a n d t h e c o n s e q u e n t n e e d t o think i n g a m e - t h e o r e t i c t e r m s ( D a w k i n s 1 9 7 6 a , p p . 1 9 7 — 2 0 1 ; A x e l r o d a n d H a m i l t o n 1 9 8 1 ) . T h e a l t r u i s m - r e c o g n i t i o n effect i s f u n d a m e n t a l l y different, t h o u g h s u p e r f i c i a l l y s i m i l a r . T h e r e i s n o n e e d for t h e a l t r u i s m r e c o g n i z e r i n d i v i d u a l t o r e p a y a g o o d t u r n d o n e t o himself. H e s i m p l y r e c o g n i z e s g o o d d e e d s d o n e t o a n y b o d y , a n d s i n g l e s o u t t h e a l t r u i s t for his o w n l a t e r f a v o u r s . It w o u l d be impossible to g i v e a sensible a c c o u n t of o u t l a w s in terms of i n d i v i d u a l s m a x i m i z i n g t h e i r f i t n e s s . T h a t i s t h e r e a s o n for g i v i n g t h e m p r o m i n e n c e i n this b o o k . A t t h e b e g i n n i n g o f t h e c h a p t e r I d i v i d e d o u t l a w s into 'allelic o u t l a w s ' a n d 'laterally spreading o u t l a w s ' . A l l the suggested o u t l a w s w e h a v e s o far c o n s i d e r e d h a v e b e e n a l l e l i c : t h e y a r e f a v o u r e d o v e r their a l l e l e s a t t h e i r o w n l o c i , w h i l e b e i n g o p p o s e d b y m o d i f i e r s a t o t h e r l o c i . I n o w turn to laterally s p r e a d i n g o u t l a w s . T h e s e are o u t l a w s u n r u l y e n o u g h to break a w a y a l t o g e t h e r from the discipline of allelic c o m p e t i t i o n w i t h i n the confines o f a l o c u s . T h e y s p r e a d t o o t h e r l o c i , e v e n c r e a t e n e w l o c i for t h e m s e l v e s b y i n c r e a s i n g t h e size o f the g e n o m e . T h e y a r e c o n v e n i e n t l y discussed
under
the
heading
'Selfish
DNA',
a
catch-phrase
which
has
r e c e n t l y a c q u i r e d c u r r e n c y i n t h e p a g e s o f Nature. T h i s w i l l b e t h e s u b j e c t o f the f i r s t p a r t o f t h e n e x t c h a p t e r .
9 Selfish D N A , J u m p i n g Genes, and a L a m a r c k i a n Scare
This
chapter
will
be
a
somewhat
miscellaneous
one,
gathering
t o g e t h e r t h e results o f m y b r i e f a n d f o o l h a r d y i n c u r s i o n s i n t o t h e h i n t e r l a n d s o f fields far f r o m m y o w n , m o l e c u l a r a n d c e l l b i o l o g y , i m m u n o l o g y a n d e m b r y o l o g y . T h e b r e v i t y I justify on the grounds that greater length w o u l d be
even
more
foolhardy.
The
foolhardiness
is
less d e f e n s i b l e ,
but
may
p e r h a p s be forgiven on the g r o u n d s that an e q u a l l y rash earlier raid yielded the g e r m o f a n i d e a w h i c h s o m e m o l e c u l a r biologists n o w take seriously under the n a m e o f Selfish D N A .
Selfish D N A . . . it a p p e a r s that the a m o u n t of D N A in organisms is m o r e than is s t r i c t l y n e c e s s a r y for b u i l d i n g t h e m : a l a r g e f r a c t i o n o f t h e D N A i s n e v e r translated into protein. F r o m the point of v i e w of the i n d i v i d u a l organism
this
seems
supervise
the
b u i l d i n g of b o d i e s ,
paradoxical.
I f the it
'purpose'
of D N A is
is s u r p r i s i n g to find
to
a large
quantity of D N A w h i c h does no such thing. Biologists are racking t h e i r b r a i n s t r y i n g t o t h i n k w h a t this s u r p l u s D N A i s d o i n g . B u t from t h e p o i n t o f v i e w o f t h e selfish g e n e s t h e m s e l v e s , t h e r e i s n o p a r a d o x . T h e t r u e ' p u r p o s e ' o f D N A i s t o s u r v i v e , n o m o r e a n d n o less. T h e simplest w a y to e x p l a i n the surplus D N A is to suppose that it is a p a r a s i t e , or at best a h a r m l e s s b u t useless p a s s e n g e r , h i t c h i n g a r i d e in the survival m a c h i n e s created b y the other D N A [ D a w k i n s 1976a, p. 47]. T h i s i d e a w a s d e v e l o p e d f u r t h e r a n d w o r k e d o u t m o r e fully b y m o l e c u l a r biologists
in
two
stimulating
papers
published
simultaneously
in
Nature
(Doolittle & S a p i e n z a 1980; O r g e l & C r i c k 1980). T h e s e papers provoked c o n s i d e r a b l e d i s c u s s i o n , i n l a t e r issues o f Nature ( s y m p o s i a i n V o l . 285, p p . 617-620
and
Vol.
288,
pp.
645-648) 156
and
elsewhere
(e.g.
BBC
radio
Selfish D N A , J u m p i n g G e n e s , a n d a L a m a r c k i a n S c a r e
157
d i s c u s s i o n ) . T h e i d e a is, o f c o u r s e , h i g h l y c o n g e n i a l t o t h e w h o l e thesis b e i n g a d v a n c e d i n this b o o k . T h e facts a r e a s f o l l o w s . T h e t o t a l a m o u n t o f D N A i n different o r g a n i s m s i s v e r y v a r i a b l e , a n d t h e v a r i a t i o n d o e s n o t m a k e o b v i o u s sense i n t e r m s o f phylogeny.
This
is
implausible
that
the
the
so-called
number
'C-value
of radically
paradox'. different
'It
genes
seems
totally
needed
in
a
s a l a m a n d e r is 20 t i m e s t h a t f o u n d in a m a n ' ( O r g e l & C r i c k 1 9 8 0 ) . It is e q u a l l y i m p l a u s i b l e t h a t s a l a m a n d e r s o n t h e W e s t side o f N o r t h A m e r i c a should need m a n y times m o r e D N A than c o n g e n e r i c s a l a m a n d e r s o n the E a s t side. A l a r g e p e r c e n t a g e o f t h e D N A i n e u k a r y o t i c g e n o m e s i s n e v e r t r a n s l a t e d . T h i s ' j u n k D N A ' m a y lie b e t w e e n c i s t r o n s , i n w h i c h c a s e i t i s k n o w n a s s p a c e r D N A , o r i t m a y consist o f u n e x p r e s s e d ' i n t r o n s ' w i t h i n cistrons,
interspersed with
(Crick
1979).
the expressed parts of the cistron,
the
'exons'
T h e apparently surplus D N A m a y b e t o v a r y i n g extents
repetitive and meaningless in terms of the genetic c o d e . S o m e is p r o b a b l y never transcribed into R N A . O t h e r portions m a y b e transcribed into R N A , but then 'spliced out' before the R N A is translated into a m i n o a c i d sequences. Either w a y , it is never expressed phenotypically, if by p h e n o t y p i c expression we m e a n expression v i a the o r t h o d o x route of c o n t r o l l i n g protein synthesis (Doolittle & S a p i e n z a 1980). T h i s does not m e a n , h o w e v e r , that the so-called j u n k D N A i s n o t subject t o n a t u r a l s e l e c t i o n . V a r i o u s ' f u n c t i o n s ' for i t h a v e b e e n p r o p o s e d , w h e r e 'function'
means
adaptive
benefit
to
the
organism.
The
'function'
of
extra D N A m a y 'simply b e t o separate the g e n e s ' ( C o h e n 1 9 7 7 , p . 1 7 2 ) . E v e n if a stretch of D N A is not itself transcribed, it c a n increase the f r e q u e n c y of c r o s s o v e r s b e t w e e n g e n e s s i m p l y b y o c c u p y i n g s p a c e b e t w e e n t h e m , a n d this is a kind of p h e n o t y p i c expression. S p a c e r D N A m i g h t , therefore, in s o m e sense b e f a v o u r e d b y n a t u r a l s e l e c t i o n b e c a u s e o f its effects o n c r o s s o v e r frequencies. It w o u l d not, h o w e v e r , be c o m p a t i b l e w i t h c o n v e n t i o n a l usage to describe a length of spacer D N A as e q u i v a l e n t to a ' g e n e for' a g i v e n r e c o m b i n a t i o n r a t e . T o q u a l i f y for this title, a g e n e m u s t h a v e a n effect o n r e c o m b i n a t i o n r a t e s in comparison with its alleles. It is m e a n i n g f u l to s p e a k of a given
length
of
spacer
DNA
as
having
alleles—differing
sequences
o c c u p y i n g the same space on other c h r o m o s o m e s in the p o p u l a t i o n . B u t since the p h e n o t y p i c effect o f s p a c i n g o u t g e n e s i s a r e s u l t s o l e l y o f t h e l e n g t h o f t h e stretch o f s p a c e r D N A , a l l a l l e l e s a t a g i v e n ' l o c u s ' m u s t h a v e t h e s a m e 'phenotypic expression' if they all h a v e the same length. If the 'function' of surplus D N A is 'to' s p a c e o u t genes, therefore, the w o r d function is b e i n g used i n a n u n u s u a l w a y . T h e n a t u r a l s e l e c t i o n p r o c e s s i n v o l v e d i s n o t t h e ordinary
natural
selection
among
alleles
at
a
locus.
Rather,
it
is
the
perpetuation of a feature of the genetic system—distance b e t w e e n genes. A n o t h e r p o s s i b l e ' f u n c t i o n ' for t h e n o n - e x p r e s s e d D N A i s t h a t s u g g e s t e d b y C a v a l i e r - S m i t h ( 1 9 7 8 ) . H i s t h e o r y i s e n c a p s u l a t e d i n his t i t l e : ' N u c l e a r
158
Selfish D N A , J u m p i n g G e n e s , and a L a m a r c k i a n Scare
v o l u m e c o n t r o l b y n u c l e o s k e l e t a l D N A , s e l e c t i o n for c e l l v o l u m e a n d cell g r o w t h rate, a n d the solution o f the D N A C - v a l u e p a r a d o x . ' H e thinks that 'K-selected' organisms
need
l a r g e r cells
than
'r-selected'
ones,
and
that
v a r y i n g the total a m o u n t of D N A per cell is a g o o d w a y of controlling cell s i z e . H e asserts t h a t ' t h e r e i s a g o o d c o r r e l a t i o n b e t w e e n s t r o n g r - s e l e c t i o n , small cells a n d l o w C - v a l u e s on the one h a n d a n d b e t w e e n K-selection, large cells a n d h i g h C - v a l u e s o n t h e o t h e r ' . I t w o u l d b e i n t e r e s t i n g t o test for this correlation
statistically,
taking
account
of
the
difficulties
inherent
in
q u a n t i t a t i v e c o m p a r a t i v e s u r v e y s ( H a r v e y & M a c e i n p r e s s ) . T h e r\K dist i n c t i o n itself, t o o , s e e m s t o a r o u s e w i d e s p r e a d d o u b t s a m o n g e c o l o g i s t s , for reasons that h a v e n e v e r b e e n quite clear to m e , and sometimes seem unclear to t h e m too.
I t i s o n e o f t h o s e c o n c e p t s t h a t i s often u s e d ,
but almost
a l w a y s a c c o m p a n i e d by a ritualistic a p o l o g y , the intellectual e q u i v a l e n t of touching wood.
S o m e o b j e c t i v e i n d e x o f a s p e c i e s ' s p o s i t i o n o n the r / K
c o n t i n u u m w o u l d b e n e e d e d b e f o r e a r i g o r o u s test o f t h e c o r r e l a t i o n c o u l d b e undertaken. While
awaiting
further
evidence
for
and
against
hypotheses
o f the
C a v a l i e r - S m i t h v a r i e t y , the thing to notice in the present c o n t e x t is that they are hypotheses m a d e in the traditional m o u l d ; they are based on the idea that D N A , like a n y o t h e r aspect of an o r g a n i s m , is selected b e c a u s e it does the
organism
some
good.
The
selfish
DNA
hypothesis
is
based
on
an
i n v e r s i o n o f this a s s u m p t i o n : p h e n o t y p i c c h a r a c t e r s a r e t h e r e b e c a u s e t h e y h e l p D N A t o r e p l i c a t e itself, a n d i f D N A c a n find q u i c k e r a n d e a s i e r w a y s t o r e p l i c a t e itself, p e r h a p s b y p a s s i n g c o n v e n t i o n a l p h e n o t y p i c e x p r e s s i o n , i t w i l l b e s e l e c t e d t o d o s o . E v e n i f t h e E d i t o r o f Nature ( V o l . 2 8 5 , p . 604, 1980) g o e s a bit far in d e s c r i b i n g it as ' m i l d l y s h o c k i n g ' , t h e t h e o r y of selfish D N A is in a w a y r e v o l u t i o n a r y . B u t o n c e w e d e e p l y i m b i b e the f u n d a m e n t a l truth that an o r g a n i s m is a tool of D N A , rather than the other w a y a r o u n d , the idea of 'selfish D N A ' b e c o m e s c o m p e l l i n g , e v e n o b v i o u s . T h e l i v i n g c e l l , e s p e c i a l l y t h e n u c l e u s i n e u k a r y o t e s , i s p a c k e d w i t h the active
machinery
of nucleic
polymerase readily whether or not
that
catalyses D N A is
acid
replication
and
the replication of any meaningful in
recombination. DNA,
DNA
regardless of
terms of the genetic code.
' S n i p p i n g o u t ' o f D N A , a n d ' s p l i c i n g i n ' o f o t h e r bits o f D N A , a r e also p a r t s o f t h e n o r m a l s t o c k i n t r a d e o f t h e c e l l u l a r a p p a r a t u s , for t h e y o c c u r e v e r y t i m e there is a crossover or other t y p e of r e c o m b i n a t i o n event. T h e fact that i n v e r s i o n s a n d o t h e r t r a n s l o c a t i o n s s o r e a d i l y o c c u r , f u r t h e r testifies t o the c a s u a l e a s e w i t h w h i c h c h u n k s o f D N A m a y b e c u t o u t o f o n e p a r t o f the g e n o m e , a n d spliced into another part. R e p l i c a b i l i t y and 'spliceability' seem t o b e a m o n g t h e m o s t s a l i e n t f e a t u r e s o f D N A i n its n a t u r a l e n v i r o n m e n t ( R i c h m o n d 1979) of cellular machinery. G i v e n the possibilities of such an e n v i r o n m e n t , g i v e n the existence of c e l l u l a r f a c t o r i e s set u p for t h e r e p l i c a t i o n a n d s p l i c i n g o f D N A , i t i s o n l y t o b e e x p e c t e d that natural selection w o u l d favour D N A variants that are able
Selfish D N A , J u m p i n g G e n e s , a n d a L a m a r c k i a n S c a r e
159
t o e x p l o i t t h e c o n d i t i o n s t o t h e i r o w n a d v a n t a g e . A d v a n t a g e , i n this c a s e , simply means multiple replication in germ-lines. A n y variety of D N A whose properties h a p p e n to m a k e it readily replicated will a u t o m a t i c a l l y b e c o m e c o m m o n e r i n the w o r l d . W h a t might such properties be? Paradoxically, we are most familiar w i t h the
more
indirect,
elaborate,
and
roundabout
methods
by
which
DNA
m o l e c u l e s s e c u r e t h e i r f u t u r e . T h e s e a r e t h e i r p h e n o t y p i c effects o n b o d i e s , a c h i e v e d by the p r o x i m a l route of c o n t r o l l i n g protein synthesis, a n d h e n c e by
the
more
distal
routes
of
controlling
embryonic
development
of
m o r p h o l o g y , physiology and b e h a v i o u r . B u t there are also m u c h m o r e direct and simple w a y s i n w h i c h varieties o f D N A c a n spread a t the e x p e n s e o f rival varieties. It is b e c o m i n g increasingly evident that, in addition to the large, orderly c h r o m o s o m e s w i t h their w e l l - r e g i m e n t e d g a v o t t e , cells are h o m e to a m o t l e y riff-raff o f D N A a n d
R N A fragments,
cashing in
on
the perfect
e n v i r o n m e n t p r o v i d e d by the cellular a p p a r a t u s . T h e s e replicating fellow-travellers go by various n a m e s d e p e n d i n g on size and properties: plasmids, episomes, insertion sequences, plasmons, virions, transposons, replicons, viruses. W h e t h e r they should be r e g a r d e d as rebels who have
broken
a w a y from
the c h r o m o s o m a l g a v o t t e ,
or as invading
p a r a s i t e s f r o m o u t s i d e , s e e m s t o m a t t e r less a n d less. T o t a k e a p a r a l l e l , w e m a y r e g a r d a p o n d , or a forest, as a c o m m u n i t y w i t h a c e r t a i n s t r u c t u r e , a n d e v e n a c e r t a i n s t a b i l i t y . B u t the s t r u c t u r e a n d s t a b i l i t y a r e m a i n t a i n e d i n t h e face
of a
constant
turnover
of participants.
Individuals
immigrate
and
emigrate, n e w ones are b o r n a n d old ones die. T h e r e is a fluidity, a j u m p i n g in and out of c o m p o n e n t parts, so that it b e c o m e s m e a n i n g l e s s to try to distinguish 'true' c o m m u n i t y m e m b e r s from foreign invaders. So it is w i t h the g e n o m e . It is n o t a s t a t i c s t r u c t u r e , b u t a fluid c o m m u n i t y . ' J u m p i n g genes' immigrate and emigrate (Cohen 1976).
S i n c e t h e r a n g e o f p o s s i b l e hosts i n n a t u r e a t l e a s t for t r a n s f o r m i n g D N A a n d for p l a s m i d s s u c h a s R P 4 i s s o l a r g e , o n e feels t h a t a t least i n G r a m - n e g a t i v e b a c t e r i a all p o p u l a t i o n s m a y i n d e e d b e c o n n e c t e d . I t i s k n o w n that b a c t e r i a l D N A c a n b e expressed i n w i d e l y different host
species . . . It
may
indeed
by
impossible
to
view
bacterial
evolution in terms of simple family trees; rather, a n e t w o r k , w i t h converging as well as diverging junctions, m a y be a more appropriate metaphor [Broda 1979, p. 140]. Some
authors
speculate
that
the
network
is
not
confined
to
bacterial
evolution (e.g. M a r g u l i s 1976). T h e r e i s s u b s t a n t i a l e v i d e n c e t h a t o r g a n i s m s a r e n o t l i m i t e d for t h e i r evolution
to genes that b e l o n g to the g e n e pool of their species.
R a t h e r it seems m o r e plausible that in the time-scale of e v o l u t i o n the
160
Selfish D N A , J u m p i n g G e n e s , and a L a m a r c k i a n Scare
w h o l e o f t h e g e n e p o o l o f the b i o s p h e r e i s a v a i l a b l e t o a l l o r g a n i s m s and
t h a t t h e m o r e d r a m a t i c steps a n d
apparent discontinuities in
e v o l u t i o n a r e i n f a c t a t t r i b u t a b l e t o v e r y r a r e e v e n t s i n v o l v i n g the a d o p t i o n of part or all of a foreign g e n o m e . O r g a n i s m s and genomes m a y thus be r e g a r d e d as c o m p a r t m e n t s of the biosphere through w h i c h genes
in
general circulate at various
rates and
in which
i n d i v i d u a l g e n e s a n d o p e r o n s m a y b e i n c o r p o r a t e d i f o f sufficient a d v a n t a g e . . .' [ J e o n & D a n i e l l i 1 9 7 1 ] . T h a t e u k a r y o t e s , i n c l u d i n g o u r s e l v e s , m a y not
b e i n s u l a t e d from this
h y p o t h e t i c a l g e n e t i c traffic i s s u g g e s t e d b y t h e f a s t - g r o w i n g s u c c e s s o f the technology definition
of
'genetic
of g e n e
engineering',
manipulation
in
or
gene
Britain
manipulation. is
'the
The
formation
legal
of new
c o m b i n a t i o n s of heritable material by the insertion of nucleic acid molecules, p r o d u c e d by w h a t e v e r m e a n s outside the cell,
into a n y virus, bacterial
p l a s m i d o r o t h e r v e c t o r s y s t e m s o a s t o a l l o w t h e i r i n c o r p o r a t i o n i n t o a host organism in w h i c h they do not naturally occur but in w h i c h they are capable o f c o n t i n u e d p r o p a g a t i o n ' ( O l d & P r i m r o s e 1980, p . 1 ) . B u t o f c o u r s e h u m a n genetic engineers are beginners in the g a m e . T h e y are just learning to tap the expertise of the n a t u r a l g e n e t i c engineers, the viruses a n d plasmids that h a v e b e e n selected to m a k e their living at the trade. P e r h a p s t h e g r e a t e s t f e a t o f n a t u r a l g e n e t i c e n g i n e e r i n g o n the g r a n d s c a l e is the c o m p l e x of manipulations associated with sexual reproduction in eukaryotes:
meiosis, crossing-over a n d fertilization. T w o o f our foremost
m o d e r n e v o l u t i o n i s t s h a v e f a i l e d t o e x p l a i n t o t h e i r o w n s a t i s f a c t i o n the advantage
o f this
extraordinary
procedure
for
the
individual
organism
(Williams 1 9 7 5 ; M a y n a r d Smith 1978a). As M a y n a r d Smith (1978a, p. 113) a n d W i l l i a m s ( 1 9 7 9 ) b o t h n o t e , this m a y b e o n e a r e a w h e r e , i f n o w h e r e else, w e s h a l l h a v e t o s w i t c h o u r a t t e n t i o n a w a y from i n d i v i d u a l o r g a n i s m s t o t r u e replicators. W h e n w e try t o solve the p a r a d o x o f the cost o f meiosis, perhaps i n s t e a d o f w o r r y i n g a b o u t h o w s e x h e l p s t h e organism w e s h o u l d s e a r c h for r e p l i c a t i n g 'engineers' of meiosis, intracellular agents w h i c h actually cause meiosis to h a p p e n . T h e s e h y p o t h e t i c a l engineers, fragments of nucleic acid w h i c h m i g h t lie i n s i d e o r o u t s i d e t h e c h r o m o s o m e s , w o u l d h a v e t o a c h i e v e their o w n r e p l i c a t i o n success as a b y p r o d u c t of forcing meiosis u p o n the organism. In bacteria, r e c o m b i n a t i o n is a c h i e v e d by a separate fragment of D N A o r ' s e x f a c t o r ' w h i c h , i n o l d e r t e x t b o o k s , w a s t r e a t e d a s a p a r t o f the bacterium's o w n adaptive machinery, but w h i c h is better regarded as a r e p l i c a t i n g g e n e t i c e n g i n e e r w o r k i n g for its o w n g o o d . I n a n i m a l s , c e n t r i o l e s are
thought
mitochondria,
to
be
self-replicating
entities
with
their
own
DNA,
like
a l t h o u g h u n l i k e m i t o c h o n d r i a t h e y often pass t h r o u g h the
m a l e as w e l l as the female line. A l t h o u g h at present it is just a j o k e to picture c h r o m o s o m e s b e i n g d r a g g e d k i c k i n g and s c r e a m i n g into the second anaphase
Selfish D N A , J u m p i n g G e n e s , a n d a L a m a r c k i a n S c a r e
161
b y r u t h l e s s l y selfish c e n t r i o l e s o r o t h e r m i n i a t u r e g e n e t i c e n g i n e e r s , s t r a n g e r ideas h a v e
b e c o m e c o m m o n p l a c e in the past.
And,
after a l l ,
orthodox
t h e o r i z i n g h a s s o far failed t o d e n t t h e p a r a d o x o f t h e c o s t o f m e i o s i s . O r g e l a n d C r i c k ( 1 9 8 0 ) s a y m u c h t h e s a m e a b o u t t h e lesser p a r a d o x o f v a r i a b l e C v a l u e s a n d a b o u t the selfish D N A t h e o r y t o a c c o u n t for i t : ' T h e m a i n facts a r e , a t first s i g h t , s o o d d t h a t o n l y a s o m e w h a t u n c o n v e n t i o n a l idea is likely to e x p l a i n t h e m . ' By a c o m b i n a t i o n of fact a n d d a y d r e a m e d e x t r a p o l a t i o n , I h a v e t r i e d t o set a s t a g e o n t o w h i c h selfish D N A i t s e l f c a n e n t e r a l m o s t u n n o t i c e d ; t o p a i n t a b a c k d r o p a g a i n s t w h i c h selfish D N A w i l l appear,
not
unconventional
but
almost
inescapable.
DNA
that
is
not
translated into protein, w h o s e c o d o n s w o u l d spell m e a n i n g l e s s g i b b e r i s h if t h e y e v e r w e r e t r a n s l a t e d , m a y y e t v a r y i n its r e p l i c a b i l i t y , its s p l i c e a b i l i t y , a n d its r e s i s t a n c e t o d e t e c t i o n a n d d e l e t i o n b y t h e d e b u g g i n g r o u t i n e s o f t h e cellular
machinery.
'Intragenomic
selection'
can
therefore
lead
to
an
i n c r e a s e i n the a m o u n t o f c e r t a i n t y p e s o f m e a n i n g l e s s , o r u n t r a n s c r i b e d , D N A , littered a r o u n d a n d cluttering u p the c h r o m o s o m e s . T r a n s l a t e d D N A , too, m a y b e s u b j e c t t o this k i n d o f s e l e c t i o n , a l t h o u g h h e r e t h e i n t r a g e n o m i c selection pressures will p r o b a b l y be s w a m p e d by m o r e p o w e r f u l pressures, p o s i t i v e a n d n e g a t i v e , r e s u l t i n g f r o m c o n v e n t i o n a l p h e n o t y p i c effects. C o n v e n t i o n a l s e l e c t i o n results i n c h a n g e s i n t h e f r e q u e n c y o f r e p l i c a t o r s relative to their alleles at defined loci on the c h r o m o s o m e s of p o p u l a t i o n s . I n t r a g e n o m i c s e l e c t i o n o f selfish D N A i s a d i f f e r e n t k i n d o f s e l e c t i o n . H e r e we are not d e a l i n g w i t h the relative success of alleles at o n e locus in a g e n e p o o l , b u t w i t h t h e s p r e a d a b i l i t y o f c e r t a i n k i n d s o f D N A t o different l o c i o r the c r e a t i o n o f n e w l o c i . M o r e o v e r , t h e s e l e c t i o n o f selfish D N A i s n o t l i m i t e d to the time-scale of i n d i v i d u a l g e n e r a t i o n s ; it c a n selectively increase in a n y mitotic cell division in the germ-lines of d e v e l o p i n g bodies. In
conventional
selection,
the
variation
on
which
selection
acts
is
produced, ultimately, by mutation, but we usually think of it as mutation within the constraints of an o r d e r l y system of l o c i : m u t a t i o n p r o d u c e s a variant gene at a n a m e d locus. It is therefore possible to think of selection as c h o o s i n g a m o n g a l l e l e s a t s u c h a d i s c r e t e l o c u s . M u t a t i o n i n t h e l a r g e r sense, h o w e v e r , includes m o r e r a d i c a l c h a n g e s in the g e n e t i c system, m i n o r ones such as inversions, and major ones such as c h a n g e s in c h r o m o s o m e n u m b e r or ploidy, a n d c h a n g e s from s e x u a l i t y to a s e x u a l i t y a n d v i c e versa. T h e s e l a r g e r m u t a t i o n s ' c h a n g e t h e r u l e s o f t h e g a m e ' b u t t h e y a r e still, i n v a r i o u s senses, s u b j e c t t o n a t u r a l s e l e c t i o n . I n t r a g e n o m i c s e l e c t i o n for selfish D N A b e l o n g s i n t h e list o f u n c o n v e n t i o n a l t y p e s o f s e l e c t i o n , n o t i n v o l v i n g c h o i c e a m o n g alleles at a discrete locus. Selfish D N A i s s e l e c t e d for its p o w e r t o s p r e a d ' l a t e r a l l y ' , t o g e t i t s e l f duplicated into n e w loci elsewhere in the g e n o m e . It does not spread at the e x p e n s e o f a p a r t i c u l a r set o f a l l e l e s ,
in the w a y that,
say,
a g e n e for
m e l a n i s m i n m o t h s s p r e a d s i n i n d u s t r i a l a r e a s a t t h e e x p e n s e o f its a l l e l e s a t
Selfish D N A , J u m p i n g G e n e s , and a L a m a r c k i a n Scare
the s a m e locus.
It is this t h a t d i s t i n g u i s h e s it,
as a ' l a t e r a l l y s p r e a d i n g
o u t l a w ' , from the 'allelic o u t l a w s ' w h i c h w e r e the subject of the previous c h a p t e r . L a t e r a l s p r e a d i n g to n e w loci is like the spread of a virus through a p o p u l a t i o n , or like the spread of c a n c e r cells t h r o u g h a b o d y . O r g e l and C r i c k i n d e e d refer t o t h e s p r e a d i n g o f f u n c t i o n l e s s r e p l i c a t o r s a s a ' c a n c e r o f the g e n o m e ' . A s for t h e q u a l i t i e s w h i c h a r e a c t u a l l y l i k e l y t o b e f a v o u r e d i n the s e l e c t i o n o f selfish D N A , I w o u l d h a v e t o b e a m o l e c u l a r b i o l o g i s t i n o r d e r t o p r e d i c t them in detail. O n e does not h a v e to be a molecular biologist, however, to s u r m i s e t h a t t h e y m i g h t b e classified i n t o t w o m a i n c l a s s e s : q u a l i t i e s t h a t m a k e for e a s e o f d u p l i c a t i o n
and
insertion,
and
qualities
that
make
it
difficult for d e f e n c e m e c h a n i s m s o f t h e c e l l t o seek t h e m o u t a n d d e s t r o y t h e m . J u s t a s a c u c k o o e g g seeks p r o t e c t i o n b y m i m i c k i n g the host e g g s w h i c h l e g i t i m a t e l y i n h a b i t t h e nest, s o selfish D N A m i g h t e v o l v e m i m e t i c q u a l i t i e s t h a t ' m a k e i t m o r e l i k e o r d i n a r y D N A a n d so, p e r h a p s , less e a s y t o r e m o v e ' ( O r g e l & C r i c k ) . J u s t a s a full u n d e r s t a n d i n g o f c u c k o o a d a p t a t i o n s is l i k e l y to r e q u i r e a k n o w l e d g e of t h e p e r c e p t u a l s y s t e m s of hosts, so a full a p p r e c i a t i o n o f t h e d e t a i l s o f selfish D N A a d a p t a t i o n s w i l l r e q u i r e d e t a i l e d knowledge of exactly how D N A polymerase works, exactly how snipping and s p l i c i n g o c c u r , e x a c t l y w h a t g o e s o n i n m o l e c u l a r ' p r o o f - r e a d i n g ' . W h i l e full k n o w l e d g e o f t h e s e m a t t e r s c a n o n l y c o m e f r o m d e t a i l e d r e s e a r c h w o r k o f the k i n d t h a t m o l e c u l a r b i o l o g i s t s h a v e s o b r i l l i a n t l y s u c c e e d e d i n b e f o r e , i t is, perhaps, not too m u c h to h o p e that m o l e c u l a r biologists m i g h t be aided in t h e i r r e s e a r c h b y t h e r e a l i z a t i o n t h a t D N A i s n o t w o r k i n g for t h e g o o d o f the c e l l b u t for t h e g o o d o f itself. T h e m a c h i n e r y o f r e p l i c a t i o n , s p l i c i n g , a n d p r o o f - r e a d i n g m a y b e b e t t e r u n d e r s t o o d i f i t i s s e e n a s i n p a r t the p r o d u c t o f a ruthless a r m s r a c e . T h e point m a y be e m p h a s i z e d w i t h the aid of an analogy. I m a g i n e t h a t M a r s i s a U t o p i a i n w h i c h t h e r e i s c o m p l e t e trust, t o t a l h a r m o n y , n o selfishness a n d n o d e c e i t . N o w i m a g i n e a scientist f r o m M a r s t r y i n g t o m a k e s e n s e o f h u m a n life a n d t e c h n o l o g y . S u p p o s e h e s t u d i e d o n e o f o u r l a r g e d a t a p r o c e s s i n g c e n t r e s — a n e l e c t r o n i c c o m p u t e r w i t h its a s s o c i a t e d machinery
of duplication,
assumption—natural designed
for
the
to
editing
his
common
own
and
error-correction.
society—that
good,
he
would
the go
If he
machinery a
long
made had
way
the been
towards
u n d e r s t a n d i n g it. E r r o r - c o r r e c t i n g d e v i c e s , for i n s t a n c e , w o u l d c l e a r l y b e designed
to
combat
the
inevitable
and
non-malevolent
Second
L a w of
T h e r m o d y n a m i c s . But certain aspects w o u l d remain p u z z l i n g . H e would m a k e n o sense o f the e l a b o r a t e a n d costly systems o f security a n d p r o t e c t i o n : secret passwords a n d c o d e n u m b e r s that h a v e to be typed in by c o m p u t e r users. If o u r M a r t i a n e x a m i n e d a military electronic c o m m u n i c a t i o n system h e m i g h t d i a g n o s e its p u r p o s e a s t h e r a p i d a n d efficient t r a n s m i s s i o n o f useful i n f o r m a t i o n , a n d h e m i g h t t h e r e f o r e b e baffled b y t h e t r o u b l e a n d e x p e n s e t o
Selfish D N A , J u m p i n g G e n e s , a n d a L a m a r c k i a n S c a r e
163
w h i c h t h e s y s t e m s e e m s t o g o i n o r d e r t o e n c o d e its m e s s a g e s i n a w a y w h i c h i s o b s c u r e a n d h a r d t o d e c o d e . I s this n o t w a n t o n a n d a b s u r d i n e f f i c i e n c y ? B r o u g h t up as he is in a trusting U t o p i a , it m i g h t require a m a j o r flash of r e v o l u t i o n a r y i n s i g h t for o u r M a r t i a n t o see t h a t m u c h o f h u m a n t e c h n o l o g y o n l y m a k e s sense w h e n y o u r e a l i z e t h a t h u m a n s distrust e a c h o t h e r , t h a t s o m e h u m a n s w o r k a g a i n s t the best i n t e r e s t s o f o t h e r h u m a n s . T h e r e i s a s t r u g g l e b e t w e e n those w h o w i s h t o o b t a i n i l l i c i t i n f o r m a t i o n f r o m a c o m m u n i c a t i o n s y s t e m a n d those w h o w i s h t o w i t h h o l d t h a t i n f o r m a t i o n f r o m t h e m . M u c h o f h u m a n t e c h n o l o g y is the p r o d u c t of arms races a n d c a n o n l y be u n d e r s t o o d in those t e r m s . S p e c t a c u l a r as their a c h i e v e m e n t s h a v e been, is it possible that m o l e c u l a r biologists h a v e hitherto, like biologists at other levels, b e e n in s o m e t h i n g like the p o s i t i o n o f o u r M a r t i a n ? B y a s s u m i n g t h a t t h e c e l l i s a p l a c e w h e r e m o l e c u l a r m a c h i n e r y w h i r r s for the g o o d o f t h e o r g a n i s m , t h e y h a v e c o m e a long w a y . T h e y m a y g o further i f they n o w c u l t i v a t e a m o r e c y n i c a l v i e w a n d c o u n t e n a n c e the p o s s i b i l i t y t h a t s o m e m o l e c u l e s m a y b e u p t o n o g o o d f r o m the p o i n t o f v i e w o f t h e rest. O b v i o u s l y t h e y a l r e a d y d o this w h e n t h e y contemplate viruses and other i n v a d i n g parasites. A l l that is n e e d e d is to t u r n the s a m e c y n i c a l e y e o n t h e c e l l ' s ' o w n ' D N A . I t i s b e c a u s e t h e y a r e s t a r t i n g t o d o j u s t this t h a t I f i n d t h e p a p e r s o f D o o l i t t l e a n d S a p i e n z a a n d O r g e l and C r i c k so exciting, in comparison w i t h the objections of C a v a l i e r S m i t h (1980), D o v e r (1980) a n d others, a l t h o u g h o f course the objectors m a y be right in
the
particular detailed
points
they make.
Orgel
and
Crick
s u m m a r i z e the message w e l l :
I n s h o r t , w e m a y e x p e c t a k i n d o f m o l e c u l a r s t r u g g l e for e x i s t e n c e w i t h i n the D N A o f the c h r o m o s o m e s , using the process o f n a t u r a l s e l e c t i o n . T h e r e i s n o r e a s o n t o b e l i e v e t h a t this i s l i k e l y t o b e m u c h simpler or more easy to predict than evolution at a n y other level. At b o t t o m , t h e e x i s t e n c e o f selfish D N A i s p o s s i b l e b e c a u s e D N A i s a m o l e c u l e w h i c h i s r e p l i c a t e d v e r y e a s i l y a n d b e c a u s e selfish D N A occurs in an environment in w h i c h D N A replication is a necessity. It thus has the o p p o r t u n i t y of s u b v e r t i n g these essential m e c h a n i s m s to its o w n p u r p o s e . I n w h a t sense i s selfish D N A a n o u t l a w ? I t i s a n o u t l a w t o t h e e x t e n t t h a t organisms
would
be
b e t t e r off w i t h o u t it.
Perhaps
it
wastes
space
and
molecular raw materials, perhaps it wastefully consumes v a l u a b l e running t i m e o n the d u p l i c a t i n g a n d p r o o f r e a d i n g m a c h i n e r y . I n a n y e v e n t w e m a y e x p e c t t h a t s e l e c t i o n w i l l t e n d t o e l i m i n a t e selfish D N A f r o m t h e g e n o m e . W e m a y d i s t i n g u i s h t w o k i n d s o f 'anti-selfish D N A ' s e l e c t i o n . F i r s t l y , s e l e c t i o n might favour positive adaptations
t o rid o r g a n i s m s o f selfish D N A .
For
e x a m p l e , the a l r e a d y discovered proofreading p r i n c i p l e m i g h t b e e x t e n d e d .
Selfish D N A , J u m p i n g G e n e s , a n d a L a m a r c k i a n Scare
L o n g s e q u e n c e s m i g h t b e e x a m i n e d for ' s e n s e ' a n d e x c i s e d i f f o u n d w a n t i n g . I n p a r t i c u l a r , h i g h l y r e p e t i t i v e D N A m i g h t b e r e c o g n i z e d b y its statistical uniformity. T h e s e positive adaptations are w h a t I had in mind in my above d i s c u s s i o n o f a r m s r a c e s , ' m i m i c r y ' , e t c . W e a r e t a l k i n g , h e r e , a b o u t the e v o l u t i o n o f anti-selfish D N A m a c h i n e r y w h i c h c o u l d b e a s e l a b o r a t e and a s s p e c i a l i z e d a s t h e a n t i p r e d a t o r a d a p t a t i o n s o f insects. T h e r e is, h o w e v e r , a s e c o n d k i n d o f s e l e c t i o n t h a t c o u l d a c t a g a i n s t selfish D N A , w h i c h i s m u c h simpler and cruder. A n y organism that h a p p e n e d t o e x p e r i e n c e a r a n d o m d e l e t i o n o f p a r t o f its selfish D N A w o u l d , b y d e f i n i t i o n , be a m u t a n t o r g a n i s m . T h e deletion itself w o u l d be a m u t a t i o n , a n d it w o u l d b e f a v o u r e d b y n a t u r a l s e l e c t i o n t o t h e e x t e n t t h a t o r g a n i s m s possessing i t benefited from wastage
it,
of space,
p r e s u m a b l y because they did materials
and
time
n o t suffer t h e e c o n o m i c
t h a t selfish
D N A brings.
Mutant
o r g a n i s m s w o u l d , o t h e r things b e i n g e q u a l , r e p r o d u c e at a h i g h e r rate than the
loaded
down
'wild-type'
individuals,
and
the
deletion
would
con-
s e q u e n t l y b e c o m e m o r e c o m m o n in the g e n e pool. N o t e that I am not n o w t a l k i n g a b o u t s e l e c t i o n i n f a v o u r o f t h e capacity t o d e l e t e selfish D N A : t h a t w a s t h e s u b j e c t o f t h e p r e v i o u s p a r a g r a p h . H e r e w e a r e r e c o g n i z i n g t h a t the d e l e t i o n itself, t h e absence of t h e selfish D N A , is itself a r e p l i c a t i n g e n t i t y (a replicating absence!), w h i c h can be favoured by selection. It is t e m p t i n g to include under the h e a d i n g of outlaws somatic mutations that c a u s e cells to o u t - r e p r o d u c e the n o n - m u t a n t cells of a b o d y , to the u l t i m a t e d e t r i m e n t o f t h e b o d y itself. B u t a l t h o u g h t h e r e i s a k i n d o f q u a s i D a r w i n i a n s e l e c t i o n t h a t c a n g o o n i n c a n c e r t u m o u r s , a n d C a i r n s ( 1 9 7 5 ) has ingeniously d r a w n attention to w h a t appear to be bodily adaptations to forestall s u c h w i t h i n - b o d y selection, I think that to a p p l y the o u t l a w c o n c e p t h e r e w o u l d n o t b e h e l p f u l . N o t , t h a t i s t o s a y , u n l e s s the m u t a n t g e n e s concerned
somehow
manage
to
propagate
themselves
indefinitely.
They
c o u l d d o this e i t h e r b y g e t t i n g t h e m s e l v e s t r a n s p o r t e d i n v i r u s - l i k e v e c t o r s , say t h r o u g h the air, or by s o m e h o w b u r r o w i n g into the n u c l e a r germ-line. In either of these t w o cases they w o u l d qualify as ' g e r m - l i n e replicators' as d e f i n e d i n C h a p t e r 5 a n d t h e title o f o u t l a w w o u l d b e a p p r o p r i a t e . There
has
been
one
startling recent
suggestion
that genes w h i c h
are
b e n e f i c i a r i e s o f s o m a t i c s e l e c t i o n m i g h t i n d e e d b u r r o w i n t o the g e r m - l i n e , t h o u g h i n this c a s e t h e y a r e n o t c a n c e r o u s a n d n o t n e c e s s a r i l y o u t l a w s . I w a n t t o m e n t i o n this w o r k b e c a u s e i t h a s b e e n g i v e n p u b l i c i t y a s a w o u l d - b e resuscitator of the so-called
' L a m a r c k i a n ' theory of evolution.
S i n c e the
t h e o r e t i c a l p o s i t i o n a d o p t e d i n this b o o k i s f a i r l y d e s c r i b a b l e a s ' e x t r e m e Weismannism',
I a m b o u n d t o see a n y s e r i o u s r e v i v a l o f L a m a r c k i s m a s
u n d e r m i n i n g m y p o s i t i o n . I t i s t h e r e f o r e n e c e s s a r y t o discuss it.
A L a m a r c k i a n scare I use t h e w o r d ' s c a r e ' b e c a u s e , t o b e p a i n f u l l y h o n e s t , I c a n t h i n k o f few
Selfish D N A , J u m p i n g G e n e s , and a L a m a r c k i a n S c a r e
165
things t h a t w o u l d m o r e d e v a s t a t e m y w o r l d v i e w t h a n a d e m o n s t r a t e d n e e d to
return
to
the
theory
of evolution
that
is
traditionally
attributed
to
L a m a r c k . I t i s o n e o f t h e f e w c o n t i n g e n c i e s for w h i c h I m i g h t offer t o e a t m y h a t . It is t h e r e f o r e all t h e m o r e i m p o r t a n t to g i v e a full a n d fair h e a r i n g to some claims m a d e on b e h a l f of Steele (1979) (1980,
1981). Before Steele's (1979)
and Gorczynski and Steele
book w a s available in Britain,
The
Sunday Times o f L o n d o n ( 1 3 J u l y 1980) p r i n t e d a f u l l - p a g e a r t i c l e a b o u t his ideas and 'astonishing e x p e r i m e n t w h i c h seems t o c h a l l e n g e D a r w i n i s m a n d r e s u r r e c t L a m a r c k ' . T h e B B C h a v e g i v e n t h e results s i m i l a r p u b l i c i t y , i n a t least t w o t e l e v i s i o n p r o g r a m m e s a n d s e v e r a l r a d i o p r o g r a m m e s : a s w e h a v e a l r e a d y seen, ' s c i e n t i f i c ' j o u r n a l i s t s a r e c o n s t a n t l y o n t h e a l e r t for a n y t h i n g that s o u n d s l i k e a c h a l l e n g e t o D a r w i n . N o less a s c i e n t i s t t h a n S i r P e t e r M e d a w a r forced us to take Steele's w o r k seriously by d o i n g so himself. He was quoted as b e i n g properly cautious a b o u t the need to repeat the w o r k , and as c o n c l u d i n g : 'I h a v e no i d e a w h a t the o u t c o m e w i l l be, b u t I h o p e S t e e l e is r i g h t '
(The Sunday
Times).
N a t u r a l l y a n y scientist h o p e s t h a t t h e t r u t h , w h a t e v e r i t is, w i l l o u t . B u t a scientist i s also e n t i t l e d t o his i n n e r m o s t h o p e s a s t o w h a t t h a t t r u t h w i l l t u r n out to b e — a revolution in one's head is b o u n d to be a painful e x p e r i e n c e — a n d I confess t h a t m y o w n h o p e s d i d n o t i n i t i a l l y c o i n c i d e w i t h S i r P e t e r ' s ! I h a d m y d o u b t s a b o u t w h e t h e r his c o u l d r e a l l y c o i n c i d e w i t h t h o s e a t t r i b u t e d t o h i m , u n t i l I r e c a l l e d his, t o m e a l w a y s s l i g h t l y p u z z l i n g (see p a g e 2 2 ) , r e m a r k t h a t ' T h e m a i n w e a k n e s s o f m o d e r n e v o l u t i o n a r y t h e o r y i s its l a c k o f a fully w o r k e d o u t t h e o r y o f v a r i a t i o n , t h a t is, o f candidature for e v o l u t i o n , o f the f o r m i n w h i c h g e n e t i c v a r i a n t s a r e p r o f f e r e d for s e l e c t i o n .
We have
therefore n o c o n v i n c i n g a c c o u n t o f e v o l u t i o n a r y p r o g r e s s — o f the o t h e r w i s e inexplicable tendency of organisms to adopt ever more c o m p l i c a t e d solutions o f the p r o b l e m s o f r e m a i n i n g a l i v e ' ( M e d a w a r 1 9 6 7 ) . M e d a w a r i s o n e o f those w h o h a v e , m o r e r e c e n t l y , t r i e d v e r y h a r d , a n d y e t f a i l e d , t o r e p l i c a t e S t e e l e ' s f i n d i n g s ( B r e n t et al. 1 9 8 1 ) . T o a n t i c i p a t e t h e c o n c l u s i o n I s h a l l c o m e to, I n o w v i e w w i t h e q u a n i m i t y , if w i t h d w i n d l i n g e x p e c t a t i o n ( B r e n t et al. 1 9 8 1 ; M c L a r e n et al. 1 9 8 1 ) , t h e prospect of Steele's theory being upheld, because I n o w realize that, in the d e e p e s t a n d fullest sense, it is a D a r w i n i a n t h e o r y ; a v a r i e t y of D a r w i n i a n theory m o r e o v e r w h i c h , like the theory of j u m p i n g genes, is p a r t i c u l a r l y c o n g e n i a l to t h e thesis of this b o o k , s i n c e it stresses s e l e c t i o n at a l e v e l o t h e r than t h a t o f t h e i n d i v i d u a l o r g a n i s m . T h o u g h p a r d o n a b l e , t h e c l a i m t h a t i t challenges D a r w i n i s m turns out to be j u s t a journalistic g l o a t ,
provided
D a r w i n i s m is understood in the w a y that I think it o u g h t to be understood. A s for S t e e l e ' s t h e o r y itself, e v e n i f the facts d o n o t u p h o l d it, i t w i l l h a v e done us the v a l u a b l e service of forcing us to shar pen o u r p e r c e p t i o n of D a r w i n i s m . I am not qualified to e v a l u a t e the t e c h n i c a l details of Steele's e x p e r i m e n t s a n d those o f his c r i t i c s ( a g o o d e v a l u a t i o n i s g i v e n b y H o w a r d
Selfish D N A , J u m p i n g G e n e s , and a L a m a r c k i a n Scare
166
1981), a n d w i l l c o n c e n t r a t e o n d i s c u s s i n g t h e i m p a c t o f his t h e o r y , s h o u l d t h e facts e v e n t u a l l y p r o v e t o s u p p o r t it. Steele
forges
a
threefold
union
of Burnet's
(1969)
theory
of clonal
s e l e c t i o n , T e m i n ' s ( 1 9 7 4 ) p r o v i r u s t h e o r y , a n d his o w n a t t a c k o n the s a n c t i t y o f W e i s m a n n ' s g e r m - l i n e . F r o m B u r n e t h e gets the idea o f somatic mutation l e a d i n g to g e n e t i c diversity a m o n g the cells of the b o d y . N a t u r a l selection w i t h i n t h e b o d y t h e n sees t o i t t h a t t h e b o d y b e c o m e s p o p u l a t e d b y successful v a r i e t i e s o f c e l l s a t t h e e x p e n s e o f u n s u c c e s s f u l v a r i e t i e s . B u r n e t limits the i d e a t o a s p e c i a l class o f c e l l s w i t h i n t h e i m m u n e s y s t e m , a n d ' s u c c e s s ' m e a n s success in n e u t r a l i z i n g i n v a d i n g antigens, but Steele w o u l d generalize it to other cells.
From Temin
he gets
the idea of R N A viruses serving as
i n t e r c e l l u l a r m e s s e n g e r s , t r a n s c r i b i n g g e n e s i n o n e c e l l , c a r r y i n g the i n f o r m a tion to a n o t h e r cell a n d reverse-transcribing it b a c k into D N A in the second cell using reverse transcriptase. S t e e l e uses t h e T e m i n t h e o r y , b u t w i t h a n i m p o r t a n t a d d i t i o n a l e m p h a s i s o n germ-line c e l l s a s r e c i p i e n t s o f r e v e r s e - t r a n s c r i b e d g e n e t i c i n f o r m a t i o n . H e w i s e l y l i m i t s m o s t o f his d i s c u s s i o n t o t h e i m m u n e s y s t e m , a l t h o u g h his a m b i t i o n s for his t h e o r y a r e l a r g e r . H e c i t e s f o u r s t u d i e s o n ' i d i o t y p y ' i n the rabbit.
If injected
with
a foreign substance,
different
individual
rabbits
c o m b a t it by m a k i n g different antibodies. E v e n if m e m b e r s of a genetically identical clone are subjected to the same antigen, each individual responds w i t h its o w n u n i q u e ' i d i o t y p e ' . N o w , i f t h e r a b b i t s r e a l l y a r e g e n e t i c a l l y identical, the difference in their idiotypes must be due to environmental or c h a n c e differences, a n d should not, a c c o r d i n g to o r t h o d o x y , be inherited. Of the four studies cited, o n e g a v e a surprising result. T h e i d i o t y p e of a rabbit t u r n e d o u t t o b e i n h e r i t e d b y its c h i l d r e n , a l t h o u g h n o t s h a r e d b y its c l o n e m a t e s . S t e e l e stresses t h e f a c t t h a t i n this s t u d y t h e p a r e n t r a b b i t s w e r e e x p o s e d t o t h e a n t i g e n before m a t i n g t o p r o d u c e t h e o f f s p r i n g . I n t h e o t h e r t h r e e s t u d i e s t h e p a r e n t s w e r e i n j e c t e d w i t h a n t i g e n after m a t i n g , a n d the offspring did not inherit their idiotypes. If i d i o t y p e w e r e inherited as a part of a n i n v i o l a t e g e r m - p l a s m , i t s h o u l d n o t h a v e m a d e a n y d i f f e r e n c e w h e t h e r the r a b b i t s m a t e d b e f o r e o r after i n j e c t i o n . Steele's interpretation begins w i t h the B u r n e t theory. S o m a t i c mutation generates
genetic
diversity
in
the
population
of i m m u n e
cells.
Clonal
s e l e c t i o n f a v o u r s t h o s e g e n e t i c v a r i e t i e s o f c e l l t h a t s a t i s f a c t o r i l y d e s t r o y the antigen, and they b e c o m e v e r y numerous. T h e r e is m o r e than one solution to a n y a n t i g e n i c p r o b l e m , a n d t h e e n d result o f t h e s e l e c t i o n p r o c e s s i s different i n e v e r y r a b b i t . N o w T e m i n ' s p r o v i r u s e s s t e p in. T h e y t r a n s c r i b e a r a n d o m s a m p l e o f t h e g e n e s i n t h e i m m u n e c e l l s . B e c a u s e c e l l s c a r r y i n g successful a n t i b o d y g e n e s o u t n u m b e r t h e o t h e r s , t h e s e successful g e n e s a r e s t a t i s t i c a l l y m o s t l i k e l y t o b e t r a n s c r i b e d . T h e p r o v i r u s e s c a r t t h e s e g e n e s off t o t h e g e r m cells,
burrow
into
the
germ-line
chromosomes
and
leave
them
there,
p r e s u m a b l y s n i p p i n g o u t t h e i n c u m b e n t o c c u p a n t s o f the l o c u s a s t h e y d o so.
Selfish D N A , J u m p i n g G e n e s , and a L a m a r c k i a n S c a r e
167
T h e next generation of rabbits is thereby a b l e to benefit directly from the i m m u n o l o g i c a l e x p e r i e n c e o f its p a r e n t s , w i t h o u t h a v i n g t o e x p e r i e n c e t h e relevant antigens themselves, a n d w i t h o u t the painfully slow a n d wasteful intervention of selective organism death. T h e r e a l l y i m p r e s s i v e e v i d e n c e o n l y b e c a m e a v a i l a b l e after S t e e l e ' s t h e o r y was cut and dried and published, a striking and rather surprising instance of science p r o c e e d i n g in the w a y philosophers think it p r o c e e d s . G o r c z y n s k i a n d Steele
(1980)
investigated
the
inheritance,
via
the
father,
of i m m u n e
tolerance in mice.
U s i n g an e x t r e m e l y h i g h - d o s a g e version of the classic
M e d a w a r method,
they e x p o s e d b a b y m i c e t o cells from a n o t h e r strain,
thereby r e n d e r i n g t h e m tolerant as adults to s u b s e q u e n t grafts from the s a m e d o n o r strain. T h e y then bred from these tolerant m a l e s , a n d c o n c l u d e d that their tolerance w a s inherited b y a b o u t h a l f their c h i l d r e n , w h o w e r e n o t e x p o s e d a s i n f a n t s t o t h e f o r e i g n a n t i g e n s . F u r t h e r m o r e , t h e effect s e e m e d t o carry over to the g r a n d c h i l d g e n e r a t i o n . Subject
to
inheritance
confirmation,
of
acquired
we
have
here
characteristics.
a
prima-facie
Gorczynski
and
case
for
Steele's
the brief
discussion o f their e x p e r i m e n t , a n d o f e x t e n d e d e x p e r i m e n t s r e p o r t e d m o r e recently ( G o r c z y n s k i & Steele 1 9 8 1 ) , resembles Steele's interpretation of the rabbit w o r k , p a r a p h r a s e d a b o v e . T h e m a i n differences b e t w e e n the t w o cases are firstly
that
the
rabbits
could
have
inherited
something
in
maternal
cytoplasm w h i l e the m i c e c o u l d not; a n d s e c o n d l y that the rabbits w e r e alleged to h a v e inherited an acquired i m m u n i t y , w h i l e the m i c e are supposed to have inherited
an acquired
tolerance.
T h e s e differences are p r o b a b l y
i m p o r t a n t ( R i d l e y 1 9 8 0 b ; B r e n t e t al. 1 9 8 1 ) , b u t I s h a l l n o t m a k e m u c h o f them,
since
themselves.
I
am
not
attempting
to
evaluate
the
experimental
results
I shall c o n c e n t r a t e on the question of w h e t h e r , in a n y case,
Steele is really offering 'a L a m a r c k i a n c h a l l e n g e to D a r w i n i s m ' . There
are
some
historical
points
to
get
out
of the
way
first.
The
i n h e r i t a n c e o f a c q u i r e d c h a r a c t e r i s t i c s i s n o t t h e a s p e c t o f his t h e o r y t h a t L a m a r c k h i m s e l f e m p h a s i z e d a n d , contra S t e e l e ( 1 9 7 9 , p . 6 ) , i t i s n o t t r u e t h a t the i d e a o r i g i n a t e d w i t h h i m : h e s i m p l y t o o k o v e r t h e c o n v e n t i o n a l w i s d o m o f his t i m e a n d g r a f t e d t o i t o t h e r p r i n c i p l e s l i k e ' s t r i v i n g ' a n d ' u s e a n d disuse'. Steele's viruses seem m o r e reminiscent of D a r w i n ' s o w n p a n g e n e t i c 'gemmules' than of a n y t h i n g postulated by L a m a r c k . B u t I mention history just to get it out of the w a y . We g i v e the n a m e D a r w i n i s m to the t h e o r y that undirected variation in an insulated germ-line is acted upon by selection of its p h e n o t y p i c c o n s e q u e n c e s . W e g i v e t h e n a m e L a m a r c k i s m t o t h e t h e o r y that the g e r m - l i n e is not insulated, improvements
may
directly
mould
and it.
In
that this
environmentally sense,
is
imprinted
Steele's
theory
Lamarckian and anti-Darwinian? By inheriting their parents' a c q u i r e d idiotypes, rabbits w o u l d u n d o u b t e d l y benefit. T h e y w o u l d b e g i n life w i t h a h e a d start i n t h e i m m u n o l o g i c a l b a t t l e
168
Selfish D N A , J u m p i n g G e n e s , and a L a m a r c k i a n Scare
against p l a g u e s that their parents met, a n d that they themselves are likely to meet. T h i s is a directed, a d a p t i v e c h a n g e , then. But is it really imprinted by the e n v i r o n m e n t ? If a n t i b o d y formation w o r k e d a c c o r d i n g to some kind of 'instructive' theory, the a n s w e r w o u l d be yes. T h e e n v i r o n m e n t , in the shape of
antigenic
protein
molecules,
would
than
directly
mould
antibody
m o l e c u l e s i n p a r e n t r a b b i t s . I f the o f f s p r i n g o f those r a b b i t s t u r n e d o u t t o i n h e r i t a p r e d i l e c t i o n t o m a k e t h e s a m e a n t i b o d i e s , w e w o u l d h a v e fullb l o o d e d L a m a r c k i s m . But the conformations o f the a n t i b o d y proteins w o u l d , o n this t h e o r y , s o m e h o w h a v e t o b e r e v e r s e - t r a n s l a t e d i n t o n u c l e o t i d e c o d e . Steele
(p.
36)
is
adamant
that
there is no suggestion of such
reverse
t r a n s l a t i o n , o n l y r e v e r s e transcription f r o m R N A t o D N A . H e i s not p r o p o s i n g any violation of C r i c k ' s central d o g m a , although of course others are at l i b e r t y t o d o s o ( I s h a l l r e t u r n t o this p o i n t i n a m o r e g e n e r a l c o n t e x t l a t e r ) . T h e v e r y e s s e n c e o f S t e e l e ' s h y p o t h e s i s i s t h a t the a d a p t i v e i m p r o v e m e n t comes a b o u t through selection of initially r a n d o m variation. It is about as D a r w i n i a n a theory as it is possible to be, p r o v i d e d we think of the replicator and not the organism as the unit of selection. N o r is it just v a g u e l y analogous t o D a r w i n i s m , i n t h e w a y of, s a y , t h e ' m e m e ' t h e o r y , o r P r i n g l e ' s ( 1 9 5 1 ) theory
that
frequencies
learning in
a
results
from
selection
among
of
neuronal
coupled
population
a
pool
of oscillation
oscillators.
Steele's
r e p l i c a t o r s a r e D N A m o l e c u l e s i n c e l l n u c l e i . T h e y a r e n o t j u s t analogous t o the replicators o f D a r w i n i s m . scheme
for
modification
natural to
selection
plug
T h e y are
the v e r y s a m e replicators. T h e
which
I
outlined
into
the
Steele
straight
in
Chapter
theory.
5
needs no
Steele's
kind
of
L a m a r c k i s m o n l y s e e m s l i k e t h e i m p r i n t i n g o f e n v i r o n m e n t a l f e a t u r e s o n the g e r m - l i n e if we think at the level of the i n d i v i d u a l o r g a n i s m . It is true that he i s c l a i m i n g t h a t c h a r a c t e r i s t i c s a c q u i r e d b y t h e organism a r e i n h e r i t e d . B u t i f we look at the l o w e r level of genetic replicators, it is clear that the a d a p t a t i o n c o m e s a b o u t t h r o u g h s e l e c t i o n n o t ' i n s t r u c t i o n ' (see b e l o w ) . I t j u s t h a p p e n s t o b e s e l e c t i o n w i t h i n t h e o r g a n i s m . S t e e l e ( 1 9 7 9 , p . 43) w o u l d not d i s a g r e e : ' . . . it
depends
very
much
on
essential
Darwinian
principles
of natural
selection'. Despite Steele's a v o w e d indebtedness to A r t h u r K o e s t l e r , there is naught h e r e for t h e c o m f o r t o f t h o s e , u s u a l l y n o n - b i o l o g i s t s , w h o s e a n t i p a t h y t o D a r w i n i s m i s f u n d a m e n t a l l y p r o v o k e d b y t h e b o g y o f ' b l i n d c h a n c e ' . O r , for that m a t t e r , the t w i n b o g y of a ruthlessly indifferent g r i m reaper, m o c k i n g us as the sole First C a u s e of o u r e x a l t e d persons, m o d i f y i n g 'all things by blindly s t a r v i n g a n d m u r d e r i n g e v e r y t h i n g t h a t i s n o t l u c k y e n o u g h t o s u r v i v e i n the u n i v e r s a l s t r u g g l e for h o g w a s h ' should
hear
no
triumphant
(Shaw 1921).
chuckles
from
the
If Steele proves right, we shade
of Bernard
Shaw!
S h a w ' s l i v e s p i r i t r e b e l l e d p a s s i o n a t e l y a g a i n s t the D a r w i n i a n ' c h a p t e r o f a c c i d e n t s ' . ' . . . i t s e e m s s i m p l e , b e c a u s e y o u d o n o t a t first r e a l i z e a l l t h a t i t i n v o l v e s . B u t w h e n its w h o l e s i g n i f i c a n c e d a w n s o n y o u , y o u r h e a r t sinks i n t o
Selfish D N A , J u m p i n g G e n e s , and a L a m a r c k i a n S c a r e
169
a h e a p o f s a n d w i t h i n y o u . T h e r e i s a h i d e o u s f a t a l i s m a b o u t it, a g h a s t l y a n d damnable reduction of beauty and intelligence, of strength and purpose, of honor and aspiration .. .'
I f w e must p l a c e e m o t i o n
before truth,
I
have
always found natural selection to h a v e an inspiring, if grim a n d austere, p o e t r y o f its o w n — a ' g r a n d e u r i n this v i e w o f life' ( D a r w i n 1 8 5 9 ) . A l l I a m saying here is that if y o u are squeamish a b o u t 'blind c h a n c e ' , do not look to S t e e l e ' s t h e o r y for a n e s c a p e . B u t p e r h a p s i t i s n o t t o o m u c h t o h o p e t h a t a proper understanding of Steele's theory m a y help to show that 'blind c h a n c e ' is not
the
adequate epitome of Darwinism
that
Shaw,
Cannon
(1959),
K o e s t l e r ( 1 9 6 7 ) a n d o t h e r s t h i n k i t is. Steele's
theory,
then, is a version of D a r w i n i s m . T h e cells w h i c h are
s e l e c t e d , a c c o r d i n g t o t h e B u r n e t t h e o r y , a r e v e h i c l e s for a c t i v e r e p l i c a t o r s , n a m e l y the s o m a t i c a l l y m u t a t e d g e n e s w i t h i n t h e m . T h e y a r e a c t i v e , b u t a r e t h e y germ-line r e p l i c a t o r s ? T h e e s s e n c e o f w h a t I a m s a y i n g i s t h a t t h e a n s w e r is an e m p h a t i c yes, if Steele's addition to the B u r n e t theory is true. T h e y do not b e l o n g t o w h a t w e h a v e c o n v e n t i o n a l l y t h o u g h t o f a s t h e g e r m - l i n e , b u t it is a logical i m p l i c a t i o n of the theory that we h a v e simply b e e n m i s t a k e n as t o w h a t the g e r m - l i n e t r u l y is. A n y g e n e i n a ' s o m a t i c ' c e l l w h i c h i s a c a n d i d a t e for p r o v i r a l c o n v e y a n c e i n t o a g e r m c e l l is, by definition, a g e r m - l i n e replicator. being
S t e e l e ' s b o o k m i g h t be r e t i t l e d
uncomfortable
for
neo-Weismannists,
The Extended Germ-line! F a r f r o m it
turns
out
to
be
deeply
c o n g e n i a l to us. Perhaps, then, it is not really all that ironic that, a p p a r e n t l y u n k n o w n to S t e e l e , s o m e t h i n g b e a r i n g m o r e t h a n a p a s s i n g r e s e m b l a n c e t o his t h e o r y w a s a d o p t e d b y , o f all p e o p l e , W e i s m a n n himself, i n 1 8 9 4 . T h e f o l l o w i n g a c c o u n t i s t a k e n f r o m R i d l e y (in p r e s s ; M a y n a r d S m i t h , 1 9 8 0 , a l s o n o t e d t h e p r e c e d e n t ) . W e i s m a n n d e v e l o p e d a n idea from R o u x , w h i c h h e c a l l e d 'intras e l e c t i o n ' . I q u o t e from R i d l e y : ' R o u x h a d a r g u e d t h a t t h e r e i s a s t r u g g l e for food b e t w e e n t h e p a r t s o f a n o r g a n i s m j u s t l i k e t h e s t r u g g l e for e x i s t e n c e between organisms . . .
R o u x ' s theory w a s that the struggle o f the parts,
t o g e t h e r w i t h t h e i n h e r i t a n c e o f a c q u i r e d c h a r a c t e r s , w a s sufficient t o e x p l a i n a d a p t a t i o n . ' S u b s t i t u t e ' c l o n e s ' for ' p a r t s ' , a n d y o u h a v e S t e e l e ' s t h e o r y . B u t , a s m i g h t b e e x p e c t e d , W e i s m a n n did not g o all the w a y w i t h R o u x i n p o s t u l a t i n g the l i t e r a l i n h e r i t a n c e o f a c q u i r e d c h a r a c t e r i s t i c s . I n s t e a d , i n his theory of ' g e r m i n a l selection', he i n v o k e d the p s e u d o - L a m a r c k i a n p r i n c i p l e w h i c h later b e c a m e k n o w n as the ' B a l d w i n Effect' ( W e i s m a n n w a s not the o n l y o n e t o d i s c o v e r t h e i d e a b e f o r e B a l d w i n ) . W e i s m a n n ' s use o f t h e t h e o r y o f i n t r a - s e l e c t i o n i n e x p l a i n i n g c o a d a p t a t i o n w i l l b e d e a l t w i t h b e l o w , for i t closely parallels one of Steele's o w n p r e o c c u p a t i o n s . S t e e l e d o e s n o t v e n t u r e far f r o m his o w n field o f i m m u n o l o g y , b u t h e w o u l d like a v e r s i o n o f his t h e o r y t o a p p l y e l s e w h e r e , a n d p a r t i c u l a r l y t o t h e nervous
system
and
the
adaptive
improvement
mechanism
known
as
learning. ' I f [the hypothesis] is to h a v e a n y g e n e r a l a p p l i c a b i l i t y to the
Selfish D N A , J u m p i n g G e n e s , and a L a m a r c k i a n Scare
170
e v o l u t i o n a r y a d a p t a t i o n p r o c e s s , it must account for t h e a d a p t i v e p o t e n t i a l of the n e u r o n a l n e t w o r k s of the brain a n d central nervous system' (Steele 1979, p . 4 9 , his r a t h e r s u r p r i s i n g e m p h a s i s ) . H e s e e m s a little v a g u e a s t o e x a c t l y w h a t m i g h t be selected w i t h i n the brain, a n d , in case he c a n do something w i t h it, I offer h i m a free gift o f m y o w n t h e o r y o f ' s e l e c t i v e n e u r o n e d e a t h a s a possible m e m o r y m e c h a n i s m ' ( D a w k i n s 1971). But is the t h e o r y of c l o n a l selection really likely to a p p l y outside the domain
of
the
immune
system?
Is
it
limited
by
the
very
special
c i r c u m s t a n c e s o f t h e i m m u n e s y s t e m , o r m i g h t i t b e l i n k e d u p w i t h the o l d L a m a r c k i a n p r i n c i p l e o f use a n d d i s u s e ? C o u l d c l o n a l s e l e c t i o n b e e m b r a c e d b y the b l a c k s m i t h ' s a r m s ? C o u l d the a d a p t i v e c h a n g e s b r o u g h t a b o u t b y m u s c u l a r exercise be i n h e r i t e d ? I d o u b t it very m u c h : the conditions are not r i g h t for n a t u r a l s e l e c t i o n t o w o r k w i t h i n the b l a c k s m i t h ' s a r m s i n f a v o u r of, say,
c e l l s t h a t flourish i n a n a e r o b i c e n v i r o n m e n t o v e r those p r e f e r r i n g
a n a e r o b i c b i o c h e m i s t r y , t h e successful g e n e s b e i n g r e v e r s e - t r a n s c r i b e d i n t o j u s t t h e r i g h t c h r o m o s o m a l l o c u s i n the g e r m - l i n e . B u t e v e n i f this k i n d o f t h i n g w e r e c o n c e i v a b l e for s o m e e x a m p l e o u t s i d e t h e i m m u n e s y s t e m , t h e r e i s a major theoretical difficulty. T h e p r o b l e m i s this. T h e q u a l i t i e s t h a t m a k e for s u c c e s s i n c l o n a l s e l e c t i o n w o u l d n e c e s s a r i l y b e t h o s e t h a t g i v e cells a n a d v a n t a g e o v e r r i v a l c e l l s i n the s a m e b o d y . T h e s e q u a l i t i e s n e e d h a v e n o c o n n e c t i o n w i t h w h a t i s g o o d for the b o d y as a w h o l e , a n d o u r discussion of o u t l a w s suggests that they might w e l l a c t i v e l y c o n f l i c t w i t h w h a t i s g o o d for t h e b o d y a s a w h o l e . I n d e e d , t o m e a s l i g h t l y u n s a t i s f a c t o r y a s p e c t o f t h e B u r n e t t h e o r y i t s e l f i s t h a t the s e l e c t i o n p r o c e s s at its h e a r t is c o n t r i v e d ad hoc. It is a s s u m e d t h a t those cells w h o s e a n t i b o d i e s n e u t r a l i z e i n v a d i n g antigens will p r o p a g a t e at the expense o f o t h e r c e l l s . B u t this p r o p a g a t i o n i s n o t d u e t o a n y i n t r i n s i c c e l l u l a r a d v a n t a g e : o n t h e c o n t r a r y , c e l l s t h a t d i d n o t risk t h e i r l i v e s s m o t h e r i n g a n t i g e n s b u t selfishly left t h e task t o t h e i r c o l l e a g u e s s h o u l d , o n t h e f a c e o f it, h a v e a built-in a d v a n t a g e . T h e theory has to introduce an arbitrary and u n p a r s i m o n i o u s s e l e c t i o n r u l e , i m p o s e d , a s i t w e r e , f r o m a b o v e , s o t h a t those cells w h i c h benefit the b o d y as a w h o l e b e c o m e m o r e n u m e r o u s . It is as t h o u g h a h u m a n d o g - b r e e d e r d e l i b e r a t e l y s e l e c t e d for a l t r u i s t i c h e r o i s m i n t h e f a c e o f d a n g e r . H e c o u l d p r o b a b l y a c h i e v e it, b u t natural s e l e c t i o n c o u l d not.
Unadulterated
clonal
selection
should
favour
selfish
cells
whose
b e h a v i o u r c o n f l i c t s w i t h t h e b e s t interests o f t h e b o d y a s a w h o l e . I n t h e t e r m s o f C h a p t e r 6 , w h a t I a m s a y i n g i s t h a t v e h i c l e s e l e c t i o n a t the cellular level is likely, u n d e r the B u r n e t theory, to c o m e into conflict with vehicle selection at the organism level. T h i s , of course, does not worry me, s i n c e I c a r r y n o b r i e f for t h e o r g a n i s m a s p r e - e m i n e n t v e h i c l e ; I s i m p l y a d d o n e m o r e e n t r y t o t h e list o f ' o u t l a w s I h a v e k n o w n ' ; o n e m o r e i n g e n i o u s b y w a y o f r e p l i c a t o r p r o p a g a t i o n , a l o n g w i t h j u m p i n g g e n e s a n d selfish D N A .
Selfish D N A , J u m p i n g G e n e s , a n d a L a m a r c k i a n S c a r e
171
B u t i t s h o u l d w o r r y a n y b o d y , s u c h a s S t e e l e , w h o sees c l o n a l s e l e c t i o n a s a s u p p l e m e n t a r y m e a n s b y w h i c h bodily a d a p t a t i o n s c o m e a b o u t . T h e p r o b l e m goes d e e p e r than that. It is not just that c l o n a l l y selected g e n e s w o u l d t e n d t o b e o u t l a w s a s far a s t h e rest o f t h e b o d y i s c o n c e r n e d . Steele
looks
to
clonal
selection
to
speed
up
evolution.
Conventional
D a r w i n i s m p r o c e e d s b y d i f f e r e n t i a l i n d i v i d u a l s u c c e s s , a n d its s p e e d , o t h e r things b e i n g e q u a l , will be limited by i n d i v i d u a l g e n e r a t i o n time. C l o n a l selection w o u l d be limited by cellular g e n e r a t i o n time, w h i c h is p e r h a p s t w o orders of m a g n i t u d e shorter. T h i s is w h y it m i g h t be t h o u g h t to speed up e v o l u t i o n b u t , t o a n t i c i p a t e t h e a r g u m e n t o f m y f i n a l c h a p t e r , i t raises a d e e p difficulty. T h e success of a c o m p l e x , m u l t i c e l l u l a r o r g a n , like an e y e , c a n n o t be j u d g e d in a d v a n c e of the eye's starting to w o r k . C e l l u l a r selection c o u l d n o t i m p r o v e the d e s i g n o f a n e y e , b e c a u s e t h e s e l e c t i v e e v e n t s a l l t a k e p l a c e i n the p r e f u n c t i o n a l e y e o f a n e m b r y o . T h e e m b r y o ' s e y e i s c l o s e d , a n d n e v e r sees a n i m a g e u n t i l after c e l l u l a r s e l e c t i o n , i f i t e x i s t e d , w o u l d b e c o m p l e t e . T h e general point is that cellular selection c a n n o t a c h i e v e the s p e e d i n g up of e v o l u t i o n a t t r i b u t e d t o it, i f t h e a d a p t a t i o n o f i n t e r e s t h a s t o d e v e l o p o n t h e slow scale of m u l t i c e l l u l a r c o o p e r a t i o n . Steele has a point
to m a k e about coadaptation.
As R i d l e y
(in press)
c o m p r e h e n s i v e l y d o c u m e n t s , m u l t i d i m e n s i o n a l c o a d a p t a t i o n w a s o n e o f the b u g b e a r s of the early D a r w i n i a n s . F o r instance, to take the e y e a g a i n , J. J. M u r p h y said ' I t i s p r o b a b l y n o e x a g g e r a t i o n t h a t , i n o r d e r t o i m p r o v e s u c h a n o r g a n a s t h e e y e a t a l l , i t m u s t b e i m p r o v e d i n t e n different w a y s a t o n c e ' (1866, quoted by R i d l e y ) . e v o l u t i o n of w h a l e s ,
I
I t m a y b e r e m e m b e r e d that, s p e a k i n g o f the
u s e d a s i m i l a r p r e m i s e for a different p u r p o s e in
C h a p t e r 6 . F u n d a m e n t a l i s t o r a t o r s still find the e y e o n e o f t h e i r m o s t t e l l i n g s t a n d b y s . I n c i d e n t a l l y , The Sunday Times ( 1 3 J u l y 1980) a n d The Guardian (21 N o v e m b e r 1978) both raise the d e b a t i n g point of the e y e as t h o u g h it w e r e a n e w o n e , t h e l a t t e r p a p e r r e a s s u r i n g u s t h a t a n e m i n e n t p h i l o s o p h e r (!) w a s r u m o u r e d t o b e g i v i n g t h e p r o b l e m his best a t t e n t i o n . S t e e l e s e e m s t o h a v e been
initially
coadaptation,
attracted and
he
by
Lamarckism
believes
that
his
because
clonal
of
his
selection
unease
theory
about
could
in
principle alleviate the difficulty, if difficulty there be. L e t u s m a k e use o f t h a t o t h e r c h e s t n u t o f t h e s c h o o l r o o m , t h e giraffe's n e c k , d i s c u s s i n g i t i n c o n v e n t i o n a l D a r w i n i a n t e r m s first. A m u t a t i o n t o elongate the ancestral n e c k m i g h t w o r k on, say, the v e r t e b r a e , but it seems to a
naive
observer
too
much
to
hope
that
the
same
mutation
will
simultaneously e l o n g a t e the arteries, veins, nerves, etc. A c t u a l l y , w h e t h e r it i s too m u c h t o h o p e d e p e n d s o n d e t a i l s o f e m b r y o l o g y w h i c h w e s h o u l d l e a r n t o b e m o r e a w a r e of: a m u t a t i o n t h a t a c t s s u f f i c i e n t l y e a r l y i n d e v e l o p m e n t c o u l d e a s i l y h a v e a l l those p a r a l l e l effects s i m u l t a n e o u s l y . H o w e v e r , let u s p l a y a l o n g w i t h the a r g u m e n t . T h e n e x t s t e p i s t o s a y t h a t i t i s d i f f i c u l t t o
Selfish D N A , J u m p i n g G e n e s , and a L a m a r c k i a n Scare
172
i m a g i n e a m u t a n t giraffe w i t h e l o n g a t e d v e r t e b r a e b e i n g a b l e t o e x p l o i t its t r e e t o p b r o w s i n g a d v a n t a g e , b e c a u s e its n e r v e s , b l o o d vessels, e t c . a r e t o o s h o r t for its n e c k . C o n v e n t i o n a l D a r w i n i a n s e l e c t i o n , n a i v e l y u n d e r s t o o d , h a s to w a i t
for a n
individual
that
is fortunate
enough
t o c o m b i n e all
the
necessary c o a d a p t e d mutations simultaneously. T h i s is w h e r e clonal selection c o u l d c o m e t o t h e r e s c u e . O n e m a j o r m u t a t i o n , s a y t h e e l o n g a t i o n o f the v e r t e b r a e , sets u p c o n d i t i o n s i n t h e n e c k w h i c h s e l e c t for c l o n e s o f cells t h a t c a n flourish in that e n v i r o n m e n t . M a y b e the e l o n g a t e d v e r t e b r a e p r o v i d e an o v e r s t r e t c h e d , h i g h l y strung, tense e n v i r o n m e n t in the n e c k , w h e r e only e l o n g a t e d c e l l s f l o u r i s h . I f t h e r e i s g e n e t i c v a r i a t i o n a m o n g the c e l l s , g e n e s 'for' e l o n g a t e d cells s u r v i v e a n d are passed on to the giraffe's c h i l d r e n . I h a v e put the p o i n t facetiously, but a m o r e sophisticated version of it could, I suppose, follow from the clonal selection theory. I s a i d I w o u l d r e t u r n t o W e i s m a n n a t this p o i n t , for h e t o o s a w t h e u t i l i t y of w i t h i n - b o d y
selection
as
a
solution
to
the
coadaptation
problem.
W e i s m a n n t h o u g h t that ' i n t r a - s e l e c t i o n ' — t h e selective struggle a m o n g parts w i t h i n t h e b o d y — ' w o u l d e n s u r e t h a t all t h e p a r t s i n s i d e t h e o r g a n i s m w e r e o f t h e best m u t u a l p r o p o r t i o n s ' ( R i d l e y i n p r e s s ) . ' I f I a m n o t m i s t a k e n , the phenomenon
which
Darwin
c a l l e d correlation,
and justly
regarded
as an
i m p o r t a n t f a c t o r i n e v o l u t i o n , i s for t h e m o s t p a r t a n effect o f i n t r a - s e l e c t i o n ' ( W e i s m a n n , q u o t e d in R i d l e y ) . As already stated, W e i s m a n n , unlike R o u x , did not go on to i n v o k e the direct inheritance of intra-selected varieties. Rather,
' . . . in e a c h separate i n d i v i d u a l the necessary a d a p t a t i o n will be
t e m p o r a r i l y a c c o m p l i s h e d b y intra-selection . . . T i m e w o u l d thus b e g a i n e d till, i n t h e c o u r s e o f g e n e r a t i o n s , b y c o n s t a n t s e l e c t i o n o f those g e r m s the p r i m a r y c o n s t i t u e n t s o f w h i c h a r e best s u i t e d t o o n e a n o t h e r , t h e g r e a t e s t possible d e g r e e of h a r m o n y m a y be reached.' I think I find W e i s m a n n ' s 'Baldwin
Effect'
version
of
the
theory
more
plausible
than
Steele's
L a m a r c k i a n version, a n d just as satisfying an e x p l a n a t i o n of coadaptation. I u s e d t h e w o r d ' s c a r e ' i n t h e h e a d i n g o f this s e c t i o n , a n d w e n t s o far a s t o say that a true r e v i v a l of L a m a r c k i s m w o u l d devastate my w o r l d - v i e w . Y e t t h e r e a d e r m a y n o w feel t h a t t h e s t a t e m e n t w a s a h o l l o w o n e , like t h a t o f a m a n w h o d r a m a t i c a l l y t h r e a t e n s t o e a t his h a t , w h i l e k n o w i n g full w e l l that his h a t i s m a d e o f p l e a s a n t l y f l a v o u r e d r i c e p a p e r . A L a m a r c k i a n z e a l o t m a y c o m p l a i n t h a t t h e last r e s o r t o f a D a r w i n i a n ,
h a v i n g failed
to discredit
a w k w a r d e x p e r i m e n t a l r e s u l t s , i s t o c l a i m t h e m for his o w n ; t o m a k e his o w n t h e o r y so r e s i l i e n t t h a t t h e r e is no e x p e r i m e n t a l result t h a t c o u l d falsify it. I a m s e n s i t i v e t o this c r i t i c i s m , a n d m u s t r e p l y t o it. I m u s t s h o w t h a t t h e h a t that I t h r e a t e n e d to eat really is t o u g h a n d distasteful. S o , if Steele's kind of L a m a r c k i s m is really D a r w i n i s m in disguise, w h a t kind of L a m a r c k i s m w o u l d not be? T h e k e y issue i s t h e o r i g i n o f a d a p t e d n e s s . G o u l d ( 1 9 7 9 ) m a k e s a r e l a t e d
Selfish D N A , J u m p i n g G e n e s , a n d a L a m a r c k i a n S c a r e
173
p o i n t w h e n h e s a y s t h a t t h e i n h e r i t a n c e o f a c q u i r e d c h a r a c t e r s , per se, i s n o t L a m a r c k i a n : ' L a m a r c k i s m is a t h e o r y of directed v a r i a t i o n ' ( m y e m p h a s i s ) . I d i s t i n g u i s h t w o classes o f t h e o r y o f t h e o r i g i n o f a d a p t e d n e s s . F o r f e a r o f getting c a u g h t up in historical details of exactly w h a t L a m a r c k and D a r w i n said, I shall not a n y m o r e call them L a m a r c k i s m a n d D a r w i n i s m . Instead, I shall b o r r o w from i m m u n o l o g y a n d call t h e m the instruction t h e o r y a n d the selection
theory.
As
Young
(1957),
Lorenz
(1966),
and
others
have
emphasized, we recognize adaptedness as an informational match between organism
and
environment
environment. can
be
An
regarded
animal as
that
is
embodying
well
adapted
information
to
its
about
its
e n v i r o n m e n t , in the w a y that a k e y e m b o d i e s information a b o u t the lock that it is built to u n d o . A c a m o u f l a g e d a n i m a l has b e e n said to c a r r y a p i c t u r e of its e n v i r o n m e n t o n its b a c k . L o r e n z d i s t i n g u i s h e d t w o k i n d s o f t h e o r y for t h e o r i g i n o f this k i n d o f f i t b e t w e e n o r g a n i s m a n d e n v i r o n m e n t , b u t b o t h his t h e o r i e s ( n a t u r a l s e l e c t i o n and reinforcement
learning)
are subdivisions of w h a t
selection theory. An initial pool of variation taneous
behaviour)
is worked
upon
I
am
calling the
(genetic mutation or spon-
by some
kind
of selection
process
(natural selection or r e w a r d / p u n i s h m e n t ) , w i t h the end result that o n l y the variants f i t t i n g the e n v i r o n m e n t a l lock r e m a i n . T h u s a d a p t e d n e s s i m p r o v e s by selection. T h e instruction theory is q u i t e different. W h e r e a s the selective k e y - m a k e r b e g i n s w i t h a l a r g e r a n d o m p o o l o f k e y s , tries t h e m a l l i n t h e l o c k , and discards those that d o n ' t fit, the instructive k e y - m a k e r s i m p l y takes a wax
impression
o f the
lock,
instructively camouflaged
and
makes
up
a
good
key directly.
The
a n i m a l r e s e m b l e s its e n v i r o n m e n t b e c a u s e t h e
e n v i r o n m e n t d i r e c t l y i m p r i n t s its a p p e a r a n c e o n t h e a n i m a l , a s e l e p h a n t s m e r g e i n t o t h e b a c k g r o u n d b e c a u s e t h e y a r e c o v e r e d b y its d u s t . I t h a s b e e n alleged that French mouths eventually b e c o m e p e r m a n e n t l y deformed into a s h a p e s u i t a b l e for p r o n o u n c i n g F r e n c h v o w e l s . I f so, this w o u l d b e a n i n s t r u c tive a d a p t a t i o n . S o , perhaps, is b a c k g r o u n d r e s e m b l a n c e in c h a m e l e o n s , t h o u g h o f c o u r s e t h e capacity t o c h a n g e c o l o u r a d a p t i v e l y i s p r e s u m a b l y a selective adaptation. T h e a d a p t i v e changes in p h y s i o l o g y to w h i c h we g i v e n a m e s like a c c l i m a t i z a t i o n a n d t r a i n i n g , t h e effects o f e x e r c i s e , u s e a n d d i s u s e , are p r o b a b l y all instructive. C o m p l e x a n d e l a b o r a t e a d a p t i v e f i t s c a n b e a c h i e v e d b y i n s t r u c t i o n , a s i n the l e a r n i n g o f a p a r t i c u l a r h u m a n l a n g u a g e . As already explained, it is clear that in Steele's theory the adaptedness c o m e s not from instruction b u t from selection, a n d g e n e t i c r e p l i c a t o r selection at that.
My world-view will
genetic
inheritance,
be overturned if somebody demonstrates
not just
of an
'acquired
characteristic'
but
the
of an
instructively acquired adaptation. T h e reason is that the inheritance of an instructively embryology.
acquired
adaptation would
violate
the
'central
dogma'
of
174
Selfish D N A , J u m p i n g G e n e s , and a L a m a r c k i a n Scare
The poverty of preformationism O d d l y , my b e l i e f in the i n v i o l a b i l i t y of the central d o g m a is not a d o g m a t i c o n e ! I t i s b a s e d o n r e a s o n . I m u s t b e c a u t i o u s h e r e , a n d d i s t i n g u i s h t w o forms o f c e n t r a l d o g m a , the central d o g m a o f m o l e c u l a r genetics and the central dogma
of embryology.
The
first
is
the
one
stated
by
Crick:
genetic
i n f o r m a t i o n m a y b e t r a n s l a t e d f r o m n u c l e i c a c i d t o p r o t e i n , b u t n o t the o t h e r w a y . S t e e l e ' s t h e o r y , a s h e h i m s e l f i s c a r e f u l t o p o i n t o u t , d o e s n o t v i o l a t e this d o g m a . H e m a k e s use o f r e v e r s e t r a n s c r i p t i o n f r o m R N A t o D N A , b u t n o t reverse translation from protein to R N A . I am not a m o l e c u l a r biologist, and so c a n n o t j u d g e the extent to w h i c h the theoretical b o a t w o u l d be rocked if such reverse
translation were
ever discovered.
It
does
not seem
to me
o b v i o u s l y i m p o s s i b l e i n p r i n c i p l e , b e c a u s e the t r a n s l a t i o n f r o m n u c l e i c a c i d to protein, or from protein to nucleic acid, is a simple dictionary look-up procedure, only slightly more c o m p l e x than the D N A / R N A transcription. In b o t h cases there is a o n e - t o - o n e m a p p i n g b e t w e e n the t w o codes. If a h u m a n , or a c o m p u t e r , e q u i p p e d w i t h the d i c t i o n a r y , c a n translate from protein to R N A , I d o n ' t see w h y n a t u r e s h o u l d n o t . T h e r e m a y b e a g o o d t h e o r e t i c a l r e a s o n , o r i t m a y just b e a n e m p i r i c a l l a w t h a t has n o t y e t b e e n v i o l a t e d . T h e r e i s n o n e e d for m e t o p u r s u e t h e m a t t e r b e c a u s e , i n a n y c a s e , a v e r y g o o d t h e o r e t i c a l c a s e c a n b e m a d e a g a i n s t v i o l a t i n g t h e o t h e r c e n t r a l d o g m a , the c e n t r a l d o g m a o f e m b r y o l o g y . T h i s i s t h e d o g m a t h a t the m a c r o s c o p i c form a n d b e h a v i o u r o f a n o r g a n i s m m a y b e , i n s o m e sense, c o d e d i n t h e g e n e s , b u t t h e c o d e i s i r r e v e r s i b l e . I f C r i c k ' s c e n t r a l d o g m a states t h a t p r o t e i n m a y not b e t r a n s l a t e d b a c k i n t o D N A , t h e c e n t r a l d o g m a o f e m b r y o l o g y states t h a t bodily form and b e h a v i o u r m a y not be translated back into protein. If y o u sleep in the sun w i t h y o u r h a n d o v e r y o u r chest, a w h i t e i m a g e of your hand will be imprinted on your otherwise tanned body. This image is a n a c q u i r e d c h a r a c t e r i s t i c . I n o r d e r for i t t o b e i n h e r i t e d , g e m m u l e s o r R N A viruses, or w h a t e v e r a g e n t of reverse translation is postulated, w o u l d have to scan
t h e macroscopic o u t l i n e o f t h e
hand
m o l e c u l a r structure of D N A necessary
image
and
translate it
into
the
to p r o g r a m the d e v e l o p m e n t of a
s i m i l a r h a n d i m a g e . I t i s s u g g e s t i o n s o f this k i n d t h a t c o n s t i t u t e a v i o l a t i o n o f the central d o g m a o f e m b r y o l o g y . The
central
common
sense.
dogma
of embryology
Rather,
it
is
a
does
logical
not
follow
implication
inevitably of
from
rejecting
the
preformationist v i e w of d e v e l o p m e n t . I suggest, i n d e e d , that there is a close l i n k b e t w e e n t h e e p i g e n e t i c v i e w o f d e v e l o p m e n t a n d the D a r w i n i a n v i e w o f adaptation,
and
between
preformationism
and
the
Lamarckian
view
of
a d a p t a t i o n . Y o u m a y b e l i e v e i n i n h e r i t a n c e o f L a m a r c k i a n (i.e. ' i n s t r u c t i v e ' ) adaptations,
but only if y o u are prepared to e m b r a c e a preformationistic
v i e w o f e m b r y o l o g y . I f d e v e l o p m e n t were preformationistic, i f D N A really were a ' b l u e p r i n t for a b o d y ' , r e a l l y w e r e a c o d i f i e d h o m u n c u l u s , r e v e r s e development—looking-glass embryology—would be conceivable.
Selfish D N A , J u m p i n g G e n e s , a n d a L a m a r c k i a n S c a r e
175
B u t the b l u e p r i n t m e t a p h o r o f t h e t e x t b o o k s i s d r e a d f u l l y m i s l e a d i n g , for i t i m p l i e s a o n e - t o - o n e m a p p i n g b e t w e e n bits o f b o d y a n d bits o f g e n o m e . B y inspecting a house, we m a y reconstruct a blueprint from w h i c h s o m e b o d y else c o u l d b u i l d a n i d e n t i c a l h o u s e , u s i n g t h e s a m e b u i l d i n g t e c h n i q u e a s w a s used for t h e o r i g i n a l h o u s e . T h e i n f o r m a t i o n a l a r r o w s f r o m b l u e p r i n t t o h o u s e a r e r e v e r s i b l e . T h e r e l a t i v e p o s i t i o n s o f t h e i n k lines i n t h e b l u e p r i n t a n d o f t h e b r i c k w a l l s i n the h o u s e a r e t r a n s f o r m a b l e , o n e i n t o t h e o t h e r , b y a few s i m p l e s c a l i n g r u l e s . T o g o f r o m b l u e p r i n t t o h o u s e , y o u m u l t i p l y a l l m e a s u r e m e n t s b y , say t w e n t y . T o g o from house t o b l u e p r i n t , y o u d i v i d e all measurements by t w e n t y . If the house s o m e h o w a c q u i r e s a n e w feature, say a w e s t w i n g , a s i m p l e , a u t o m a t i c p r o c e d u r e c o u l d b e w r i t t e n d o w n for a d d i n g a s c a l e d - d o w n m a p of the west w i n g to the b l u e p r i n t . If the g e n o m e w e r e a blueprint with a one-to-one m a p p i n g from g e n o t y p e to p h e n o t y p e , it w o u l d n o t b e i n c o n c e i v a b l e t h a t the w h i t e i m p r i n t o f a h a n d o n a n o t h e r w i s e t a n n e d chest c o u l d b e m a p p e d o n t o a sort o f m i n i a t u r e g e n e t i c s h a d o w o f itself, a n d so i n h e r i t e d . B u t this i s u t t e r l y a l i e n t o e v e r y t h i n g w e n o w u n d e r s t a n d a b o u t t h e w a y d e v e l o p m e n t w o r k s . T h e g e n o m e i s n o t , i n a n y sense w h a t s o e v e r , a s c a l e m o d e l o f t h e b o d y . I t i s a set o f i n s t r u c t i o n s w h i c h , i f f a i t h f u l l y o b e y e d i n t h e right order and under the right conditions, will result in a b o d y . I h a v e p r e v i o u s l y u s e d t h e m e t a p h o r o f a c a k e ( D a w k i n s i n press a ) . W h e n y o u m a k e a c a k e y o u m a y , i n s o m e sense, s a y t h a t y o u a r e ' t r a n s l a t i n g ' f r o m recipe to cake. But it is an irreversible process. Y o u c a n n o t dissect a c a k e and
thereby
reconstruct
the
original
recipe.
There
is
no
one-to-one,
reversible m a p p i n g from w o r d s of recipe to c r u m b s of c a k e . T h i s is not to say that a skilled c o o k c o u l d not a c h i e v e a passable reversal, by t a k i n g a c a k e p r e s e n t e d t o h i m a n d m a t c h i n g its taste a n d p r o p e r t i e s a g a i n s t his o w n p a s t experience of cakes a n d recipes, a n d then r e c o n s t r u c t i n g the r e c i p e . B u t that w o u l d b e a k i n d o f m e n t a l s e l e c t i o n p r o c e d u r e , a n d w o u l d i n n o sense b e a translation from c a k e t o r e c i p e ( a g o o d d i s c u s s i o n o f t h e d i f f e r e n c e b e t w e e n reversible and irreversible codes, in the c o n t e x t of the n e r v o u s system, is given by Barlow 1961). A c a k e i s t h e c o n s e q u e n c e o f t h e o b e y i n g o f a series o f i n s t r u c t i o n s , w h e n t o m i x the v a r i o u s i n g r e d i e n t s , w h e n t o a p p l y h e a t , e t c . I t i s n o t t r u e t h a t t h e c a k e i s those i n s t r u c t i o n s r e n d e r e d i n t o a n o t h e r c o d i n g m e d i u m . I t i s n o t l i k e a t r a n s l a t i o n o f the r e c i p e f r o m F r e n c h i n t o E n g l i s h , w h i c h i s i n p r i n c i p l e r e v e r s i b l e ( g i v e or t a k e a f e w nuances). A b o d y , t o o , is t h e c o n s e q u e n c e of t h e o b e y i n g o f a series o f i n s t r u c t i o n s ; n o t s o m u c h w h e n t o a p p l y h e a t a s w h e n to apply e n z y m e s speeding up particular c h e m i c a l reactions. If the process of e m b r y o n i c d e v e l o p m e n t i s c o r r e c t l y set i n m o t i o n i n t h e r i g h t e n v i r o n m e n t , the e n d result w i l l b e a w e l l - f o r m e d a d u l t b o d y , m a n y o f w h o s e a t t r i b u t e s w i l l b e i n t e r p r e t a b l e a s c o n s e q u e n c e s o f its g e n e s . B u t y o u c a n n o t r e c o n s t r u c t a n i n d i v i d u a l ' s g e n o m e b y i n s p e c t i n g his b o d y , a n y m o r e t h a n y o u c o u l d
176
Selfish D N A , J u m p i n g G e n e s , and a L a m a r c k i a n Scare
r e c o n s t r u c t W i l l i a m S h a k e s p e a r e b y d e c o d i n g his c o l l e c t e d w o r k s . C a n n o n ' s a n d G o u l d ' s false a r g u m e n t o f p . 1 1 6 i s v a l i d l y a d a p t e d t o e m b r y o l o g y . L e t m e p u t t h e m a t t e r i n a n o t h e r w a y . I f a m a n i s p a r t i c u l a r l y fat, there a r e m a n y w a y s i n w h i c h this m i g h t h a v e c o m e a b o u t . H e m i g h t h a v e a g e n e t i c p r e d i s p o s i t i o n t o m e t a b o l i z e his food p a r t i c u l a r l y t h o r o u g h l y . O r h e might
have been
overfed.
T h e end
result o f a n
e x c e s s o f food
may be
i d e n t i c a l t o t h e e n d r e s u l t o f a p a r t i c u l a r g e n e . I n b o t h c a s e s the m a n i s fat. B u t t h e r o u t e s b y w h i c h t h e t w o c a u s a l a g e n t s p r o d u c e d t h e i r c o m m o n effects a r e t o t a l l y d i f f e r e n t . F o r a m a n w h o i s a r t i f i c i a l l y stuffed w i t h food t o pass o n his a c q u i r e d fatness t o his c h i l d r e n g e n e t i c a l l y , s o m e m e c h a n i s m w o u l d h a v e to e x i s t t h a t s e n s e d his fatness, t h e n l o c a t e d a 'fatness g e n e ' a n d c a u s e d it to m u t a t e . B u t h o w c o u l d s u c h a fatness g e n e b e l o c a t e d ? T h e r e i s n o t h i n g i n t r i n s i c i n t h e n a t u r e o f t h e g e n e t h a t m a k e s i t r e c o g n i z a b l e a s a fatness g e n e . I t h a s its o b e s e effect o n l y a s a result o f t h e l o n g a n d c o m p l e x u n f o l d i n g sequence that is epigenetic development. T h e only w a y , in principle, to r e c o g n i z e a 'fatness g e n e ' for w h a t it is, is to a l l o w it to e x e r t its effects on the normal
processes
of development,
and
this
means
development
in
the
normal, forward direction. T h i s is w h y b o d i l y a d a p t a t i o n s c a n c o m e a b o u t by selection. G e n e s are a l l o w e d t o e x e r t t h e i r n o r m a l effects o n d e v e l o p m e n t . T h e i r d e v e l o p m e n t a l consequences—phenotypic
effects—feed
back on
those g e n e s '
chances of
s u r v i v i n g , a n d as a result g e n e frequencies c h a n g e in s u c c e e d i n g generations in a d a p t i v e directions. S e l e c t i v e theories of a d a p t a t i o n , but not instructive t h e o r i e s , c a n c o p e w i t h t h e f a c t t h a t t h e r e l a t i o n s h i p b e t w e e n a g e n e a n d its p h e n o t y p i c effect i s n o t a n i n t r i n s i c p r o p e r t y o f t h e g e n e , b u t a p r o p e r t y o f t h e f o r w a r d d e v e l o p m e n t a l c o n s e q u e n c e s o f the g e n e w h e n i n t e r a c t i n g w i t h the c o n s e q u e n c e s o f m a n y other genes a n d m a n y e x t e r n a l factors. C o m p l e x a d a p t a t i o n t o a n e n v i r o n m e n t m a y arise i n i n d i v i d u a l o r g a n i s m s through happens.
instruction from But,
given
an
that environment. assumption
In
m a n y c a s e s this c e r t a i n l y
of epigenetic,
not
preformationistic
e m b r y o l o g y , to e x p e c t such c o m p l e x a d a p t a t i o n s to be translated into the m e d i u m o f the g e n e t i c c o d e , b y some m e a n s other than the selection o f u n d i r e c t e d v a r i a t i o n , is a gross v i o l a t i o n of a l l t h a t I h o l d r a t i o n a l . T h e r e are other e x a m p l e s o f w h a t looks like true L a m a r c k i a n 'instruction' from the e n v i r o n m e n t b e i n g inherited. N o n - g e n e t i c a n o m a l i e s that appear, or e v e n that are s u r g i c a l l y i n d u c e d , in the cortex of ciliates, m a y be directly inherited.
This
has
been
demonstrated
by
Sonneborn
and
others.
By
B o n n e r ' s a c c o u n t , t h e y c u t o u t a s m a l l p o r t i o n o f the c o r t e x o f Paramecium a n d r e v e r s e d it. ' T h e r e s u l t i s a Paramecium w i t h p a r t o f o n e r o w o f b a s a l b o d i e s i n w h i c h t h e fine s t r u c t u r e a n d d e t a i l s a r e all p o i n t e d 180° a w a y from t h e rest o f t h e s u r f a c e . T h i s a n o m a l o u s k i n e t y i s n o w i n h e r i t e d ; i t a p p e a r s t o b e a p e r m a n e n t f i x t u r e o f t h e p r o g e n y ( w h i c h h a v e b e e n c a r r i e d t h r o u g h 800 generations)'
(Bonner 1974, p.
180). T h e inheritance a p p e a r s to be non-
Selfish D N A , J u m p i n g G e n e s , and a L a m a r c k i a n Scare
genic
and
is
obviously
non-nuclear.
' . . . the
cortex
is
made
177
up
of
m a c r o m o l e c u l e s t h a t a s s e m b l e i n a p a r t i c u l a r p a t t e r n , a n d . . . this p a t t e r n , even in a disturbed state, is directly inherited. . . . we h a v e a l a r g e a n d e x c e e d i n g l y c o m p l e x cortex w h o s e pattern of fitting together is a p r o p e r t y of the m a c r o m o l e c u l e s a t t h e c o r t e x a n d i s n o t d i r e c t l y u n d e r n u c l e a r c o n t r o l . O v e r w h a t must h a v e been a long time and a vast n u m b e r of cell cycles, a s u r f a c e s t r u c t u r e e v o l v e d . T h e s t r u c t u r e i t s e l f h a d p r o p e r t i e s s u c h t h a t its i m m e d i a t e form is i n d e p e n d e n t of the n u c l e u s ; at the s a m e time, it is totally d e p e n d e n t o n t h e n u c l e u s , w e p r e s u m e , for t h e s y n t h e s i s o f its s p e c i f i c a l l y shaped building blocks' (Bonner 1974). A s i n the c a s e o f S t e e l e ' s w o r k , w h e t h e r w e r e g a r d this a s t h e i n h e r i t a n c e o f acquired characteristics d e p e n d s u p o n our definition o f the g e r m - l i n e . I f w e d i r e c t o u r a t t e n t i o n t o t h e i n d i v i d u a l b o d y , a s u r g i c a l m u t i l a t i o n o f its c o r t e x is clearly an acquired characteristic h a v i n g n o t h i n g to do with the nuclear g e r m - l i n e . If, o n the o t h e r h a n d , w e l o o k a t u n d e r l y i n g r e p l i c a t o r s , i n this case perhaps general
the
heading
basal
bodies of cilia,
of replicator
the
propagation.
p h e n o m e n o n falls Given
that
under
the
macromolecular
structures in the cortex are true replicators, s u r g i c a l l y r o t a t i n g a p o r t i o n of c o r t e x i s a n a l o g o u s t o c u t t i n g o u t a p o r t i o n o f c h r o m o s o m e , i n v e r t i n g it, a n d putting it b a c k . N a t u r a l l y the inversion is inherited, b e c a u s e it is part of the g e r m - l i n e . It a p p e a r s t h a t e l e m e n t s of the c o r t e x of Paramecium h a v e a g e r m line
of their
own,
although
a
particularly
remarkable
one
in
that
the
information transmitted does not seem to be e n c o d e d in nucleic acids. We s h o u l d d e f i n i t e l y p r e d i c t t h a t n a t u r a l s e l e c t i o n m i g h t a c t d i r e c t l y o n this n o n - g e n i c g e r m - l i n e , s h a p i n g s u r f a c e s t r u c t u r e for t h e a d a p t i v e b e n e f i t o f t h e r e p l i c a t i n g u n i t s i n t h e s u r f a c e itself. I f t h e r e i s a n y c o n f l i c t b e t w e e n t h e interests o f these s u r f a c e r e p l i c a t o r s a n d n u c l e a r g e n e s , t h e r e s o l u t i o n o f t h e conflict should m a k e a fascinating study. T h i s is by no means the only e x a m p l e of non-nuclear inheritance. It is b e c o m i n g increasingly clear that non-nuclear genes, either in organelles such a s m i t o c h o n d r i a o r l o o s e i n c y t o p l a s m , e x e r t n o t i c e a b l e effects o n p h e n o t y p e s (Grun
1976).
Plasmagene,
I
had
discussing
intended the
to
expected
include
a
section
consequences
called
of selection
The
Selfish
acting
on
c y t o p l a s m i c r e p l i c a t o r s , a n d t h e l i k e l y results o f c o n f l i c t s w i t h n u c l e a r g e n e s . However,
I
mitochondria'
had
got
no
further
(now in C h a p t e r
than
some
brief remarks
12), w h e n two papers arrived
on
'selfish
(Eberhard
1980; C o s m i d e s & T o o b y 1981) w h i c h , independently, say e v e r y t h i n g I m i g h t h a v e said a n d m u c h m o r e . T o g i v e j u s t o n e e x a m p l e , ' T h e m i g r a t i o n of e g g m i t o c h o n d r i a to cluster a r o u n d the e g g nucleus, so as to favor their i n c l u s i o n i n t h e " n e o c y t o p l a s m " o f t h e p r o e m b r y o i n t h e g y m n o s p e r m s Larix a n d Pseudotsuga . . . m a y result f r o m c o m p e t i t i o n for i n c l u s i o n in t h e e m b r y o ' (Eberhard, p. 238). R a t h e r than extensively duplicate w h a t is in them I w o u l d prefer simply to r e c o m m e n d readers to consult b o t h these e x c e l l e n t
178
Selfish D N A , J u m p i n g G e n e s , and a L a m a r c k i a n Scare
papers. I will o n l y a d d that both papers are g o o d e x a m p l e s of the kind of discussion
that I
believe will b e c o m e c o m m o n p l a c e , once the replicator
replaces the i n d i v i d u a l o r g a n i s m as the f u n d a m e n t a l c o n c e p t u a l unit in our thinking a b o u t natural selection. O n e does not h a v e to be clairvoyant to p r o p h e s y , for e x a m p l e , t h e rise o f a f l o u r i s h i n g n e w d i s c i p l i n e o f ' p r o k a r y o t i c sociobiology'. N e i t h e r E b e r h a r d nor C o s m i d e s and T o o b y explicitly justify o r d o c u m e n t t h e g e n e s ' - e y e v i e w o f l i f e : t h e y s i m p l y assume i t : ' T h e r e c e n t shift t o w a r d s v i e w i n g t h e g e n e a s t h e u n i t o f s e l e c t i o n , c o u p l e d w i t h a r e c o g n i t i o n o f the different
modes
symbiosis,
of genetic
inheritance
makes
the
concept
of parasitism,
conflict, cooperation, and c o e v o l u t i o n — w h i c h w e r e developed
with reference to w h o l e organisms—relevant to genes within an organism' ( C o s m i d e s & T o o b y ) . T h e s e p a p e r s h a v e w h a t I c a n o n l y d e s c r i b e a s the flavour of post-revolutionary normal science ( K u h n 1970).
10 An Agony in Five Fits
T h e r e a d e r m a y r e m a r k t h a t w e h a v e c o m e t h u s far w i t h s c a r c e l y a m e n t i o n o f 'fitness'. T h i s w a s d e l i b e r a t e . I h a v e m i s g i v i n g s a b o u t t h e t e r m , but I h a v e been h o l d i n g my fire. S e v e r a l of the earlier c h a p t e r s h a v e b e e n a i m e d , in their different w a y s , at e x p o s i n g the w e a k n e s s e s in the i n d i v i d u a l o r g a n i s m ' s c a n d i d a c y for the title o f o p t i m o n , adaptations
may
be said
to work.
'Fitness',
the as
it
u n i t for w h o s e b e n e f i t is
normally
used
by
e c o l o g i s t s a n d e t h o l o g i s t s , is a v e r b a l t r i c k , a d e v i c e c o n t r i v e d to m a k e it possible t o t a l k i n t e r m s o f i n d i v i d u a l s , a s o p p o s e d t o t r u e r e p l i c a t o r s , a s beneficiaries of a d a p t a t i o n . T h e w o r d is therefore a kind of v e r b a l s y m b o l of the p o s i t i o n t h a t I a m t r y i n g t o a r g u e a g a i n s t . M o r e t h a n t h a t , t h e w o r d i s actively confusing because it has b e e n used in so m a n y different w a y s . It is therefore fitting to end the critical section of the b o o k w i t h a discussion of fitness. Herbert Spencer's
(1864)
term 'survival of the fittest' w a s a d o p t e d by
D a r w i n (1866) a t the u r g i n g o f W a l l a c e ( 1 8 6 6 ) . W a l l a c e ' s a r g u m e n t m a k e s f a s c i n a t i n g r e a d i n g t o d a y , a n d I c a n n o t resist q u o t i n g h i m a t s o m e l e n g t h : My dear Darwin,—I
h a v e been so repeatedly struck by the utter
i n a b i l i t y o f n u m b e r s o f i n t e l l i g e n t p e r s o n s t o see c l e a r l y , o r a t a l l , t h e s e l f - a c t i n g a n d n e c e s s a r y effects o f N a t u r a l S e l e c t i o n , t h a t I a m led t o conclude
that
the
term
itself,
and
your
mode
of illustrating
it,
h o w e v e r c l e a r a n d b e a u t i f u l t o m a n y o f us, a r e y e t n o t t h e b e s t a d a p t e d to impress it on the g e n e r a l naturalist p u b l i c . . . in J a n e t ' s recent w o r k o n the ' M a t e r i a l i s m o f the Present D a y ' . . . h e considers y o u r w e a k p o i n t t o b e t h a t y o u d o n o t see t h a t ' t h o u g h t a n d d i r e c t i o n a r e essential t o t h e a c t i o n o f N a t u r a l S e l e c t i o n ' . T h e s a m e o b j e c t i o n has been m a d e a score of times by y o u r c h i e f o p p o n e n t s , a n d I h a v e h e a r d i t a s often s t a t e d m y s e l f i n c o n v e r s a t i o n . N o w , I t h i n k this arises almost entirely from y o u r c h o i c e of the term N a t u r a l S e l e c t i o n , a n d so c o n s t a n t l y c o m p a r i n g i t i n its effects t o m a n ' s s e l e c t i o n , a n d a l s o t o 179
180
An A g o n y in Five F i t s
y o u r so frequently personifying nature as 'selecting', as 'preferring', as ' s e e k i n g o n l y t h e g o o d o f t h e s p e c i e s ' , e t c . , e t c . T o the few this i s a s clear
as
daylight,
and
beautifully
suggestive,
but
to
many
it
is
e v i d e n t l y a s t u m b l i n g b l o c k . I w i s h , t h e r e f o r e , to s u g g e s t to y o u the p o s s i b i l i t y o f e n t i r e l y a v o i d i n g this s o u r c e o f m i s c o n c e p t i o n i n y o u r g r e a t w o r k (if n o w n o t t o o l a t e ) , a n d a l s o i n a n y f u t u r e e d i t i o n s o f the 'Origin',
and I
t h i n k i t m a y b e d o n e w i t h o u t difficulty a n d v e r y
e f f e c t u a l l y b y a d o p t i n g S p e n c e r ' s t e r m ( w h i c h h e g e n e r a l l y uses i n p r e f e r e n c e t o N a t u r a l S e l e c t i o n ) , v i z . ' S u r v i v a l o f the F i t t e s t ' . T h i s term is the p l a i n expression of the fact; m e t a p h o r i c a l e x p r e s s i o n of it,
and
' N a t u r a l S e l e c t i o n ' is a
to a c e r t a i n d e g r e e indirect a n d
incorrect, s i n c e , e v e n p e r s o n i f y i n g N a t u r e , she d o e s n o t s o m u c h select s p e c i a l v a r i a t i o n s as e x t e r m i n a t e t h e m o s t u n f a v o u r a b l e o n e s . . . [ T h e Wallace-Darwin Correspondence].
I t m a y s e e m h a r d t o b e l i e v e t h a t a n y o n e c o u l d h a v e b e e n m i s l e d i n the w a y that W a l l a c e indicates, but Y o u n g ( 1 9 7 1 )
provides ample evidence
c o n f i r m i n g t h a t D a r w i n ' s c o n t e m p o r a r i e s often w e r e s o m i s l e d . E v e n t o d a y t h e c o n f u s i o n i s n o t u n k n o w n , a n d a n a n a l o g o u s m u d d l e arises o v e r the catch-phrase There
is
'selfish g e n e ' :
no
reason
for
' T h i s is an ingenious theory but far-fetched.
imputing
the
complex
emotion
o f selfishness
to
m o l e c u l e s ' ( B e t h e l l 1 9 7 8 ) ; ' G e n e s c a n n o t b e selfish o r unselfish, a n y m o r e than
atoms
can
be jealous,
elephants
abstract
or
biscuits
teleological'
( M i d g l e y 1 9 7 9 ; see r e p l y i n D a w k i n s 1 9 8 1 ) . D a r w i n ( 1 8 6 6 ) w a s i m p r e s s e d b y W a l l a c e ' s l e t t e r , w h i c h h e f o u n d 'as c l e a r a s d a y l i g h t ' , a n d h e r e s o l v e d t o i n c o r p o r a t e ' s u r v i v a l o f t h e f i t t e s t ' i n t o his w r i t i n g s , a l t h o u g h h e c a u t i o n e d t h a t ' t h e t e r m N a t u r a l S e l e c t i o n has n o w b e e n so largely used a b r o a d a n d at h o m e that I d o u b t w h e t h e r it could be g i v e n u p , a n d w i t h a l l its faults I s h o u l d b e s o r r y t o see the a t t e m p t m a d e . Whether
it
will
be
rejected
must
now depend
on
the
" s u r v i v a l of the
fittest" . . . ' ( D a r w i n c l e a r l y understood the ' m e m e ' p r i n c i p l e ) . ' A s i n time t h e t e r m m u s t g r o w i n t e l l i g i b l e , t h e o b j e c t i o n s t o its use w i l l g r o w w e a k e r and weaker.
I d o u b t w h e t h e r t h e use o f a n y t e r m w o u l d h a v e m a d e the
s u b j e c t i n t e l l i g i b l e t o s o m e m i n d s . . . A s for M . J a n e t , h e i s a m e t a p h y s i c i a n , a n d such g e n t l e m e n are so a c u t e that
I
t h i n k t h e y often m i s u n d e r s t a n d
c o m m o n folk.' W h a t neither W a l l a c e nor D a r w i n could h a v e foreseen w a s that 'survival o f t h e fittest' w a s d e s t i n e d t o g e n e r a t e m o r e s e r i o u s c o n f u s i o n t h a n ' n a t u r a l selection' e v e r h a d . A familiar e x a m p l e is the a t t e m p t , rediscovered with almost pathetic eagerness by successive generations of a m a t e u r (and even professional)
philosophers
('so
acute
that
they
misunderstand
common
f o l k ' ? ) , to d e m o n s t r a t e that the theory of natural selection is a worthless t a u t o l o g y (an a m u s i n g v a r i a n t is t h a t it is u n f a l s i f i a b l e a n d t h e r e f o r e f a l s e ! ) .
An A g o n y in F i v e F i t s
181
I n fact the i l l u s i o n o f t a u t o l o g y s t e m s e n t i r e l y f r o m t h e p h r a s e ' s u r v i v a l o f t h e fittest', a n d n o t f r o m t h e t h e o r y i t s e l f a t a l l . T h e a r g u m e n t i s a r e m a r k a b l e e x a m p l e of the e l e v a t i o n of w o r d s a b o v e their station, in w h i c h respect it resembles St A n s e l m ' s ontological p r o o f of the existence of G o d . L i k e G o d , natural selection is too big a theory to be p r o v e d or d i s p r o v e d by w o r d games.
God
and
natural selection are,
after a l l ,
the only
two workable
theories w e h a v e o f w h y w e exist. B r i e f l y , t h e t a u t o l o g y i d e a i s this. survival of the fittest, a n d
N a t u r a l selection is defined as the
the fittest are defined
as
those
that survive.
T h e r e f o r e the w h o l e of D a r w i n i s m is an unfalsifiable t a u t o l o g y a n d we d o n ' t have
to
worry
our
heads
about
it
any
more.
Fortunately,
several
a u t h o r i t a t i v e r e p l i e s t o this w h i m s i c a l little c o n c e i t a r e a v a i l a b l e ( M a y n a r d Smith
1969; Stebbins 1 9 7 7 ; A l e x a n d e r 1980), and I n e e d not l a b o u r my
o w n . I w i l l , h o w e v e r , c h a l k u p t h e t a u t o l o g y i d e a o n m y list o f m u d d l e s a t t r i b u t a b l e t o t h e c o n c e p t o f fitness. It is, as I h a v e s a i d , a p u r p o s e of this c h a p t e r to s h o w t h a t fitness is a v e r y difficult c o n c e p t , a n d t h a t t h e r e m i g h t b e s o m e t h i n g t o b e s a i d for d o i n g w i t h o u t i t w h e n e v e r w e c a n . O n e w a y I s h a l l d o this i s t o s h o w t h a t t h e w o r d h a s b e e n u s e d b y b i o l o g i s t s i n a t l e a s t f i v e d i f f e r e n t senses. T h e first a n d o l d e s t m e a n i n g i s t h e o n e closest t o e v e r y d a y u s a g e . Fit the F i r s t W h e n S p e n c e r , W a l l a c e a n d D a r w i n o r i g i n a l l y used the t e r m 'fitness', the charge of t a u t o l o g y w o u l d not h a v e o c c u r r e d to a n y o n e .
I s h a l l c a l l this
original usage fitness[1]. It did not h a v e a precise technical m e a n i n g , and the f i t t e s t w e r e n o t defined a s
those that survive.
Fitness
meant,
roughly,
the
capacity to survive and reproduce, but it was not defined and measured as precisely s y n o n y m o u s w i t h r e p r o d u c t i v e success. It h a d a r a n g e of specific meanings,
depending
upon
the
particular
aspect
o f life
that
one
was
e x a m i n i n g . If the subject of attention w a s efficiency in g r i n d i n g v e g e t a b l e f o o d , the f i t t e s t i n d i v i d u a l s w e r e t h o s e w i t h t h e h a r d e s t t e e t h o r t h e m o s t powerful j a w muscles. I n different contexts the f i t t e s t i n d i v i d u a l s w o u l d b e t a k e n t o m e a n those w i t h t h e k e e n e s t e y e s , t h e s t r o n g e s t l e g m u s c l e s , t h e s h a r p e s t e a r s , t h e swiftest r e f l e x e s . T h e s e c a p a c i t i e s a n d a b i l i t i e s , a l o n g w i t h countless others, w e r e supposed to i m p r o v e o v e r the g e n e r a t i o n s , a n d n a t u r a l s e l e c t i o n effected t h a t i m p r o v e m e n t . ' S u r v i v a l o f t h e f i t t e s t ' w a s a g e n e r a l characterization
of
these
particular
improvements.
There
is
nothing
tautological a b o u t that. It w a s only later that fitness w a s a d o p t e d as a t e c h n i c a l term. Biologists t h o u g h t t h e y n e e d e d a w o r d for t h a t h y p o t h e t i c a l q u a n t i t y t h a t t e n d s t o b e m a x i m i z e d as a result of n a t u r a l selection. T h e y c o u l d h a v e c h o s e n 'selective potential', or 'survivability', or
'W'
b u t i n f a c t t h e y lit u p o n 'fitness'. T h e y
d i d the e q u i v a l e n t o f r e c o g n i z i n g t h a t t h e d e f i n i t i o n t h e y w e r e s e e k i n g m u s t
182
An A g o n y in Five F i t s
b e ' w h a t e v e r i t t a k e s t o m a k e t h e s u r v i v a l o f t h e fittest i n t o a t a u t o l o g y ' . T h e y r e d e f i n e d fitness a c c o r d i n g l y . B u t t h e t a u t o l o g y i s n o t a p r o p e r t y o f D a r w i n i s m itself, m e r e l y o f the c a t c h p h r a s e w e s o m e t i m e s use t o d e s c r i b e it. I f I s a y t h a t a t r a i n t r a v e l l i n g a t a n a v e r a g e v e l o c i t y o f 1 2 0 m . p . h . w i l l r e a c h its d e s t i n a t i o n i n h a l f t h e t i m e i t t a k e s a t r a i n t r a v e l l i n g at 60 m . p . h . , t h e f a c t t h a t I h a v e u t t e r e d a t a u t o l o g y does
not
prevent
the
trains
from
running,
nor
does
it
stop
us
asking
m e a n i n g f u l q u e s t i o n s a b o u t w h a t m a k e s o n e t r a i n faster t h a n t h e o t h e r : d o e s i t h a v e a l a r g e r e n g i n e , s u p e r i o r fuel, a m o r e s t r e a m l i n e d s h a p e , o r w h a t ? T h e c o n c e p t o f v e l o c i t y i s defined i n s u c h a w a y a s t o m a k e s t a t e m e n t s s u c h a s t h e o n e a b o v e t a u t o l o g i c a l l y t r u e . I t i s this t h a t m a k e s t h e c o n c e p t o f v e l o c i t y useful. A s M a y n a r d S m i t h (1969) w i t h e r i n g l y p u t it: ' O f course D a r w i n i s m c o n t a i n s t a u t o l o g i c a l f e a t u r e s : a n y s c i e n t i f i c t h e o r y c o n t a i n i n g t w o lines o f a l g e b r a d o e s s o . ' A n d w h e n H a m i l t o n ( 1 9 7 5 a ) , s p e a k i n g o f ' s u r v i v a l o f the fittest', s a i d
t h a t ' a c c u s a t i o n s o f t a u t o l o g y s e e m h a r d l y fair o n this s m a l l
p h r a s e i t s e l f , h e w a s p u t t i n g i t m i l d l y . G i v e n t h e p u r p o s e for w h i c h f i t n e s s w a s r e d e f i n e d , ' s u r v i v a l o f t h e f i t t e s t ' had t o b e c o m e a t a u t o l o g y . T o r e d e f i n e f i t n e s s i n a s p e c i a l t e c h n i c a l sense m i g h t h a v e d o n e n o h a r m , other than to g i v e some earnest philosophers a field day, but unfortunately its e x a c t t e c h n i c a l m e a n i n g h a s v a r i e d w i d e l y , a n d this h a s h a d the m o r e serious
effect
of confusing
unexceptionable
of the
some
various
biologists technical
too.
The
meanings
is
most that
precise adopted
and by
population geneticists.
Fit the Second F o r p o p u l a t i o n geneticists, fitness is an o p e r a t i o n a l measure, e x a c t l y defined in terms of a m e a s u r e m e n t p r o c e d u r e . T h e w o r d is a p p l i e d not really to a w h o l e i n d i v i d u a l o r g a n i s m b u t to a g e n o t y p e , usually at a single locus. T h e fitness W of a g e n o t y p e , s a y Aa, m a y be d e f i n e d as I — S, w h e r e S is the coefficient of selection against the g e n o t y p e
(Falconer
1960).
It m a y be
r e g a r d e d as a m e a s u r e of the n u m b e r of offspring that a t y p i c a l i n d i v i d u a l of g e n o t y p e Aa is e x p e c t e d to b r i n g up to reproductive age, w h e n all other v a r i a t i o n is a v e r a g e d out. It is usually expressed relative to the correspondi n g f i t n e s s o f o n e p a r t i c u l a r g e n o t y p e a t the l o c u s , w h i c h i s a r b i t r a r i l y defined as I. T h e n there is said to be selection, at that locus, in favour of g e n o t y p e s w i t h h i g h e r fitness, relative to g e n o t y p e s w i t h l o w e r fitness. I shall c a l l this s p e c i a l p o p u l a t i o n g e n e t i c i s t s ' m e a n i n g o f t h e t e r m f i t n e s s [ 2 ] . W h e n we say that b r o w n - e y e d individuals are fitter than blue-eyed individuals we a r e t a l k i n g a b o u t f i t n e s s [ 2 ] . W e a s s u m e t h a t a l l o t h e r v a r i a t i o n a m o n g the i n d i v i d u a l s i s a v e r a g e d o u t , a n d w e a r e , i n effect, a p p l y i n g t h e w o r d fitness t o t w o g e n o t y p e s at a single locus.
An A g o n y in F i v e F i t s
183
Fit the T h i r d But
while
population
geneticists
are
interested
directly
in
changes
in
genotype frequencies and gene frequencies, ethologists and ecologists look at whole
organisms
as
integrated
systems
that
appear
to
be
maximizing
s o m e t h i n g . F i t n e s s [ 3 ] , o r ' c l a s s i c a l fitness', i s a p r o p e r t y o f a n i n d i v i d u a l o r g a n i s m , often e x p r e s s e d a s t h e p r o d u c t o f s u r v i v a l a n d f e c u n d i t y . I t i s a m e a s u r e o f t h e i n d i v i d u a l ' s r e p r o d u c t i v e s u c c e s s , o r its s u c c e s s i n p a s s i n g its genes on to future generations. F o r instance, as m e n t i o n e d in C h a p t e r 7, C l u t t o n - B r o c k et al. (in press) a r e c o n d u c t i n g a l o n g - t e r m s t u d y of a r e d d e e r population on the island of R h u m , a n d part of their a i m is to c o m p a r e the lifetime r e p r o d u c t i v e s u c c e s s e s o r fitness[3] o f i d e n t i f i e d i n d i v i d u a l s t a g s a n d hinds. N o t i c e the difference b e t w e e n
the fitness[3] of an i n d i v i d u a l a n d
the
fitness[2] o f a g e n o t y p e . T h e m e a s u r e d f i t n e s s [ 2 ] o f t h e b r o w n - e y e d g e n o t y p e will contribute t o the f i t n e s s [ 3 ] o f a n i n d i v i d u a l w h o h a p p e n s t o h a v e b r o w n e y e s , b u t s o w i l l t h e f i t n e s s [ 2 ] o f his g e n o t y p e a t a l l o t h e r l o c i . T h u s t h e fitness[2] of a g e n o t y p e at a locus c a n be r e g a r d e d as an a v e r a g e of the f i t n e s s [ 3 ] s o f a l l i n d i v i d u a l s p o s s e s s i n g t h a t g e n o t y p e . A n d t h e fitness[3] o f a n i n d i v i d u a l c a n b e r e g a r d e d a s i n f l u e n c e d b y t h e f i t n e s s [ 2 ] o f his g e n o t y p e , a v e r a g e d o v e r a l l his l o c i ( F a l c o n e r 1 9 6 0 ) . It is e a s y to m e a s u r e t h e fitness[2] of a g e n o t y p e at a l o c u s , b e c a u s e e a c h g e n o t y p e , AA, Aa, e t c . , o c c u r s a c o u n t a b l e n u m b e r o f t i m e s i n s u c c e s s i v e g e n e r a t i o n s i n a p o p u l a t i o n . B u t t h e s a m e i s n o t t r u e o f t h e fitness[3] o f a n organism.
You
c a n ' t c o u n t the n u m b e r o f times a n o r g a n i s m o c c u r s i n
successive generations, because h e o n l y occurs o n c e , ever. T h e f i t n e s s [ 3 ] o f a n o r g a n i s m i s often m e a s u r e d a s t h e n u m b e r o f his o f f s p r i n g r e a r e d t o a d u l t h o o d , b u t t h e r e i s s o m e d i s p u t e o v e r t h e usefulness o f this. O n e p r o b l e m i s raised b y W i l l i a m s ( 1 9 6 6 ) c r i t i c i z i n g M e d a w a r ( 1 9 6 0 ) w h o h a d s a i d : ' T h e genetical usage of "fitness" is an extreme attenuation of the ordinary u s a g e : i t is, i n effect, a s y s t e m o f p r i c i n g t h e e n d o w m e n t s o f o r g a n i s m s i n t h e c u r r e n c y o f o f f s p r i n g , i.e., i n t e r m s o f n e t r e p r o d u c t i v e p e r f o r m a n c e . I t i s a genetic valuation of goods, not a statement a b o u t their nature or q u a l i t y . ' W i l l i a m s is w o r r i e d
that
this
is
a
retrospective definition,
s u i t a b l e for
particular individuals w h o h a v e existed. It suggests a p o s t h u m o u s e v a l u a t i o n of particular a n i m a l s as ancestors, not a w a y of e v a l u a t i n g the qualities that c a n b e e x p e c t e d t o m a k e for s u c c e s s i n g e n e r a l .
' M y m a i n criticism of
M e d a w a r ' s s t a t e m e n t i s t h a t i t focuses a t t e n t i o n o n t h e r a t h e r t r i v i a l p r o b l e m o f the d e g r e e t o w h i c h a n o r g a n i s m a c t u a l l y a c h i e v e s r e p r o d u c t i v e s u r v i v a l . T h e central biological
p r o b l e m is not survival as such,
b u t d e s i g n for
s u r v i v a l ' ( W i l l i a m s 1 9 6 6 , p . 1 5 8 ) . W i l l i a m s is, i n a sense, h a n k e r i n g after t h e p r e - t a u t o l o g i c a l v i r t u e s o f f i t n e s s [ 1 ] , a n d t h e r e i s m u c h t o b e s a i d i n his f a v o u r . B u t the f a c t i s t h a t f i t n e s s [ 3 ] h a s b e c o m e w i d e l y u s e d b y b i o l o g i s t s i n
184
An A g o n y in F i v e F i t s
t h e sense d e s c r i b e d laymen
and
by
Medawar.
was surely
an
M e d a w a r ' s passage was addressed to
attempt
to
enable
them
to
follow
standard
b i o l o g i c a l t e r m i n o l o g y w h i l e a v o i d i n g the otherwise i n e v i t a b l e confusion w i t h c o m m o n - u s a g e ' a t h l e t i c ' fitness. The
concept
o f fitness
has
the
power
to
confuse
even
distinguished
biologists. C o n s i d e r the f o l l o w i n g m i s u n d e r s t a n d i n g o f W a d d i n g t o n (1957) b y E m e r s o n ( 1 9 6 0 ) . W a d d i n g t o n h a d u s e d t h e w o r d ' s u r v i v a l ' i n the sense o f r e p r o d u c t i v e s u r v i v a l o r f i t n e s s [ 3 ] : ' . . . s u r v i v a l d o e s n o t , o f c o u r s e , m e a n the b o d i l y e n d u r a n c e o f a s i n g l e i n d i v i d u a l . . . t h a t i n d i v i d u a l " s u r v i v e s " best w h i c h l e a v e s m o s t o f f s p r i n g ' . E m e r s o n q u o t e s this, t h e n g o e s o n : ' C r i t i c a l d a t a o n this c o n t e n t i o n a r e d i f f i c u l t t o find, a n d i t i s l i k e l y t h a t m u c h n e w investigation is n e e d e d before the point is either verified or refuted.' F o r once,
the
ritual
lip-service
to
the
need
for
more
research
is
utterly
inappropriate. W h e n we are talking a b o u t matters of definition, empirical r e s e a r c h c a n n o t h e l p us. W a d d i n g t o n w a s c l e a r l y defining s u r v i v a l i n a s p e c i a l s e n s e ( t h e sense o f f i t n e s s [ 3 ] ) , n o t m a k i n g a p r o p o s i t i o n o f fact s u b j e c t t o empirical
verification
or
falsification.
Yet
Emerson
apparently
thought
W a d d i n g t o n w a s m a k i n g t h e p r o v o c a t i v e s t a t e m e n t t h a t those i n d i v i d u a l s w i t h t h e h i g h e s t c a p a c i t y t o s u r v i v e t e n d a l s o t o b e t h e i n d i v i d u a l s w i t h the l a r g e s t n u m b e r o f o f f s p r i n g . H i s f a i l u r e t o g r a s p the t e c h n i c a l c o n c e p t o f f i t n e s s [ 3 ] , i s i n d i c a t e d b y a n o t h e r q u o t a t i o n from t h e s a m e p a p e r : ' I t w o u l d be e x t r e m e l y difficult to e x p l a i n the e v o l u t i o n of the uterus a n d m a m m a r y glands
in
individual.'
m a m m a l s . . . as
the
result
of natural
In a c c o r d a n c e w i t h the influential
selection
of the fittest
C h i c a g o - b a s e d school of
t h o u g h t o f w h i c h h e w a s a l e a d e r ( A l l e e , E m e r s o n e l al. 1 9 4 9 ) , E m e r s o n used this a s a n a r g u m e n t i n f a v o u r o f g r o u p s e l e c t i o n . M a m m a r y g l a n d s a n d u t e r u s e s w e r e , for h i m , a d a p t a t i o n s for t h e c o n t i n u a t i o n o f t h e s p e c i e s . W o r k e r s w h o c o r r e c t l y use t h e c o n c e p t o f f i t n e s s [ 3 ] a d m i t t h a t i t c a n b e m e a s u r e d o n l y as a c r u d e a p p r o x i m a t i o n . If it is m e a s u r e d as the n u m b e r of c h i l d r e n b o r n i t n e g l e c t s j u v e n i l e m o r t a l i t y a n d fails t o a c c o u n t for p a r e n t a l c a r e . If it is m e a s u r e d as n u m b e r of offspring r e a c h i n g r e p r o d u c t i v e age it neglects v a r i a t i o n in r e p r o d u c t i v e success of the g r o w n offspring. If it is m e a s u r e d a s n u m b e r o f g r a n d c h i l d r e n i t n e g l e c t s . . . a n d s o o n a d infinitum. I d e a l l y w e m i g h t c o u n t t h e r e l a t i v e n u m b e r o f d e s c e n d a n t s a l i v e after s o m e very
large
number of generations.
But such
an
'ideal'
m e a s u r e h a s the
c u r i o u s p r o p e r t y t h a t , i f c a r r i e d t o its l o g i c a l c o n c l u s i o n , i t c a n t a k e o n l y t w o v a l u e s ; i t i s a n a l l - o r - n o n e m e a s u r e . I f w e l o o k far e n o u g h i n t o t h e future, either I shall h a v e no d e s c e n d a n t s at all, or all persons a l i v e will be my d e s c e n d a n t s ( F i s h e r 1 9 3 0 a ) . I f I a m d e s c e n d e d from a p a r t i c u l a r i n d i v i d u a l m a l e w h o lived a million years a g o , it is virtually certain that y o u are d e s c e n d e d from him too. T h e f i t n e s s o f any particular long-dead individual, as measured in present-day descendants, is either zero or total. Williams w o u l d p r e s u m a b l y s a y t h a t if this is a p r o b l e m it is so o n l y for p e o p l e t h a t
An A g o n y in Five F i t s
185
w i s h t o m e a s u r e t h e actual r e p r o d u c t i v e s u c c e s s o f p a r t i c u l a r i n d i v i d u a l s . If, o n the o t h e r h a n d , w e a r e i n t e r e s t e d i n q u a l i t i e s t h a t t e n d , o n a v e r a g e , t o m a k e i n d i v i d u a l s likely t o e n d u p i n t h e set o f a n c e s t o r s , t h e p r o b l e m d o e s n o t arise. I n a n y c a s e a m o r e b i o l o g i c a l l y i n t e r e s t i n g s h o r t c o m i n g o f t h e c o n c e p t o f f i t n e s s [ 3 ] h a s led t o t h e d e v e l o p m e n t o f t w o n e w e r u s a g e s o f t h e t e c h n i c a l term fitness.
Fit the F o u r t h Hamilton
(1964a,b),
in a pair of p a p e r s w h i c h we c a n n o w see to h a v e
m a r k e d a turning point in the history of e v o l u t i o n a r y theory, m a d e us a w a r e of an important deficiency in classical fitness[3], the m e a s u r e based on the reproductive
success
of an
organism.
The
reason
reproductive
success
matters, as opposed to m e r e i n d i v i d u a l survival, is that r e p r o d u c t i v e success i s a m e a s u r e o f s u c c e s s i n p a s s i n g o n g e n e s . T h e o r g a n i s m s w e see a r o u n d u s are d e s c e n d e d from ancestors, and they h a v e inherited s o m e of the attributes that m a d e those individuals ancestors as o p p o s e d to non-ancestors.
If an
o r g a n i s m exists i t c o n t a i n s t h e g e n e s o f a l o n g l i n e o f s u c c e s s f u l a n c e s t o r s . T h e f i t n e s s [ 3 ] o f a n o r g a n i s m i s its s u c c e s s a s a n a n c e s t o r , o r , a c c o r d i n g t o taste, its c a p a c i t y for s u c c e s s a s a n a n c e s t o r . B u t H a m i l t o n g r a s p e d t h e c e n t r a l importance of w h a t , previously, h a d been only g l a n c i n g l y referred to in stray sentences
of Fisher
(1930a)
and
Haldane
(1955).
This
is
that
natural
selection will favour organs a n d b e h a v i o u r that cause the i n d i v i d u a l ' s genes t o b e p a s s e d o n , w h e t h e r o r n o t t h e i n d i v i d u a l is, h i m s e l f , a n a n c e s t o r . A n i n d i v i d u a l t h a t assists his b r o t h e r t o b e a n a n c e s t o r m a y t h e r e b y e n s u r e t h e survival in the g e n e - p o o l of the genes 'for' brotherly assistance. H a m i l t o n s a w t h a t p a r e n t a l c a r e i s r e a l l y o n l y a s p e c i a l c a s e o f c a r i n g for c l o s e r e l a t i v e s w i t h a h i g h p r o b a b i l i t y o f c o n t a i n i n g t h e g e n e s for c a r i n g . C l a s s i c a l f i t n e s s [ 3 ] , r e p r o d u c t i v e s u c c e s s , w a s t o o n a r r o w . I t h a d t o b e b r o a d e n e d t o inclusive fitness, w h i c h will here be called fitness[4]. I t i s s o m e t i m e s s u p p o s e d t h a t t h e i n c l u s i v e fitness o f a n i n d i v i d u a l i s his o w n fitness[3] plus h a l f the fitnesses[3] of e a c h b r o t h er plus o n e - e i g h t h of the fitness[3] of e a c h cousin,
etc.
(e.g.
B y g o t t e t al.
1979).
Barash
(1980)
e x p l i c i t l y defines i t a s ' t h e s u m o f i n d i v i d u a l f i t n e s s ( r e p r o d u c t i v e s u c c e s s ) a n d the r e p r o d u c t i v e s u c c e s s o f a n i n d i v i d u a l ' s r e l a t i v e s , w i t h e a c h r e l a t i v e d e v a l u e d in proportion as it is m o r e distantly related'. T h i s w o u l d not be a sensible m e a s u r e t o try t o u s e , a n d , a s W e s t - E b e r h a r d ( 1 9 7 5 ) e m p h a s i z e s , i t i s n o t the m e a s u r e H a m i l t o n offered us. T h e r e a s o n i t w o u l d n o t b e s e n s i b l e can be stated in various w a y s . O n e w a y of p u t t i n g it is that it a l l o w s children to be counted m a n y times, as though they h a d m a n y existences (Grafen 1 9 7 9 ) . T h e n a g a i n , i f a c h i l d i s b o r n t o o n e o f a set o f b r o t h e r s , t h e i n c l u s i v e f i t n e s s o f a l l the o t h e r b r o t h e r s w o u l d , a c c o r d i n g t o this v i e w , i m m e d i a t e l y rise a n e q u a l n o t c h , r e g a r d l e s s w h e t h e r a n y o f t h e m lifted a f i n g e r t o f e e d t h e
186
An A g o n y in F i v e F i t s
infant.
Indeed the inclusive fitness of another brother yet unborn would
t h e o r e t i c a l l y b e i n c r e a s e d b y t h e b i r t h o f his e l d e r n e p h e w . F u r t h e r , this l a t e r b r o t h e r c o u l d b e a b o r t e d s h o r t l y after c o n c e p t i o n a n d still, a c c o r d i n g t o this erroneous v i e w , enjoy a massive 'inclusive fitness' t h r o u g h the descendants of his e l d e r b r o t h e r s . T o p u s h t o t h e reductio a d absurdum, h e n e e d n ' t e v e n b o t h e r t o b e c o n c e i v e d , y e t still h a v e a h i g h ' i n c l u s i v e f i t n e s s ' ! H a m i l t o n c l e a r l y s a w this f a l l a c y , a n d t h e r e f o r e his c o n c e p t o f i n c l u s i v e fitness w a s m o r e subtle. T h e inclusive fitness of an organism is not a property of himself,
but
a p r o p e r t y o f his a c t i o n s o r effects.
Inclusive fitness is
c a l c u l a t e d f r o m a n i n d i v i d u a l ' s o w n r e p r o d u c t i v e s u c c e s s p l u s his effects o n the
reproductive
success
of
his
relatives,
each
one
weighed
by
the
a p p r o p r i a t e c o e f f i c i e n t o f r e l a t e d n e s s . T h e r e f o r e , for i n s t a n c e , i f m y b r o t h e r e m i g r a t e s t o A u s t r a l i a , s o I c a n h a v e n o effect, o n e w a y o r t h e o t h e r , o n his r e p r o d u c t i v e s u c c e s s , m y i n c l u s i v e fitness d o e s n o t g o u p e a c h t i m e h e h a s a child! N o w 'effects' o f p u t a t i v e causes c a n o n l y b e m e a s u r e d b y c o m p a r i s o n w i t h other putative causes, or by c o m p a r i s o n with their absence. We cannot, then, t h i n k o f t h e effects o f i n d i v i d u a l A o n t h e s u r v i v a l a n d r e p r o d u c t i o n o f his r e l a t i v e s i n a n y a b s o l u t e s e n s e . W e c o u l d c o m p a r e t h e effects o f his c h o o s i n g t o p e r f o r m a c t X r a t h e r t h a n a c t Y . O r w e c o u l d t a k e t h e effects o f his l i f e t i m e ' s set o f d e e d s a n d c o m p a r e t h e m w i t h a h y p o t h e t i c a l l i f e t i m e o f t o t a l i n a c t i o n — a s t h o u g h h e h a d n e v e r b e e n c o n c e i v e d . I t i s this l a t t e r u s a g e t h a t is n o r m a l l y m e a n t by the inclusive fitness of an individual organism. T h e point is
that inclusive fitness is not an
absolute property of an
organism in the same w a y as classical fitness[3] could in theory be, if m e a s u r e d i n c e r t a i n w a y s . I n c l u s i v e fitness i s a p r o p e r t y o f a t r i p l e c o n s i s t i n g o f a n o r g a n i s m o f i n t e r e s t , a n a c t o r set o f a c t s o f i n t e r e s t , a n d a n a l t e r n a t i v e set o f a c t s for c o m p a r i s o n . W e a s p i r e t o m e a s u r e , t h e n , n o t t h e a b s o l u t e i n c l u s i v e f i t n e s s o f t h e o r g a n i s m I , b u t t h e effect o n I ' s i n c l u s i v e f i t n e s s o f his d o i n g a c t X i n c o m p a r i s o n w i t h his d o i n g a c t Y . I f ' a c t ' X i s t a k e n t o b e I's e n t i r e life s t o r y , Y m a y b e t a k e n a s e q u i v a l e n t t o a h y p o t h e t i c a l w o r l d i n w h i c h I did not exist. An organism's inclusive fitness, then, is defined so that it is not affected by the r e p r o d u c t i v e success of relatives on another continent w h o m h e n e v e r meets a n d w h o m h e has n o w a y o f affecting. T h e m i s t a k e n v i e w that the inclusive fitness of an o r g a n i s m is a w e i g h t e d s u m o f t h e r e p r o d u c t i v e s u c c e s s e s o f a l l its r e l a t i v e s e v e r y w h e r e , w h o h a v e ever lived, and w h o will ever live, is extremely c o m m o n . A l t h o u g h Hamilton i s n o t r e s p o n s i b l e for t h e e r r o r s o f his f o l l o w e r s , this m a y b e o n e r e a s o n w h y m a n y p e o p l e h a v e s o m u c h difficulty d e a l i n g w i t h the c o n c e p t o f inclusive f i t n e s s , a n d i t m a y p r o v i d e a r e a s o n for a b a n d o n i n g t h e c o n c e p t a t s o m e t i m e in the future. T h e r e is y e t a fifth m e a n i n g of fitness, w h i c h was designed to a v o i d this p a r t i c u l a r d i f f i c u l t y o f i n c l u s i v e f i t n e s s , b u t w h i c h h a s difficulties o f its o w n .
An A g o n y in F i v e F i t s
187
Fit the Fifth F i t n e s s [ 5 ] i s ' p e r s o n a l fitness' i n t h e sense o f O r l o v e ( 1 9 7 5 , 1 9 7 9 ) . I t c a n b e t h o u g h t o f a s a k i n d o f b a c k w a r d s w a y o f l o o k i n g a t i n c l u s i v e fitness. W h e r e i n c l u s i v e f i t n e s s [ 4 ] f o c u s e s o n t h e effects t h e i n d i v i d u a l o f i n t e r e s t h a s o n t h e fitness[3] o f his r e l a t i v e s , p e r s o n a l fitness[5] f o c u s e s o n t h e effects t h a t t h e i n d i v i d u a l ' s r e l a t i v e s h a v e o n his f i t n e s s [ 3 ] . T h e fitness[3] o f a n i n d i v i d u a l i s s o m e m e a s u r e o f t h e n u m b e r o f his o f f s p r i n g o r d e s c e n d a n t s . B u t H a m i l t o n ' s logic has s h o w n us that we m a y e x p e c t an i n d i v i d u a l to end up w i t h m o r e offspring t h e n h e c o u l d r e a r himself, b e c a u s e his r e l a t i v e s c o n t r i b u t e t o w a r d s rearing
some
o f his
offspring.
An
animal's
fitness[5]
may
be
briefly
c h a r a c t e r i z e d a s ' t h e s a m e a s his fitness[3] b u t d o n ' t f o r g e t t h a t this m u s t i n c l u d e the e x t r a o f f s p r i n g h e g e t s a s a r e s u l t o f h e l p f r o m his r e l a t i v e s ' T h e advantage, in practice, of using personal fitness[5] over inclusive fitness[4] i s t h a t w e e n d u p s i m p l y c o u n t i n g o f f s p r i n g , a n d t h e r e i s n o risk o f a given child's being mistakenly counted m a n y times over. A g i v e n child is a p a r t o f t h e f i t n e s s [ 5 ] o f his p a r e n t s o n l y . H e p o t e n t i a l l y c o r r e s p o n d s t o a t e r m i n t h e i n c l u s i v e fitness[4] o f a n i n d e f i n i t e n u m b e r o f u n c l e s , a u n t s , c o u s i n s , etc., l e a d i n g t o a d a n g e r o f his b e i n g c o u n t e d s e v e r a l t i m e s ( G r a f e n 1 9 7 9 ; Hines & M a y n a r d Smith 1979). Inclusive fitness[4] w h e n
properly
used,
and
personal fitness[5], give
e q u i v a l e n t results. B o t h a r e m a j o r t h e o r e t i c a l a c h i e v e m e n t s a n d t h e i n v e n t o r of either of them w o u l d deserve lasting honour. It is entirely characteristic that H a m i l t o n himself q u i e t l y i n v e n t e d b o t h in the s a m e p a p e r , s w i t c h i n g from o n e t o a n o t h e r w i t h a swiftness t h a t b e w i l d e r e d a t l e a s t o n e l a t e r a u t h o r (Cassidy
1978,
p.
581).
Hamilton's
(1964a)
name
for
fitness[5]
was
' n e i g h b o u r - m o d u l a t e d f i t n e s s ' . H e c o n s i d e r e d t h a t its u s e , t h o u g h c o r r e c t , w o u l d b e u n w i e l d y , a n d for this r e a s o n h e i n t r o d u c e d i n c l u s i v e f i t n e s s [ 4 ] a s a more manageable alternative approach. M a y n a r d Smith
(in press)
agrees
t h a t i n c l u s i v e f i t n e s s [ 4 ] i s o f t e n e a s i e r t o use t h a n n e i g h b o u r - m o d u l a t e d fitness[5], and
he
illustrates
the
point
by
working
through
a
particular
hypothetical e x a m p l e using both methods in turn. N o t i c e t h a t b o t h these f i t n e s s e s , l i k e ' c l a s s i c a l ' f i t n e s s [ 3 ] , a r e f i r m l y t i e d t o the i d e a o f t h e i n d i v i d u a l o r g a n i s m a s ' m a x i m i z i n g a g e n t ' . I t i s o n l y p a r t l y facetiously that I h a v e characterized inclusive fitness as 'that property of an individual organism w h i c h will a p p e a r to be m a x i m i z e d w h e n w h a t is really being maximized is gene survival' (Dawkins 1978a). ( O n e might generalize this p r i n c i p l e t o o t h e r ' v e h i c l e s ' . A g r o u p s e l e c t i o n i s t m i g h t d e f i n e his o w n v e r s i o n o f i n c l u s i v e f i t n e s s a s ' t h a t p r o p e r t y o f a group w h i c h w i l l a p p e a r t o b e maximized w h e n w h a t is really being m a x i m i z e d is gene survival'!) H i s t o r i c a l l y , i n d e e d , I see t h e c o n c e p t o f i n c l u s i v e f i t n e s s a s t h e i n s t r u m e n t of a brilliant last-ditch rescue attempt, an attempt to save the i n d i v i d u a l organism
as
the
level
at which
we
u n d e r l y i n g spirit o f H a m i l t o n ' s ( 1 9 6 4 )
think
about
natural
selection.
The
p a p e r s o n i n c l u s i v e fitness i s g e n e
An A g o n y in Five F i t s
188
selectionist. T h e brief note of 1963 w h i c h preceded them is explicitly so: ' D e s p i t e t h e p r i n c i p l e o f " s u r v i v a l o f t h e f i t t e s t " t h e u l t i m a t e c r i t e r i o n that d e t e r m i n e s w h e t h e r G will spread is not w h e t h e r the b e h a v i o r is to the b e n e f i t of t h e b e h a v e r b u t w h e t h e r it is to t h e b e n e f i t of t h e g e n e G . . .' T o g e t h e r w i t h W i l l i a m s ( 1 9 6 6 ) , H a m i l t o n could fairly be regarded as one of the
fathers
of gene
selectionism
in
modern
behavioural
and
ecological
studies: A g e n e i s b e i n g f a v o r e d i n n a t u r a l s e l e c t i o n i f t h e a g g r e g a t e o f its replicas forms an increasing fraction of the total g e n e pool. We are going
to
be concerned
with genes supposed
t o affect
the social
b e h a v i o r o f t h e i r b e a r e r s , s o let u s try t o m a k e t h e a r g u m e n t m o r e v i v i d by a t t r i b u t i n g to the genes, t e m p o r a r i l y , intelligence and a certain freedom of choice.
I m a g i n e t h a t a g e n e i s c o n s i d e r i n g the
p r o b l e m o f i n c r e a s i n g t h e n u m b e r o f its r e p l i c a s a n d i m a g i n e that i t c a n c h o o s e b e t w e e n c a u s i n g p u r e l y s e l f - i n t e r e s t e d b e h a v i o r b y its bearer
A
(leading
'disinterested'
to
behavior
more that
reproduction benefits
in
by
some
A) way
and a
causing
relative,
B
[Hamilton 1972]. H a v i n g m a d e use o f his i n t e l l i g e n t g e n e m o d e l , H a m i l t o n l a t e r e x p l i c i t l y a b a n d o n s i t i n f a v o u r o f the i n c l u s i v e f i t n e s s effect o f a n individual o n the p r o p a g a t i o n o f c o p i e s o f his g e n e s . I t i s p a r t o f t h e thesis o f this b o o k t h a t h e m i g h t h a v e d o n e b e t t e r t o h a v e s t u c k b y his ' i n t e l l i g e n t g e n e ' m o d e l . I f i n d i v i d u a l o r g a n i s m s c a n b e a s s u m e d t o w o r k for t h e a g g r e g a t e benefit o f all their genes, it doesn't m a t t e r w h e t h e r we think in terms of genes w o r k i n g to ensure their s u r v i v a l , or of individuals w o r k i n g to m a x i m i z e their inclusive f i t n e s s . I s u s p e c t t h a t H a m i l t o n felt m o r e c o m f o r t a b l e w i t h t h e i n d i v i d u a l a s t h e a g e n t o f b i o l o g i c a l s t r i v i n g , o r p e r h a p s h e s u r m i s e d t h a t m o s t o f his c o l l e a g u e s w e r e n o t y e t r e a d y t o a b a n d o n t h e i n d i v i d u a l a s a g e n t . B u t , o f all t h e b r i l l i a n t t h e o r e t i c a l a c h i e v e m e n t s o f H a m i l t o n a n d his f o l l o w e r s , w h i c h h a v e b e e n e x p r e s s e d i n t e r m s o f i n c l u s i v e f i t n e s s [ 4 ] (or p e r s o n a l f i t n e s s [ 5 ] ) , I c a n n o t think of a n y that could not h a v e b e e n m o r e simply derived in terms of Hamilton's (Charnov
'intelligent
gene',
manipulating
bodies
for
its
own
ends
1977).
Individual-level thinking is superficially attractive because individuals, unlike genes, h a v e nervous systems and limbs w h i c h render them capable of w o r k i n g in o b v i o u s w a y s to m a x i m i z e something. It is therefore natural to ask w h a t q u a n t i t y , in theory, they m i g h t be e x p e c t e d to m a x i m i z e , a n d i n c l u s i v e f i t n e s s i s t h e a n s w e r . B u t w h a t m a k e s this s o d a n g e r o u s i s t h a t it, too, is really a m e t a p h o r . I n d i v i d u a l s do not consciously strive to m a x i m i z e a n y t h i n g ; t h e y b e h a v e as if m a x i m i z i n g s o m e t h i n g . It is e x a c t l y the same 'as i f logic that w e a p p l y t o 'intelligent genes'. G e n e s m a n i p u l a t e the w o r l d a s i f
189
An Agony in Five Fits
striving to m a x i m i z e their o w n survival. T h e y do not really 'strive', but my p o i n t i s t h a t i n this r e s p e c t t h e y d o n o t differ f r o m i n d i v i d u a l s . N e i t h e r individuals
nor
genes
really
strive
to
maximize
anything.
Or,
rather,
i n d i v i d u a l s m a y s t r i v e for s o m e t h i n g , b u t i t w i l l b e a m o r s e l o f f o o d , a n attractive female, or a desirable territory, not inclusive fitness. To the extent t h a t i t i s useful for u s t o t h i n k o f i n d i v i d u a l s w o r k i n g a s i f t o m a x i m i z e fitness, we m a y , with precisely the same licence, think of genes as if they w e r e striving to m a x i m i z e their survival. T h e difference is that the q u a n t i t y the genes m a y be thought of as m a x i m i z i n g (survival of replicas) is a great deal simpler and easier to deal w i t h in models than the q u a n t i t y i n d i v i d u a l s m a y be thought of as m a x i m i z i n g
(fitness).
I
repeat that if we think about
individual animals m a x i m i z i n g something, there is a serious d a n g e r of our confusing ourselves,
since
we
m a y forget w h e t h e r w e
are
using
'as
if
l a n g u a g e o r w h e t h e r w e are t a l k i n g a b o u t the a n i m a l s consciously striving for s o m e g o a l .
Since no sane
biologist
could
imagine
DNA
molecules
c o n s c i o u s l y s t r i v i n g for a n y t h i n g , t h e d a n g e r o f this c o n f u s i o n o u g h t n o t t o exist w h e n w e t a l k o f g e n e s a s m a x i m i z i n g a g e n t s . It is my belief that thinking in terms of individuals striving to m a x i m i z e s o m e t h i n g has led to o u t r i g h t error, in a w a y that t h i n k i n g in terms of genes striving to m a x i m i z e something w o u l d conclusions
that
not.
their perpetrators w o u l d
By
admit
outright are
error,
w r o n g after
I
mean further
reflection. I h a v e d o c u m e n t e d these errors in the section l a b e l l e d ' C o n f u s i o n ' of Dawkins (1978a), and in Dawkins (1979a, especially Misunderstandings 5, 6, 7 and
1 1 ) . T h e s e papers g i v e detailed e x a m p l e s , from the published
literature, of errors w h i c h , I b e l i e v e , result from ' i n d i v i d u a l - l e v e l ' t h i n k i n g . T h e r e is no need to harp on them again here, and I will just give one e x a m p l e of the kind of thing I m e a n , w i t h o u t m e n t i o n i n g n a m e s , u n d e r the title o f the ' A c e o f S p a d e s F a l l a c y ' . T h e coefficient o f relationship b e t w e e n t w o relatives, say g r a n d f a t h e r a n d grandson, c a n be taken to be e q u i v a l e n t to t w o distinct q u a n t i t i e s . It is often e x p r e s s e d a s t h e m e a n fraction o f a g r a n d f a t h e r ' s g e n o m e t h a t i s e x p e c t e d t o b e i d e n t i c a l b y d e s c e n t w i t h t h a t o f the g r a n d s o n . I t i s a l s o t h e probability t h a t a n a m e d g e n e of the g r a n d f a t h e r will be identical by descent w i t h a g e n e in the g r a n d s o n . S i n c e t h e t w o a r e n u m e r i c a l l y t h e s a m e , i t m i g h t s e e m n o t t o m a t t e r w h i c h w e t h i n k i n t e r m s of. E v e n t h o u g h t h e p r o b a b i l i t y m e a s u r e i s logically m o r e a p p r o p r i a t e , it m i g h t seem that either m e a s u r e c o u l d be used for t h i n k i n g a b o u t h o w m u c h ' a l t r u i s m ' a g r a n d f a t h e r ' o u g h t ' t o d i s p e n s e t o his g r a n d s o n . I t d o e s m a t t e r , h o w e v e r , w h e n w e s t a r t t h i n k i n g a b o u t t h e v a r i a n c e as well as the m e a n . Several people h a v e pointed out that the fraction of g e n o m e o v e r l a p between parent and child is e x a c t l y e q u a l to the coefficient of relationship, w h e r e a s for a l l o t h e r r e l a t i v e s t h e c o e f f i c i e n t o f r e l a t i o n s h i p g i v e s o n l y t h e m e a n f i g u r e ; t h e a c t u a l f r a c t i o n s h a r e d m i g h t b e m o r e a n d i t m i g h t b e less.
An Agony in Five Fits
I t h a s b e e n s a i d , t h e r e f o r e , t h a t t h e c o e f f i c i e n t o f r e l a t i o n s h i p i s ' e x a c t ' for the
parent/child
relationship,
but
'probabilistic'
for
all
others.
But
this
u n i q u e n e s s of the p a r e n t / c h i l d relationship applies o n l y if we think in terms of fractions of g e n o m e s s h a r e d . If, i n s t e a d , we t h i n k in t e r m s of probabilities of sharing
particular
genes,
the
parent/child
relationship
is just
as
'prob-
abilistic' as a n y other. T h i s still m i g h t b e t h o u g h t n o t t o m a t t e r , a n d i n d e e d i t d o e s n o t m a t t e r u n t i l w e a r e t e m p t e d t o d r a w false c o n c l u s i o n s . O n e false c o n c l u s i o n t h a t has been d r a w n in the literature is that a parent, faced w i t h a c h o i c e b e t w e e n f e e d i n g its o w n c h i l d a n d f e e d i n g a full s i b l i n g e x a c t l y t h e s a m e a g e a s its o w n child
(and
w i t h e x a c t l y the same m e a n coefficient o f relationship),
s h o u l d f a v o u r its o w n c h i l d p u r e l y o n t h e g r o u n d s t h a t its g e n e t i c r e l a t e d n e s s is a ' s u r e t h i n g ' r a t h e r t h a n a ' g a m b l e ' . B u t it is o n l y the fraction of g e n o m e s h a r e d t h a t is a s u r e t h i n g . T h e probability t h a t a p a r t i c u l a r g e n e , in this c a s e a g e n e for a l t r u i s m , is i d e n t i c a l by d e s c e n t w i t h o n e in t h e o f f s p r i n g is j u s t as c h a n c y a s i n t h e c a s e o f t h e full s i b l i n g . I t i s n e x t t e m p t i n g t o t h i n k t h a t a n a n i m a l m i g h t try t o use c u e s t o estimate w h e t h e r a particular relative happens to share m a n y genes with itself or
not.
The
reasoning
is
conveniently
expressed
in
the
currently
fashionable style of subjective m e t a p h o r : ' A l l my brothers share, on average, h a l f m y g e n o m e , b u t s o m e o f m y brothers share m o r e than half a n d others less t h a n half. I f I c o u l d w o r k o u t w h i c h o n e s s h a r e m o r e t h a n half, I c o u l d s h o w favouritism towards them, a n d thereby benefit my genes. Brother A resembles me in hair colour, eye c o l o u r and several other features, whereas b r o t h e r B h a r d l y resembles me at all. T h e r e f o r e A p r o b a b l y shares more g e n e s w i t h m e . T h e r e f o r e I s h a l l feed A i n p r e f e r e n c e t o B . ' T h a t soliloquy was supposed to be spoken by an individual animal. T h e f a l l a c y i s q u i c k l y s e e n w h e n w e c o m p o s e a s i m i l a r s o l i l o q u y , this t i m e t o b e s p o k e n b y o n e o f H a m i l t o n ' s ' i n t e l l i g e n t ' genes, a g e n e ' f o r ' f e e d i n g b r o t h e r s : ' B r o t h e r A has c l e a r l y inherited my g e n e c o l l e a g u e s from the hair-colour d e p a r t m e n t a n d from the eye-colour department, but w h a t do I care about t h e m ? T h e g r e a t q u e s t i o n is, h a s A o r B i n h e r i t e d a c o p y o f me? H a i r c o l o u r a n d e y e c o l o u r tell m e n o t h i n g a b o u t t h a t u n l e s s I h a p p e n t o b e l i n k e d t o t h o s e o t h e r g e n e s . ' L i n k a g e is, t h e n , i m p o r t a n t h e r e , b u t i t i s j u s t a s i m p o r t a n t for t h e ' d e t e r m i n i s t i c ' p a r e n t / o f f s p r i n g r e l a t i o n s h i p a s for a n y ' p r o b a b i l i s t i c ' relationship. T h e fallacy i s c a l l e d the A c e o f S p a d e s F a l l a c y b e c a u s e o f the following analogy. Suppose it is important to me to know whether your hand of thirteen cards contains the ace of spades. If I am given no information, I k n o w that the o d d s are thirteen in fifty-two, or one in four, that y o u h a v e the a c e . T h i s is my first guess as to the p r o b a b i l i t y . If s o m e b o d y whispers to me that y o u h a v e a v e r y strong h a n d in spades, I w o u l d be justified in revising u p w a r d s my initial estimate of the p r o b a b i l i t y that y o u h a v e the a c e . If I am
An A g o n y in F i v e Fit:
191
told t h a t y o u h a v e t h e k i n g , q u e e n , j a c k , 1 0 , 8 , 6 , 5 , 4 , 3 a n d 2 , I w o u l d b e correct in c o n c l u d i n g that y o u h a v e a very strong h a n d in spades. But, so l o n g as the d e a l w a s honest, I w o u l d be a m u g if I therefore p l a c e d a bet on your h a v i n g the a c e ! ( A c t u a l l y the a n a l o g y is a bit unfair here, b e c a u s e the odds of y o u r h a v i n g the a c e are n o w three in f o r t y - t w o , substantially l o w e r t h a n t h e p r i o r o d d s o f o n e i n four.) I n t h e b i o l o g i c a l c a s e w e m a y a s s u m e t h a t , l i n k a g e a s i d e , k n o w l e d g e o f a b r o t h e r ' s e y e c o l o u r tells u s n o t h i n g , o n e w a y o r t h e o t h e r , a b o u t w h e t h e r h e s h a r e s a p a r t i c u l a r g e n e for b r o t h e r l y altruism. T h e r e is no reason to suppose that the theorists w h o h a v e p e r p e t r a t e d the biological versions o f the A c e o f S p a d e s F a l l a c y are b a d g a m b l e r s . I t w a s n ' t their p r o b a b i l i t y theory they g o t w r o n g , but their b i o l o g i c a l a s s u m p t i o n s . In particular, they assumed that an individual o r g a n i s m , as a coherent entity, w o r k s o n b e h a l f o f c o p i e s o f a l l t h e g e n e s i n s i d e it. I t w a s a s i f a n a n i m a l ' c a r e d ' a b o u t t h e s u r v i v a l o f c o p i e s o f its e y e - c o l o u r g e n e s , h a i r - c o l o u r g e n e s , e t c . I t i s b e t t e r t o a s s u m e t h a t o n l y g e n e s 'for c a r i n g ' c a r e , a n d t h e y o n l y c a r e about copies of themselves. I m u s t stress t h a t I
a m n o t s u g g e s t i n g t h a t e r r o r s o f this k i n d f o l l o w
i n e v i t a b l y from t h e i n c l u s i v e fitness a p p r o a c h . W h a t I d o s u g g e s t i s t h a t t h e y a r e t r a p s for the u n w a r y t h i n k e r a b o u t i n d i v i d u a l - l e v e l m a x i m i z a t i o n , w h i l e they
present
no
danger
to
the
thinker about
gene-level
maximization,
h o w e v e r u n w a r y . E v e n H a m i l t o n has m a d e a n error, afterwards pointed out b y himself, w h i c h I a t t r i b u t e t o i n d i v i d u a l - l e v e l t h i n k i n g . T h e p r o b l e m arises i n H a m i l t o n ' s c a l c u l a t i o n o f c o e f f i c i e n t s o f r e l a t i o n ship, r, in h y m e n o p t e r a n families. As is n o w well k n o w n , he m a d e brilliant use o f t h e o d d r v a l u e s r e s u l t i n g f r o m the h a p l o d i p l o i d s e x - d e t e r m i n i n g s y s t e m o f H y m e n o p t e r a , n o t a b l y t h e c u r i o u s f a c t t h a t r b e t w e e n sisters i s ¾ . But consider the relationship b e t w e e n a female a n d her father. O n e h a l f of the f e m a l e ' s g e n o m e i s i d e n t i c a l b y d e s c e n t w i t h t h a t o f h e r f a t h e r : t h e ' o v e r l a p ' o f h e r g e n o m e w i t h his i s ½ , a n d H a m i l t o n c o r r e c t l y g a v e ½ a s t h e coefficient o f r e l a t i o n s h i p b e t w e e n a f e m a l e a n d h e r f a t h e r . T h e t r o u b l e comes w h e n we look at the same relationship the other w a y r o u n d . W h a t is the
coefficient
of relationship
between
a
male
and
his
daughter?
One
n a t u r a l l y e x p e c t s it to be r e f l e x i v e , ½ a g a i n , b u t t h e r e is a d i f f i c u l t y . S i n c e a m a l e i s h a p l o i d , h e h a s h a l f a s m a n y g e n e s a s his d a u g h t e r i n t o t a l . H o w , then, c a n w e c a l c u l a t e the ' o v e r l a p ' , the fraction o f genes s h a r e d ? D o w e say that
the m a l e ' s g e n o m e o v e r l a p s w i t h
h a l f his d a u g h t e r ' s g e n o m e ,
and
therefore that r is ½? Or do we say that e v e r y single o n e of the m a l e ' s genes w i l l be f o u n d in his d a u g h t e r , a n d t h e r e f o r e r is 1 ? H a m i l t o n o r i g i n a l l y g a v e ½ a s t h e f i g u r e , t h e n i n 1 9 7 1 c h a n g e d his m i n d and g a v e 1. In 1964 he h a d tried to solve the difficulty of h o w to c a l c u l a t e an o v e r l a p b e t w e e n a h a p l o i d a n d a diploid g e n o t y p e by arbitrarily treating the male as a kind of h o n o r a r y diploid. ' T h e relationships c o n c e r n i n g males are
192 An
Agony
in
Five
Fits
w o r k e d o u t b y a s s u m i n g e a c h m a l e t o c a r r y a " c i p h e r " g e n e t o m a k e u p his diploid pair, one " c i p h e r " never being considered identical by descent with a n o t h e r ' ( H a m i l t o n 1 9 6 4 b ) . A t t h e t i m e , h e r e c o g n i z e d t h a t this p r o c e d u r e was
'arbitrary
in
the
sense
that
some
other
value
for
the
fundamental
m o t h e r - s o n a n d f a t h e r - d a u g h t e r link w o u l d h a v e g i v e n a n e q u a l l y coherent s y s t e m ' . H e l a t e r p r o n o u n c e d this m e t h o d o f c a l c u l a t i o n p o s i t i v e l y e r r o n e o u s a n d , i n a n a p p e n d i x a d d e d t o a r e p r i n t i n g o f his c l a s s i c p a p e r , g a v e the c o r r e c t r u l e s for c a l c u l a t i n g r i n h a p l o d i p l o i d s y s t e m s ( H a m i l t o n 1 9 7 1 b ) . H i s r e v i s e d m e t h o d o f c a l c u l a t i o n g i v e s r b e t w e e n a m a l e a n d his d a u g h t e r a s 1 ( n o t ½), a n d r b e t w e e n a m a l e a n d his b r o t h e r as ½ (not ¼). C r o z i e r ( 1 9 7 0 ) i n d e p e n d e n t l y c o r r e c t e d the error. T h e p r o b l e m w o u l d never h a v e arisen, and n o arbitrary 'honorary diploid' m e t h o d w o u l d h a v e b e e n c a l l e d for, h a d w e a l l a l o n g t h o u g h t i n t e r m s o f selfish
genes
maximizing
their
survival
rather
than
in
terms
o f selfish
i n d i v i d u a l s m a x i m i z i n g t h e i r i n c l u s i v e fitness. C o n s i d e r a n ' i n t e l l i g e n t g e n e ' sitting in
the b o d y of a m a l e h y m e n o p t e r a n ,
'contemplating'
an act of
a l t r u i s m t o w a r d s a d a u g h t e r . I t k n o w s for c e r t a i n t h a t t h e d a u g h t e r ' s b o d y c o n t a i n s a c o p y o f itself. I t d o e s n o t ' c a r e ' t h a t h e r g e n o m e c o n t a i n s t w i c e a s m a n y g e n e s a s its p r e s e n t , m a l e , b o d y .
It ignores the other half of her
genome,
when
secure
in
the
knowledge
that
the
daughter
reproduces,
m a k i n g g r a n d c h i l d r e n for t h e p r e s e n t m a l e , it, t h e i n t e l l i g e n t g e n e itself, h a s a 50 per cent c h a n c e of getting into e a c h grandchild. To the intelligent gene in a h a p l o i d m a l e , a g r a n d c h i l d is as v a l u a b l e as an o r d i n a r y offspring w o u l d be in a n o r m a l d i p l o i d system. By the s a m e token, a d a u g h t e r is twice as v a l u a b l e a s a d a u g h t e r w o u l d b e i n a n o r m a l d i p l o i d s y s t e m . F r o m the intelligent g e n e ' s p o i n t of v i e w , the coefficient of relationship b e t w e e n father and d a u g h t e r is i n d e e d 1, not ½. N o w look a t the relationship the other w a y r o u n d . T h e intelligent gene a g r e e s w i t h H a m i l t o n ' s o r i g i n a l f i g u r e o f ½ for t h e c o e f f i c i e n t o f r e l a t i o n s h i p b e t w e e n a f e m a l e h y m e n o p t e r a n a n d h e r f a t h e r . A g e n e sits in a f e m a l e a n d c o n t e m p l a t e s an act of altruism t o w a r d s the father of that female. It k n o w s t h a t i t h a s a n e q u a l c h a n c e o f h a v i n g c o m e from t h e f a t h e r o r from t h e m o t h e r o f t h e f e m a l e i n w h i c h i t sits. F r o m its p o i n t o f v i e w , t h e n , t h e c o e f f i c i e n t o f r e l a t i o n s h i p b e t w e e n its p r e s e n t b o d y a n d e i t h e r o f t h e t w o p a r e n t b o d i e s is A, T h e s a m e k i n d o f r e a s o n i n g l e a d s t o a n a n a l o g o u s n o n - r e f l e x i v e n e s s i n the b r o t h e r - s i s t e r r e l a t i o n s h i p . A g e n e in a f e m a l e sees a sister as h a v i n g ¾ of a c h a n c e o f c o n t a i n i n g itself, a n d a b r o t h e r a s h a v i n g ¼ o f a c h a n c e o f c o n t a i n i n g itself. A g e n e i n a m a l e , h o w e v e r , l o o k s a t t h e sister o f t h a t m a l e a n d sees t h a t s h e h a s ½ a c h a n c e of c o n t a i n i n g a c o p y of itself, n o t ¼ as Hamilton's original cipher gene ('honorary diploid') method gave. I b e l i e v e i t w i l l b e a d m i t t e d t h a t h a d H a m i l t o n u s e d his o w n ' i n t e l l i g e n t g e n e ' t h o u g h t e x p e r i m e n t w h e n c a l c u l a t i n g these c o e f f i c i e n t s o f r e l a t i o n s h i p ,
An Agony in Five Fits
193
i n s t e a d o f t h i n k i n g i n t e r m s o f individuals a s a g e n t s m a x i m i z i n g s o m e t h i n g , h e w o u l d h a v e g o t t h e r i g h t a n s w e r t h e first t i m e .
If these errors h a d b e e n
simple miscalculations it w o u l d obviously be p e d a n t i c to discuss t h e m , o n c e their original a u t h o r h a d p o i n t e d t h e m out. B u t they w e r e n o t m i s c a l c u lations, they w e r e based on a h i g h l y instructive c o n c e p t u a l error. T h e s a m e is true o f the n u m b e r e d ' M i s u n d e r s t a n d i n g s o f K i n S e l e c t i o n ' t h a t I q u o t e d before. I h a v e tried
to s h o w in
this c h a p t e r t h a t t h e c o n c e p t of fitness as a
technical term is a confusing o n e . It is confusing b e c a u s e it c a n l e a d to admitted
error,
as
in
the
case
of Hamilton's
original
calculation
of
h a p l o d i p l o i d coefficients o f r e l a t i o n s h i p , a n d a s i n t h e c a s e o f s e v e r a l o f m y '12 Misunderstandings of K i n Selection'. It is confusing because it can lead philosophers to think the w h o l e theory of n a t u r a l selection is a t a u t o l o g y . A n d i t i s c o n f u s i n g e v e n t o b i o l o g i s t s b e c a u s e i t h a s b e e n u s e d i n a t least five different senses, m a n y o f w h i c h h a v e b e e n m i s t a k e n for a t l e a s t o n e o f t h e others. Emerson, as we h a v e seen, confused fitness[3] w i t h fitness[1]. I n o w g i v e an
example
of a
confusion
o f fitness[3]
with
fitness[2].
Wilson
(1975)
p r o v i d e s a useful g l o s s a r y o f t e r m s n e e d e d b y s o c i o b i o l o g i s t s . U n d e r 'fitness' h e refers u s t o ' g e n e t i c f i t n e s s ' . W e t u r n t o ' g e n e t i c f i t n e s s ' a n d find i t d e f i n e d as ' T h e contribution to the next g e n e r a t i o n of o n e g e n o t y p e in a p o p u l a t i o n relative to the contributions of other g e n o t y p e s . ' E v i d e n t l y 'fitness' is b e i n g used i n the sense o f t h e p o p u l a t i o n g e n e t i c i s t ' s f i t n e s s [ 2 ] . B u t t h e n , i f w e l o o k u p ' i n c l u s i v e f i t n e s s ' i n the g l o s s a r y w e f i n d : ' T h e s u m o f a n i n d i v i d u a l ' s o w n f i t n e s s p l u s a l l its i n f l u e n c e o n f i t n e s s i n its r e l a t i v e s o t h e r t h a n d i r e c t descendants . . . '
Here,
f i t n e s s [ 3 ] (since
it
is
'the
individual's
applied
to
o w n fitness' must
individuals),
not
the
be
'classical'
g e n o t y p i c fitness
(fitness[2]) w h i c h i s t h e o n l y 'fitness' d e f i n e d i n t h e g l o s s a r y . T h e g l o s s a r y is, then, i n c o m p l e t e , a p p a r e n t l y because of a confusion b e t w e e n fitness of a g e n o t y p e a t a l o c u s (fitness[2])
and r e p r o d u c t i v e success of an i n d i v i d u a l
(fitness [ 3 ] ) . A s i f m y f i v e f o l d list w e r e n o t c o n f u s i n g e n o u g h a l r e a d y , i t m a y n e e d extending. For reasons concerned w i t h an interest in b i o l o g i c a l 'progress', Thoday
(1953)
seeks t h e 'fitness' o f a l o n g - t e r m l i n e a g e , d e f i n e d a s t h e
p r o b a b i l i t y t h a t t h e l i n e a g e w i l l c o n t i n u e for a v e r y l o n g t i m e s u c h a s 1 0
8
generations, and contributed to by such 'biotic' factors ( W i l l i a m s 1966) as ' g e n e t i c f l e x i b i l i t y ' . T h o d a y ' s f i t n e s s d o e s n o t c o r r e s p o n d t o a n y o f m y list o f five. T h e n a g a i n , the fitness[2] of p o p u l a t i o n geneticists is a d m i r a b l y c l e a r a n d useful, b u t m a n y p o p u l a t i o n g e n e t i c i s t s a r e , for r e a s o n s b e s t k n o w n t o themselves, very interested in another q u a n t i t y w h i c h is called the m e a n f i t n e s s o f a p o p u l a t i o n . W i t h i n the g e n e r a l c o n c e p t o f ' i n d i v i d u a l f i t n e s s ' , Brown ( 1 9 7 5 ; B r o w n & B r o w n 1981) wishes to m a k e a distinction b e t w e e n 'direct fitness' and 'indirect fitness'. D i r e c t fitness is the same as w h a t I am
194
An A g o n y in F i v e F i t s
c a l l i n g fitness[3].
I n d i r e c t fitness c a n b e c h a r a c t e r i z e d a s s o m e t h i n g like
f i t n e s s [ 4 ] m i n u s fitness[3], i.e. t h e c o m p o n e n t o f i n c l u s i v e fitness t h a t results from the r e p r o d u c t i o n of collateral relatives as opposed to direct descendants (I
presume
grandchildren
count
in
the
direct
component,
though
the
decision is a r b i t r a r y ) . B r o w n himself is clear a b o u t the m e a n i n g of the terms, b u t I believe they h a v e considerable p o w e r to confuse. For instance, they a p p e a r to lend w e i g h t to the v i e w (not held by B r o w n , but held by a distressing n u m b e r of other authors, e.g. G r a n t 1978, and several writers on 'helpers at the nest' in birds) that there is s o m e t h i n g u n p a r s i m o n i o u s about 'kin selection' selection'
(the
(the
'indirect component')
'direct
component'),
a
as compared with view
which
I
'individual
have
criticized
sufficiently before ( D a w k i n s 1 9 7 6 a , 1978a, 1 9 7 9 a ) . T h e r e a d e r m a y h a v e b e e n b e w i l d e r e d a n d i r r i t a t e d a t m y d r a w n o u t list o f f i v e o r m o r e s e p a r a t e m e a n i n g s o f f i t n e s s . I h a v e f o u n d this a p a i n f u l c h a p t e r to write, a n d I am a w a r e that it will not h a v e been easy to read. It m a y b e t h e last r e s o r t o f a p o o r w r i t e r t o b l a m e his s u b j e c t m a t t e r , b u t I r e a l l y d o b e l i e v e i t i s t h e c o n c e p t o f f i t n e s s i t s e l f w h i c h i s r e s p o n s i b l e for the a g o n y i n this c a s e . T h e p o p u l a t i o n g e n e t i c i s t s ' f i t n e s s [ 2 ] a s i d e , the c o n c e p t o f fitness as a p p l i e d to i n d i v i d u a l organisms has b e c o m e forced and contrived. Before
Hamilton's
revolution,
our
world
was
peopled
by
individual
organisms w o r k i n g single-mindedly to keep themselves alive and to have c h i l d r e n . I n t h o s e d a y s i t w a s n a t u r a l t o m e a s u r e s u c c e s s i n this u n d e r t a k i n g at the level of the individual organism.
H a m i l t o n c h a n g e d all t h a t b u t
unfortunately,
ideas
conclusion
instead
and
of following
sweeping
the
his
individual
through
organism
from
to its
their
logical
pedestal
as
n o t i o n a l a g e n t o f m a x i m i z a t i o n , h e e x e r t e d his g e n i u s i n d e v i s i n g a m e a n s o f r e s c u i n g the i n d i v i d u a l . He c o u l d h a v e persisted in s a y i n g : g e n e survival is w h a t m a t t e r s ; let us e x a m i n e w h a t a g e n e w o u l d h a v e to do in order to p r o p a g a t e c o p i e s o f itself. I n s t e a d h e , i n effect, s a i d : g e n e s u r v i v a l i s w h a t matters; w h a t is the m i n i m u m c h a n g e we h a v e to m a k e to our old v i e w of w h a t i n d i v i d u a l s m u s t d o , i n o r d e r t h a t w e m a y c l i n g o n t o o u r i d e a o f the individual
as
the
unit
of
action?
The
result—inclusive fitness—was
t e c h n i c a l l y correct, but c o m p l i c a t e d a n d easy to misunderstand. I shall avoid m e n t i o n i n g f i t n e s s a g a i n i n this b o o k , w h i c h I trust w i l l m a k e for easier reading.
The
next
p h e n o t y p e itself.
three
chapters
develop
the
theory
o f the
extended
11 T h e Genetical Evolution of A n i m a l Artefacts
W h a t do we really m e a n by the p h e n o t y p i c
effect o f a g e n e ?
A
smattering of molecular biology m a y suggest one kind of answer. E a c h gene c o d e s for t h e s y n t h e s i s o f o n e p r o t e i n c h a i n . I n a p r o x i m a l sense t h a t p r o t e i n i s its p h e n o t y p i c effect. M o r e d i s t a l effects l i k e e y e c o l o u r o r b e h a v i o u r a r e , i n t h e i r t u r n , effects o f t h e p r o t e i n f u n c t i o n i n g a s a n e n z y m e . S u c h a s i m p l e a c c o u n t does not, h o w e v e r , b e a r m u c h s e a r c h i n g analysis. T h e 'effect' o f a n y would-be cause can be g i v e n m e a n i n g only in terms of a c o m p a r i s o n , e v e n if o n l y a n i m p l i e d c o m p a r i s o n , w i t h a t least o n e a l t e r n a t i v e c a u s e . I t i s s t r i c t l y i n c o m p l e t e t o s p e a k o f b l u e e y e s a s ' t h e effect' o f a g i v e n g e n e G 1 . I f w e s a y such
a
thing,
we
really
imply
the
potential
existence
of at
least
one
a l t e r n a t i v e a l l e l e , c a l l i t G2, a n d a t least o n e a l t e r n a t i v e p h e n o t y p e , P 2 , i n this c a s e , s a y , b r o w n e y e s . I m p l i c i t l y w e a r e m a k i n g a s t a t e m e n t a b o u t a r e l a t i o n b e t w e e n a p a i r of g e n e s {G1, G2} a n d a p a i r of d i s t i n g u i s h a b l e phenotypes { P 1 , P2}, in an environment w h i c h either is constant or varies in a
non-systematic
way
so
that
its
contribution
randomizes
out.
' E n v i r o n m e n t ' , i n t h a t last c l a u s e , i s t a k e n t o i n c l u d e a l l t h e g e n e s a t o t h e r loci t h a t m u s t
b e p r e s e n t i n o r d e r for
P1
or
P2
to
be expressed.
Our
s t a t e m e n t is t h a t t h e r e is a s t a t i s t i c a l t e n d e n c y for i n d i v i d u a l s w i t h G1 to be more likely than individuals with G2 to show P1 (rather than P 2 ) . Of course t h e r e is no n e e d to d e m a n d t h a t P1 s h o u l d always be a s s o c i a t e d w i t h G1, n o r that G1 should a l w a y s lead to P1: in the real w o r l d outside l o g i c textbooks, the s i m p l e c o n c e p t s o f ' n e c e s s a r y ' a n d ' s u f f i c i e n t ' m u s t u s u a l l y b e r e p l a c e d b y statistical e q u i v a l e n t s . S u c h an insistence that p h e n o t y p e s are not caused by g e n e s , b u t o n l y p h e n o t y p i c differences c a u s e d b y g e n e d i f f e r e n c e s ( J e n s e n 1 9 6 1 ; H i n d e 1 9 7 5 ) m a y seem to w e a k e n the c o n c e p t of genetic d e t e r m i n a t i o n to the point w h e r e i t ceases t o b e i n t e r e s t i n g . T h i s i s far f r o m t h e c a s e , a t l e a s t i f t h e s u b j e c t o f o u r interest i s n a t u r a l s e l e c t i o n , b e c a u s e n a t u r a l s e l e c t i o n t o o i s c o n c e r n e d w i t h differences ( C h a p t e r 2 ) . N a t u r a l s e l e c t i o n i s t h e p r o c e s s b y w h i c h s o m e alleles o u t - p r o p a g a t e t h e i r a l t e r n a t i v e s , a n d t h e i n s t r u m e n t s b y w h i c h t h e y 195
196
T h e Genetical Evolution of A n i m a l Artefacts
a c h i e v e this a r e t h e i r p h e n o t y p i c effects. I t f o l l o w s t h a t p h e n o t y p i c effects c a n a l w a y s b e t h o u g h t o f a s relative t o a l t e r n a t i v e p h e n o t y p i c effects. It is c u s t o m a r y to speak as if differences a l w a y s m e a n differences b e t w e e n i n d i v i d u a l bodies or other discrete 'vehicles'. T h e purpose of the next three chapters is to s h o w that we c a n e m a n c i p a t e the c o n c e p t of the p h e n o t y p i c d i f f e r e n c e f r o m t h a t o f t h e d i s c r e t e v e h i c l e a l t o g e t h e r , a n d this i s t h e m e a n i n g o f t h e title ' e x t e n d e d p h e n o t y p e ' . I s h a l l s h o w t h a t t h e o r d i n a r y l o g i c o f g e n e t i c t e r m i n o l o g y leads i n e v i t a b l y to the c o n c l u s i o n that genes c a n be said t o h a v e extended p h e n o t y p i c effects, effects w h i c h n e e d n o t b e e x p r e s s e d a t the level of a n y particular v e h i c l e . F o l l o w i n g an earlier paper ( D a w k i n s 1978a) I shall take a step-by-step a p p r o a c h to the e x t e n d e d p h e n o t y p e , b e g i n n i n g w i t h c o n v e n t i o n a l e x a m p l e s o f ' o r d i n a r y ' p h e n o t y p i c effects a n d g r a d u a l l y e x t e n d i n g t h e c o n c e p t o f t h e p h e n o t y p e o u t w a r d s s o t h a t the c o n t i n u i t y i s easy to a c c e p t . T h e i d e a of the genetic d e t e r m i n a t i o n of a n i m a l artefacts is a d i d a c t i c a l l y useful i n t e r m e d i a t e e x a m p l e , a n d this w i l l b e t h e m a i n t o p i c o f this c h a p t e r . B u t first, c o n s i d e r a g e n e A w h o s e i m m e d i a t e m o l e c u l a r effect is the s y n t h e s i s o f a b l a c k p r o t e i n w h i c h d i r e c t l y c o l o u r s t h e skin o f a n a n i m a l b l a c k . T h e n t h e g e n e ' s o n l y p r o x i m a l effect, i n t h e m o l e c u l a r b i o l o g i s t ' s s i m p l e s e n s e , is t h e s y n t h e s i s of this o n e b l a c k p r o t e i n . B u t is A a g e n e 'for b e i n g b l a c k ' ? T h e point I w a n t to m a k e is that, as a matter of definition, that d e p e n d s o n h o w t h e p o p u l a t i o n v a r i e s . A s s u m e t h a t A h a s a n a l l e l e A', w h i c h fails t o s y n t h e s i z e t h e b l a c k p i g m e n t , s o t h a t i n d i v i d u a l s h o m o z y g o u s for A ' t e n d t o b e w h i t e . I n this c a s e A i s t r u l y a g e n e ' f o r ' b e i n g b l a c k , i n t h e sense i n w h i c h I w i s h t o use t h e p h r a s e . B u t i t m a y a l t e r n a t i v e l y b e t h a t a l l the v a r i a t i o n in skin c o l o u r that a c t u a l l y occurs in the p o p u l a t i o n is d u e to v a r i a t i o n at a q u i t e d i f f e r e n t l o c u s , B. B's i m m e d i a t e b i o c h e m i c a l effect is t h e synthesis of a protein w h i c h is not a b l a c k p i g m e n t , but w h i c h acts as an e n z y m e , o n e o f w h o s e i n d i r e c t effects (in c o m p a r i s o n w i t h its a l l e l e B'), a t s o m e distant r e m o v e , is the facilitation of the synthesis by A of the black p i g m e n t in skin cells. To be sure, A, the g e n e w h o s e protein p r o d u c t is the b l a c k pigment, is n e c e s s a r y i n o r d e r for a n i n d i v i d u a l t o b e b l a c k : s o a r e t h o u s a n d s o f o t h e r g e n e s , i f o n l y b e c a u s e t h e y a r e n e c e s s a r y t o m a k e t h e i n d i v i d u a l exist a t a l l . B u t I s h a l l n o t c a l l A a g e n e for b l a c k n e s s u n l e s s s o m e of t h e v a r i a t i o n in the p o p u l a t i o n i s d u e t o l a c k o f A . I f a l l i n d i v i d u a l s , w i t h o u t fail, h a v e A , a n d t h e o n l y reason individuals are not b l a c k is that they h a v e B' rather than B, we s h a l l s a y t h a t B, b u t n o t A, is a g e n e for b l a c k n e s s . If t h e r e is v a r i a t i o n at b o t h l o c i a f f e c t i n g b l a c k n e s s , w e s h a l l refer t o b o t h A a n d B a s g e n e s for blackness. T h e point that is r e l e v a n t here is that both A a n d B are potentially e n t i t l e d t o b e c a l l e d g e n e s for b l a c k n e s s , d e p e n d i n g o n t h e a l t e r n a t i v e s t h a t exist in the p o p u l a t i o n . T h e fact that the causal c h a i n linking A to the p r o d u c t i o n o f t h e b l a c k p i g m e n t m o l e c u l e i s s h o r t , w h i l e t h a t for B i s l o n g
The Genetical Evolution of A n i m a l Artefacts
197
a n d t o r t u o u s , i s i r r e l e v a n t . M o s t g e n e effects s e e n b y w h o l e a n i m a l b i o l o g i s t s , a n d all t h o s e s e e n b y e t h o l o g i s t s , a r e l o n g a n d t o r t u o u s . A geneticist c o l l e a g u e has a r g u e d that there are virtually no b e h a v i o u r g e n e t i c traits, b e c a u s e a l l t h o s e so-far d i s c o v e r e d h a v e t u r n e d o u t t o b e ' b y p r o d u c t s ' o f m o r e f u n d a m e n t a l m o r p h o l o g i c a l o r p h y s i o l o g i c a l effects. But
what
on
physiological
earth or
does
he
think
behavioural,
any
if not
genetic
a
trait
'byproduct'
is,
morphological,
of something
more
f u n d a m e n t a l ? I f w e t h i n k t h e m a t t e r t h r o u g h w e find t h a t a l l g e n e t i c effects are ' b y p r o d u c t s ' e x c e p t protein molecules. R e t u r n i n g t o the b l a c k skin e x a m p l e , i t i s e v e n p o s s i b l e t h a t the c h a i n o f c a u s a t i o n l i n k i n g a g e n e s u c h a s B t o its b l a c k - s k i n n e d p h e n o t y p e m i g h t involve a b e h a v i o u r a l link. S u p p o s e that A c a n synthesize b l a c k p i g m e n t only in
the presence of sunlight,
and suppose
that B works
by
making
i n d i v i d u a l s seek s u n l i g h t , i n c o m p a r i s o n w i t h B ' w h i c h m a k e s t h e m s e e k shade. B individuals will then tend to be b l a c k e r than B' individuals, b e c a u s e they spend m o r e time in
t h e s u n . B i s still,
by existing t e r m i n o l o g i c a l
c o n v e n t i o n , a g e n e 'for b l a c k n e s s ' , n o less t h a n i t w o u l d b e i f its c a u s a l c h a i n involved internal biochemistry only, rather than an 'external' behavioural loop. I n d e e d , a geneticist in the p u r e sense of the w o r d n e e d not c a r e a b o u t the d e t a i l e d p a t h w a y f r o m g e n e t o p h e n o t y p i c effect. S t r i c t l y s p e a k i n g , a geneticist w h o concerns h i m s e l f w i t h these interesting matters is t e m p o r a r i l y w e a r i n g the h a t o f a n e m b r y o l o g i s t . T h e p u r e g e n e t i c i s t i s c o n c e r n e d w i t h e n d p r o d u c t s , a n d i n p a r t i c u l a r w i t h d i f f e r e n c e s b e t w e e n a l l e l e s i n t h e i r effects o n e n d p r o d u c t s . N a t u r a l s e l e c t i o n ' s c o n c e r n s a r e p r e c i s e l y t h e s a m e , for natural
selection
'works
on
outcomes'
(Lehrman
1970).
The
interim
c o n c l u s i o n i s t h a t w e a r e a l r e a d y a c c u s t o m e d t o p h e n o t y p i c effects b e i n g attached to their genes by long and devious chains of causal connection, therefore
further
extensions
overstretch our credulity. further
extension,
by
of
the
concept
of
phenotype
should
not
T h i s c h a p t e r t a k e s t h e first s t e p t o w a r d s s u c h
looking
at
animal
artefacts
as
examples
of the
phenotypic expression of genes. T h e fascinating subject of a n i m a l artefacts is r e v i e w e d by Hansell press).
He
shows
that
artefacts
provide
useful
case
studies
for
(in
several
p r i n c i p l e s o f g e n e r a l e t h o l o g i c a l i m p o r t a n c e . T h i s c h a p t e r uses t h e e x a m p l e o f artefacts in the service of e x p l a i n i n g a n o t h e r p r i n c i p l e , that of the e x t e n d e d phenotype. C o n s i d e r a h y p o t h e t i c a l species of caddis-fly w h o s e larvae build houses out of stones w h i c h t h e y select from those a v a i l a b l e on the b o t t o m of the s t r e a m . distinct
We
colours
might
observe
of house,
dark
that
the
and
light.
population By
contains
breeding
two
rather
experiments
we
establish that the c h a r a c t e r s 'dark house' a n d 'light h o u s e ' b r e e d true in some simple house.
In
M e n d e l i a n fashion, say w i t h d a r k house d o m i n a n t to light
principle
recombination
data,
it
ought where
to the
be
possible
genes
for
to
discover,
house
colour
by sit
analysing on
the
198
T h e Genetical Evolution of A n i m a l Artefacts
c h r o m o s o m e s . T h i s is, o f c o u r s e , h y p o t h e t i c a l . I d o n o t k n o w o f a n y g e n e t i c w o r k o n c a d d i s h o u s e s , a n d i t w o u l d b e difficult t o d o b e c a u s e a d u l t s a r e difficult t o b r e e d i n c a p t i v i t y ( M . H . H a n s e l l , personal c o m m u n i c a t i o n ) . But m y p o i n t i s t h a t , i f t h e p r a c t i c a l difficulties c o u l d b e o v e r c o m e , n o b o d y would
be
very
surprised
if house
colour did
turn
out
to
be
a
simple
Mendelian character in accordance with my thought experiment. (Actually, c o l o u r is a slightly unfortunate e x a m p l e to h a v e chosen, since c a d d i s vision is p o o r a n d they a l m o s t c e r t a i n l y ignore visual cues in c h o o s i n g stones. R a t h e r t h a n use a m o r e r e a l i s t i c e x a m p l e l i k e s t o n e s h a p e ( H a n s e l l ) , I s t a y w i t h c o l o u r for t h e s a k e o f t h e a n a l o g y w i t h t h e b l a c k p i g m e n t d i s c u s s e d a b o v e . ) T h e i n t e r e s t i n g s e q u e l i s this. H o u s e c o l o u r i s d e t e r m i n e d b y t h e c o l o u r o f the stones c h o s e n from the stream bed by the l a r v a , not by the b i o c h e m i c a l synthesis of a b l a c k p i g m e n t . T h e genes d e t e r m i n i n g house colour must work v i a t h e b e h a v i o u r a l m e c h a n i s m t h a t c h o o s e s s t o n e s , p e r h a p s v i a the e y e s . S o m u c h w o u l d b e a g r e e d b y a n y e t h o l o g i s t . A l l t h a t this c h a p t e r a d d s i s a logical
point:
once we have accepted
that
t h e r e a r e g e n e s for b u i l d i n g
b e h a v i o u r , t h e r u l e s o f e x i s t i n g t e r m i n o l o g y i m p l y t h a t t h e a r t e f a c t itself should be treated as part of the p h e n o t y p i c expression of genes in the a n i m a l . T h e stones are outside the b o d y of the o r g a n i s m , yet l o g i c a l l y such a g e n e is a g e n e ' f o r ' h o u s e c o l o u r , i n e x a c t l y a s s t r o n g a sense a s t h e h y p o t h e t i c a l g e n e B w a s for s k i n c o l o u r . A n d B w a s i n d e e d a g e n e for skin c o l o u r , e v e n t h o u g h i t w o r k e d b y m e d i a t i n g s u n - s e e k i n g b e h a v i o u r , i n e x a c t l y a s s t r o n g a sense a s a g e n e ' f o r ' a l b i n i s m i s c a l l e d a g e n e for s k i n c o l o u r . T h e l o g i c i s i d e n t i c a l i n all three cases. We h a v e taken the first step in e x t e n d i n g the c o n c e p t of a g e n e ' s p h e n o t y p i c effect o u t s i d e t h e i n d i v i d u a l b o d y . I t w a s n o t a difficult step to t a k e , b e c a u s e we h a d a l r e a d y softened up o u r resistance by realizing t h a t e v e n n o r m a l ' i n t e r n a l ' p h e n o t y p i c effects m a y lie a t t h e e n d o f l o n g , r a m i f i e d , a n d i n d i r e c t , c a u s a l c h a i n s . L e t u s n o w s t e p o u t a little f u r t h e r . T h e h o u s e o f a c a d d i s i s s t r i c t l y n o t a p a r t o f its c e l l u l a r b o d y , b u t i t d o e s fit s n u g l y r o u n d the b o d y .
I f the b o d y i s r e g a r d e d a s a g e n e v e h i c l e , o r
s u r v i v a l m a c h i n e , i t i s e a s y t o see t h e s t o n e h o u s e a s a k i n d o f e x t r a p r o t e c t i v e w a l l , i n a f u n c t i o n a l s e n s e t h e o u t e r p a r t o f the v e h i c l e . I t j u s t h a p p e n s t o b e m a d e of stone rather than chitin. N o w consider a spider sitting at the centre of her w e b . If she is r e g a r d e d as a g e n e v e h i c l e , her w e b is not a part of that v e h i c l e i n q u i t e t h e s a m e o b v i o u s sense a s a c a d d i s h o u s e , s i n c e w h e n she t u r n s r o u n d t h e w e b d o e s n o t t u r n w i t h h e r . B u t the d i s t i n c t i o n i s c l e a r l y a frivolous one.
In
a v e r y real
sense h e r w e b i s a t e m p o r a r y f u n c t i o n a l
extension of her b o d y , a h u g e extension of the effective c a t c h m e n t area of her predatory organs. O n c e a g a i n , I k n o w of no genetic analysis of spider w e b m o r p h o l o g y , but there is n o t h i n g difficult in p r i n c i p l e a b o u t i m a g i n i n g such an analysis. It is known
that
individual
spiders
have
consistent
idiosyncrasies
which
are
r e p e a t e d i n w e b after w e b . O n e f e m a l e Zygiella-x-notata, for i n s t a n c e , w a s
The Genetical Evolution of A n i m a l Artefacts
199
seen t o b u i l d m o r e t h a n 100 w e b s , a l l l a c k i n g a p a r t i c u l a r c o n c e n t r i c r i n g (Witt,
Read
&
Peakall
1968).
N o b o d y familiar with
the
literature
on
behaviour genetics (e.g. M a n n i n g 1971) w o u l d be surprised if the observed idiosyncrasies of individual
spiders
Indeed, our belief that spiders'
turned
out
to
have
webs have evolved
a
genetic
basis.
t h e i r efficient s h a p e
through natural selection necessarily c o m m i t s us to a b e l i e f that, at least in the p a s t , w e b v a r i a t i o n m u s t h a v e b e e n u n d e r g e n e t i c i n f l u e n c e ( C h a p t e r 2 ) . A s i n the c a s e o f t h e c a d d i s h o u s e s , t h e g e n e s m u s t h a v e w o r k e d v i a b u i l d i n g behaviour,
before
neuroanatomy,
that
before
in
embryonic
that perhaps v i a cell
development
perhaps
membrane biochemistry.
via By
w h a t e v e r e m b r y o l o g i c a l routes the genes m a y w o r k in detail, the s m a l l e x t r a step from b e h a v i o u r t o w e b i s n o t a n y m o r e d i f f i c u l t t o c o n c e i v e o f t h a n t h e m a n y c a u s a l steps w h i c h p r e c e d e d t h e b e h a v i o u r a l effect, a n d w h i c h lie b u r i e d i n the l a b y r i n t h o f n e u r o e m b r y o l o g y . N o b o d y has a n y t r o u b l e u n d e r s t a n d i n g the i d e a o f g e n e t i c c o n t r o l o f m o r p h o l o g i c a l differences. N o w a d a y s few people h a v e trouble u n d e r s t a n d i n g that
there
is,
in
principle,
no
difference
between
genetic
control
of
morphology and genetic control of behaviour, and we are unlikely to be misled by unfortunate statements such as 'Strictly s p e a k i n g , it is the brain (rather than the b e h a v i o u r ) that is g e n e t i c a l l y i n h e r i t e d '
( P u g h in press).
T h e p o i n t h e r e is, o f c o u r s e , t h a t i f t h e r e i s a n y sense i n w h i c h t h e b r a i n i s inherited, b e h a v i o u r m a y b e inherited i n e x a c t l y the s a m e sense. I f w e object to calling behaviour inherited, as some do on tenable grounds, then we must, to be consistent, object to c a l l i n g brains inherited too. A n d if we do d e c i d e to allow that both m o r p h o l o g y and b e h a v i o u r m a y b e inherited, w e c a n n o t reasonably at the s a m e time object to c a l l i n g caddis house c o l o u r a n d spider w e b shape inherited. T h e extra step from b e h a v i o u r t o e x t e n d e d p h e n o t y p e , i n this c a s e t h e s t o n e h o u s e o r t h e w e b , i s a s c o n c e p t u a l l y n e g l i g i b l e a s t h e step f r o m m o r p h o l o g y t o b e h a v i o u r . From
the
viewpoint
o f this
book an
animal
artefact,
like
any other
phenotypic product whose variation is influenced by a gene, can be regarded as a p h e n o t y p i c tool by w h i c h that g e n e c o u l d p o t e n t i a l l y l e v e r itself into the next generation. A g e n e m a y so lever itself by a d o r n i n g the tail of a m a l e bird of paradise w i t h a sexually attractive blue feather, or by c a u s i n g a m a l e b o w e r b i r d t o p a i n t his b o w e r w i t h p i g m e n t c r u s h e d i n his b i l l o u t o f b l u e b e r r i e s . T h e d e t a i l s m a y b e d i f f e r e n t i n t h e t w o c a s e s b u t t h e effect, f r o m t h e gene's point of v i e w , is the same. G e n e s that a c h i e v e sexually attractive p h e n o t y p i c effects w h e n c o m p a r e d w i t h t h e i r a l l e l e s a r e f a v o u r e d , a n d i t i s t r i v i a l w h e t h e r t h o s e p h e n o t y p i c effects a r e ' c o n v e n t i o n a l ' o r
'extended'.
T h i s is underlined by the interesting o b s e r v a t i o n that b o w e r bird species w i t h especially splendid b o w e r s tend to h a v e relatively d r a b p l u m a g e , w h i l e those species w i t h r e l a t i v e l y b r i g h t p l u m a g e
tend
to build
less e l a b o r a t e a n d
s p e c t a c u l a r b o w e r s ( G i l l i a r d 1 9 6 3 ) . I t i s a s t h o u g h s o m e s p e c i e s h a v e shifted
T h e Genetical Evolution of Animal Artefacts
200
part
of the
burden
of adaptation
from
bodily
phenotype
to
extended
phenotype. S o far t h e p h e n o t y p i c effects w e h a v e b e e n c o n s i d e r i n g h a v e e x t e n d e d o n l y a few y a r d s a w a y from the initiating genes, but in principle there is no reason w h y t h e p h e n o t y p i c l e v e r s o f g e n e p o w e r s h o u l d n o t r e a c h o u t for m i l e s . A b e a v e r d a m i s b u i l t c l o s e t o t h e l o d g e , b u t t h e effect o f t h e d a m m a y b e t o flood an a r e a thousands of square metres in extent. As to the a d v a n t a g e of t h e p o n d f r o m t h e b e a v e r ' s p o i n t o f v i e w , t h e best g u e s s s e e m s t o b e t h a t i t i n c r e a s e s t h e d i s t a n c e t h e b e a v e r c a n t r a v e l b y w a t e r , w h i c h i s safer t h a n t r a v e l l i n g b y l a n d , a n d e a s i e r for t r a n s p o r t i n g w o o d . A b e a v e r t h a t lives b y a s t r e a m q u i c k l y e x h a u s t s t h e s u p p l y o f food trees l y i n g a l o n g t h e s t r e a m b a n k w i t h i n a r e a s o n a b l e d i s t a n c e . B y b u i l d i n g a d a m a c r o s s t h e s t r e a m the b e a v e r c r e a t e s a l a r g e s h o r e l i n e w h i c h i s a v a i l a b l e for safe a n d e a s y f o r a g i n g w i t h o u t t h e b e a v e r h a v i n g t o m a k e l o n g a n d difficult j o u r n e y s o v e r l a n d . interpretation
is
right,
the
lake
may
be regarded
as
a
huge
I f this
extended
p h e n o t y p e , e x t e n d i n g the f o r a g i n g r a n g e of the b e a v e r in a w a y w h i c h is s o m e w h a t a n a l o g o u s to the w e b of the spider. As in the case of the spider w e b , n o b o d y h a s d o n e a g e n e t i c s t u d y o f b e a v e r d a m s , b u t w e r e a l l y d o not need to in o r d e r to c o n v i n c e ourselves of the rightness of r e g a r d i n g the d a m , a n d the lake, as part of the p h e n o t y p i c expression of b e a v e r genes. It is e n o u g h that we a c c e p t that b e a v e r dams must h a v e evolved by D a r w i n i a n n a t u r a l s e l e c t i o n : this c a n o n l y h a v e c o m e a b o u t i f d a m s h a v e v a r i e d u n d e r the control of genes ( C h a p t e r 2). Just by t a l k i n g a b o u t a few e x a m p l e s of a n i m a l artefacts, then, we h a v e p u s h e d the c o n c e p t u a l r a n g e of the g e n e ' s p h e n o t y p e out to m a n y miles. But n o w we c o m e up a g a i n s t a c o m p l i c a t i o n . A b e a v e r d a m is usually the w o r k of more
than
one
individual.
Mated
pairs
routinely
work
together,
and
s u c c e s s i v e g e n e r a t i o n s o f a f a m i l y m a y i n h e r i t r e s p o n s i b i l i t y for t h e u p k e e p a n d extension of a ' t r a d i t i o n a l ' d a m - c o m p l e x c o m p r i s i n g a staircase of half a d o z e n d a m s stepping d o w n s t r e a m , and m a y b e several 'canals' as well. N o w it w a s easy to a r g u e that a c a d d i s house, or a spider w e b , w a s the extended p h e n o t y p e o f t h e g e n e s o f t h e s i n g l e i n d i v i d u a l t h a t b u i l t it. B u t w h a t a r e w e to m a k e of an artefact that is the j o i n t production of a pair of animals or a f a m i l y ? W o r s e , consider the m o u n d built by a c o l o n y of c o m p a s s termites, a tombstone-shaped
slab,
one of a vista of similar
m o n o l i t h s all oriented
p r e c i s e l y n o r t h - s o u t h , a n d r i s i n g to a h e i g h t t h a t d w a r f s its b u i l d e r s as a mile-high skyscraper w o u l d d w a r f a m a n (von Frisch 1 9 7 5 ) . It is built by p e r h a p s a m i l l i o n t e r m i t e s , s e p a r a t e d b y t i m e i n t o c o h o r t s , like m e d i e v a l m a s o n s w h o c o u l d w o r k a lifetime on one c a t h e d r a l a n d n e v e r meet their c o l l e a g u e s t h a t w o u l d c o m p l e t e it. A p a r t i s a n o f t h e i n d i v i d u a l a s t h e u n i t o f s e l e c t i o n m i g h t p a r d o n a b l y ask e x a c t l y whose e x t e n d e d p h e n o t y p e t h e t e r m i t e m o u n d is supposed to be. I f this
consideration
seems
to
complicate
the
idea
of the
extended
T h e Genetical Evolution of A n i m a l Artefacts
20I
p h e n o t y p e b e y o n d all reason, I c a n o n l y point o u t that e x a c t l y the s a m e problem
has
always
arisen
with
'conventional'
phenotypes.
We
are
thoroughly a c c u s t o m e d to the i d e a that a g i v e n p h e n o t y p i c entity, an o r g a n say, or a b e h a v i o u r pattern, is influenced by a large n u m b e r of g e n e s w h o s e effects i n t e r a c t i n a d d i t i v e o r m o r e c o m p l e x w a y s . H u m a n h e i g h t a t a g i v e n a g e i s affected b y g e n e s a t m a n y l o c i , i n t e r a c t i n g w i t h e a c h o t h e r a n d w i t h d i e t a r y a n d o t h e r e n v i r o n m e n t a l effects. T h e h e i g h t o f a t e r m i t e m o u n d a t a given mound-age
is,
no doubt,
also controlled
by
many
environmental
factors a n d m a n y g e n e s , a d d i n g t o o r m o d i f y i n g e a c h o t h e r s ' effects. I t i s incidental
that in
the case of the
termite m o u n d
t h e proximal
theatre of
w i t h i n - b o d y g e n e effects h a p p e n s t o b e d i s t r i b u t e d a m o n g t h e c e l l s o f a l a r g e number of worker bodies. I f w e a r e g o i n g t o w o r r y a b o u t p r o x i m a l effects, t h e g e n e s i n f l u e n c i n g m y height act i n w a y s that are distributed a m o n g m a n y separate cells. M y b o d y i s full o f g e n e s , w h i c h h a p p e n t o b e i d e n t i c a l l y d i s t r i b u t e d a m o n g m y m a n y s o m a t i c c e l l s . E a c h g e n e e x e r t s its effects a t t h e c e l l u l a r l e v e l , o n l y a m i n o r i t y o f g e n e s e x p r e s s i n g t h e m s e l v e s i n a n y o n e c e l l . T h e s u m m e d effects o f a l l these effects o n c e l l s , t o g e t h e r w i t h s i m i l a r effects f r o m t h e e n v i r o n m e n t , m a y b e m e a s u r e d a s m y t o t a l h e i g h t . S i m i l a r l y , a t e r m i t e m o u n d i s full o f g e n e s . T h e s e genes, too, are distributed a m o n g the nuclei of a l a r g e n u m b e r of cells. It h a p p e n s that the cells are not c o n t a i n e d in q u i t e s u c h a c o m p a c t single u n i t a s the cells i n m y b o d y , b u t e v e n h e r e t h e d i f f e r e n c e i s n o t v e r y g r e a t . Termites m o v e around relative to each other more than h u m a n organs do, b u t i t i s n o t u n k n o w n for h u m a n c e l l s t o t r a v e l r a p i d l y a b o u t t h e b o d y i n pursuance
o f their
errands,
for
instance
phagocytes
hunting
down
and
e n g u l f i n g m i c r o s c o p i c p a r a s i t e s . A m o r e i m p o r t a n t d i f f e r e n c e (in t h e c a s e o f a termite m o u n d , t h o u g h not in the case of a c o r a l r e e f built by a c l o n e of individuals)
is
that
the
cells
in
the
termite
mound
are
gathered
into
genetically heterogeneous p a c k a g e s : each individual termite is a clone of cells b u t a different c l o n e f r o m a l l o t h e r i n d i v i d u a l s i n t h e nest. T h i s , h o w ever, is only a relative c o m p l i c a t i o n . F u n d a m e n t a l l y w h a t is g o i n g on is that genes, c o m p a r e d with their alleles, exert quantitative, m u t u a l l y interacting, m u t u a l l y m o d i f y i n g , effects o n a s h a r e d p h e n o t y p e , t h e m o u n d . T h e y d o this p r o x i m a l l y b y c o n t r o l l i n g the c h e m i s t r y o f cells i n w o r k e r bodies, a n d h e n c e worker b e h a v i o u r . T h e principle is the same, w h e t h e r the cells h a p p e n to be o r g a n i z e d into one large h o m o g e n e o u s c l o n e , as in the h u m a n b o d y , or into a heterogeneous collection of clones, as in the termite m o u n d . I postpone until l a t e r t h e c o m p l i c a t i n g p o i n t t h a t a t e r m i t e b o d y i t s e l f is a ' c o l o n y ' , w i t h a s u b s t a n t i a l f r a c t i o n o f its g e n e t i c r e p l i c a t o r s c o n t a i n e d i n s y m b i o t i c p r o t o z o a or bacteria. W h a t , then, w o u l d a genetics of termite m o u n d s look like? S u p p o s e we were to do a population survey of compass m o u n d s in the A u s t r a l i a n steppe, s c o r i n g a trait s u c h a s c o l o u r , b a s a l l e n g t h / w i d t h r a t i o , o r s o m e i n t e r n a l
The Genetical Evolution of A n i m a l Artefacts
202
structural 'organ'
feature—for
structure.
termite
How
could
mounds we
do
are a
like
bodies
genetic
with
study
a
complex
of such
group-
m a n u f a c t u r e d p h e n o t y p e s ? We need not hope to find normal M e n d e l i a n inheritance with simple dominance. An obvious complication, as already m e n t i o n e d , is that the g e n o t y p e s of the i n d i v i d u a l s w o r k i n g on a n y one m o u n d a r e n o t i d e n t i c a l . F o r m o s t o f t h e life o f a n a v e r a g e c o l o n y , h o w e v e r , a l l t h e w o r k e r s a r e full s i b l i n g s , t h e c h i l d r e n o f t h e p r i m a r y r o y a l p a i r o f alates w h o f o u n d e d the c o l o n y . L i k e their parents the w o r k e r s are diploid. W e m a y p r e s u m e t h a t t h e k i n g ' s t w o sets o f g e n e s a n d t h e q u e e n ' s t w o sets o f genes
are
permuted
throughout
the several
million
worker
bodies.
The
' g e n o t y p e ' o f t h e a g g r e g a t e o f w o r k e r s m a y t h e r e f o r e b e r e g a r d e d , i n a sense, a s a s i n g l e tetraploid g e n o t y p e c o n s i s t i n g o f a l l t h e g e n e s w h i c h t h e o r i g i n a l founding pair contributed.
I t i s n o t q u i t e a s s i m p l e a s t h a t , for v a r i o u s
r e a s o n s , for i n s t a n c e s e c o n d a r y r e p r o d u c t i v e s often arise i n o l d e r c o l o n i e s a n d t h e s e m a y t a k e o n t h e full r e p r o d u c t i v e r o l e i f o n e o f t h e o r i g i n a l r o y a l p a i r dies. T h i s m e a n s that the w o r k e r s b u i l d i n g the later parts of a m o u n d m a y n o t b e full s i b l i n g s o f t h o s e t h a t b e g a n t h e task, b u t t h e i r n e p h e w s a n d n i e c e s (probably inbred and rather uniform, incidentally—Hamilton
1972; Bartz
1 9 7 9 ) . T h e s e l a t e r r e p r o d u c t i v e s still d r a w t h e i r g e n e s f r o m t h e ' t e t r a p l o i d ' set i n t r o d u c e d b y t h e o r i g i n a l r o y a l p a i r , b u t t h e i r p r o g e n y w i l l p e r m u t e a particular subset
of those
original
genes.
One
of the
things
a
'mound-
g e n e t i c i s t ' m i g h t l o o k o u t for, t h e n , i s a s u d d e n c h a n g e i n d e t a i l s o f m o u n d building
after
replacement
of a
primary
reproductive
by
a
secondary
reproductive. Ignoring
the
problem
introduced
by
secondary
reproductives,
let
us
confine our hypothetical genetic study to y o u n g e r colonies whose workers c o n s i s t e n t i r e l y o f full s i b l i n g s . S o m e c h a r a c t e r s i n w h i c h m o u n d s v a r y m a y turn
out
to
be
largely
controlled
at
one
locus,
while
others
will
be
p o l y g e n i c a l l y c o n t r o l l e d a t m a n y l o c i . T h i s i s n o different f r o m o r d i n a r y diploid genetics, but our n e w quasi-tetraploid genetics n o w introduces some c o m p l i c a t i o n s . S u p p o s e the b e h a v i o u r a l m e c h a n i s m i n v o l v e d in choosing the c o l o u r of the m u d used in b u i l d i n g varies g e n e t i c a l l y .
(Again, colour is
c h o s e n for c o n t i n u i t y w i t h e a r l i e r t h o u g h t e x p e r i m e n t s , a l t h o u g h a g a i n i t w o u l d b e m o r e r e a l i s t i c t o a v o i d a v i s u a l trait, s i n c e t e r m i t e s m a k e little use of vision. If necessary, we m a y suppose the choice to be m a d e chemically, m u d c o l o u r b e i n g i n c i d e n t a l l y correlated w i t h the c h e m i c a l cues. T h i s is i n s t r u c t i v e , for i t a g a i n e m p h a s i z e s t h e fact t h a t o u r w a y o f l a b e l l i n g a p h e n o t y p i c trait is a m a t t e r of a r b i t r a r y c o n v e n i e n c e . ) F o r simplicity, assume that m u d c h o i c e is influenced by the diploid g e n o t y p e of the individual w o r k e r d o i n g the c h o o s i n g , in a simple one locus M e n d e l i a n fashion with c h o i c e of d a r k m u d d o m i n a n t o v e r c h o i c e of light m u d . T h e n a m o u n d built by
a
colony
containing
some
dark-preferring
workers
and
some
light
preferring w o r k e r s will consist of a m i x t u r e of d a r k a n d light m u d s and will
T h e G e n e t i c a l E v o l u t i o n of A n i m a l A r t e f a c t s
203
presumably be intermediate in overall colour. Of course such simple genetic assumptions are highly i m p r o b a b l e . T h e y are e q u i v a l e n t to the simplifying assumptions we ordinarily m a k e w h e n explaining elementary conventional genetics, a n d I m a k e t h e m here to e x p l a i n a n a l o g o u s l y the principles of h o w a science of 'extended genetics' might work. U s i n g these a s s u m p t i o n s , t h e n , w e c a n w r i t e d o w n t h e e x p e c t e d e x t e n d e d p h e n o t y p e s , c o n s i d e r i n g m u d c o l o u r o n l y , r e s u l t i n g f r o m crosses b e t w e e n t h e various possible f o u n d i n g pair g e n o t y p e s . F o r instance, all colonies f o u n d e d by a heterozygous king and a heterozygous q u e e n will contain d a r k - b u i l d i n g and
light-building
workers
in
the
ratio
3:1.
The
resulting
extended
p h e n o t y p e will be a m o u n d built of three parts d a r k m u d a n d one part light m u d , therefore nearly, but not c o m p l e t e l y , dark in c o l o u r . If c h o i c e of m u d colour is influenced by polygenes at m a n y loci, the 'tetraploid g e n o t y p e ' of the c o l o n y m a y b e e x p e c t e d t o i n f l u e n c e t h e e x t e n d e d p h e n o t y p e , p e r h a p s i n a n a d d i t i v e w a y . T h e c o l o n y ' s i m m e n s e s i z e w i l l l e a d t o its a c t i n g a s a statistical a v e r a g i n g d e v i c e ,
m a k i n g the m o u n d
as a w h o l e
b e c o m e the
extended p h e n o t y p i c expression of the genes of the r o y a l pair, manifested v i a the b e h a v i o u r o f s e v e r a l m i l l i o n w o r k e r s e a c h c o n t a i n i n g a d i f f e r e n t d i p l o i d s a m p l e o f those g e n e s . M u d c o l o u r w a s a n e a s y c h a r a c t e r for u s t o c h o o s e , b e c a u s e m u d i t s e l f blends in a simple additive m a n n e r : m i x dark a n d light m u d , a n d y o u get k h a k i m u d . I t w a s t h e r e f o r e e a s y for u s t o d e d u c e t h e r e s u l t o f a s s u m i n g t h a t e a c h w o r k e r g o e s its o w n w a y , c h o o s i n g m u d o f its o w n p r e f e r r e d c o l o u r (or c h e m i c a l a s s o c i a t e d w i t h c o l o u r ) , a s d e t e r m i n e d b y its o w n d i p l o i d g e n o t y p e . But w h a t can we say a b o u t a characteristic of overall m o u n d m o r p h o l o g y , say b a s a l w i d t h / l e n g t h r a t i o ? I n itself, this i s n o t a c h a r a c t e r t h a t a n y s i n g l e worker can determine.
E a c h single w o r k e r must be o b e y i n g b e h a v i o u r a l
rules, t h e result o f w h i c h , s u m m e d o v e r t h o u s a n d s o f i n d i v i d u a l s , i s t h e production of a m o u n d of regular shape a n d stated dimensions. O n c e a g a i n , the difficulty i s o n e w e h a v e m e t b e f o r e , i n t h e e m b r y o n i c d e v e l o p m e n t o f a n o r d i n a r y d i p l o i d m u l t i c e l l u l a r b o d y . E m b r y o l o g i s t s a r e still w r e s t l i n g w i t h p r o b l e m s o f this k i n d , a n d v e r y f o r m i d a b l e t h e y a r e . T h e r e d o a p p e a r t o b e some
close
analogies
with
termite
mound
development.
For
instance,
conventional embryologists frequently a p p e a l to the c o n c e p t of the c h e m i c a l g r a d i e n t , w h i l e i n Macrotermes t h e r e i s e v i d e n c e t h a t t h e s h a p e a n d s i z e o f t h e royal cell is d e t e r m i n e d by a p h e r o m o n a l g r a d i e n t a r o u n d the b o d y of the queen
(Bruinsma & Leuthold
1 9 7 7 ) . E a c h cell in a d e v e l o p i n g e m b r y o
behaves as if it ' k n o w s ' w h e r e it is in the b o d y , a n d it g r o w s to h a v e a form and
physiology
appropriate
to
that
part
of the
body
(Wolpert
1970).
S o m e t i m e s t h e effects o f a m u t a t i o n a r e e a s y t o i n t e r p r e t a t t h e c e l l u l a r l e v e l . F o r i n s t a n c e , a m u t a t i o n t h a t affects skin p i g m e n t a t i o n h a s a r a t h e r o b v i o u s l o c a l effect o n e a c h skin c e l l . B u t o t h e r m u t a t i o n s affect c o m p l e x c h a r a c t e r s in
drastic
ways.
Well-known
examples
are
the
'homeotic'
mutants
of
T h e Genetical Evolution of A n i m a l Artefacts
204
Drosophila, s u c h a s t h e o n e t h a t g r o w s a c o m p l e t e a n d w e l l - f o r m e d l e g i n the socket w h e r e an a n t e n n a o u g h t to be. F o r a c h a n g e in one single g e n e to w r e a k s u c h a m a j o r , y e t o r d e r l y , c h a n g e i n t h e p h e n o t y p e , i t m u s t m a k e its lesion rather h i g h in a h i e r a r c h i c a l c h a i n of c o m m a n d . By a n a l o g y , if a single i n f a n t r y m a n g o e s off his h e a d h e a l o n e r u n s a m o k ; b u t i f a g e n e r a l loses his reason an entire a r m y behaves crazily on a grand scale—invades an ally instead of an e n e m y , s a y — w h i l e each individual soldier in that army is o b e y i n g o r d e r s n o r m a l l y a n d s e n s i b l y , a n d his i n d i v i d u a l b e h a v i o u r a s h e p u t s o n e foot i n front o f t h e o t h e r w i l l b e i n d i s t i n g u i s h a b l e f r o m t h a t o f a soldier in an a r m y w i t h a sane general. P r e s u m a b l y an individual
t e r m i t e w o r k i n g o n a little c o r n e r o f a b i g
m o u n d is in a s i m i l a r p o s i t i o n to a c e l l in a d e v e l o p i n g e m b r y o , or a s i n g l e soldier tirelessly o b e y i n g orders w h o s e purpose in the larger s c h e m e of things he does not u n d e r s t a n d . N o w h e r e in the single termite's nervous system is t h e r e a n y t h i n g r e m o t e l y e q u i v a l e n t t o a c o m p l e t e i m a g e o f w h a t t h e finished m o u n d will look like ( W i l s o n 1 9 7 1 , p. 228). E a c h w o r k e r is e q u i p p e d with a small toolkit of b e h a v i o u r a l rules, choose an already
and he/she is probably stimulated to
i t e m o f b e h a v i o u r b y local stimuli e m a n a t i n g from
accomplished,
no
matter
whether
he/she
or
other
the w o r k workers
a c c o m p l i s h e d i t — s t i m u l i e m a n a t i n g f r o m t h e p r e s e n t s t a t e o f t h e nest i n the worker's i m m e d i a t e vicinity ('stigmergie', Grasse 1959). For my purposes it d o e s n ' t m a t t e r e x a c t l y w h a t t h e b e h a v i o u r a l rules a r e , b u t t h e y w o u l d b e something like: ' I f you c o m e upon a heap of mud with a certain pheromone o n it, p u t a n o t h e r d o l l o p o f m u d o n t h e t o p . ' T h e i m p o r t a n t p o i n t a b o u t s u c h r u l e s i s t h a t t h e y h a v e a p u r e l y l o c a l effect. T h e g r a n d d e s i g n o f t h e w h o l e m o u n d e m e r g e s o n l y a s the s u m m e d c o n s e q u e n c e s o f thousands o f o b e y i n g s of micro-rules
( H a n s e l l in press). P a r t i c u l a r interest attaches to the local
r u l e s t h a t a r e r e s p o n s i b l e for d e t e r m i n i n g g l o b a l p r o p e r t i e s s u c h a s t h e b a s e l e n g t h o f the c o m p a s s m o u n d . H o w d o the i n d i v i d u a l w o r k e r s o n the g r o u n d ' k n o w ' that they h a v e r e a c h e d the b o u n d a r y o f the g r o u n d p l a n ? Perhaps i n s o m e t h i n g like the s a m e w a y as the cells at the b o u n d a r y of a liver ' k n o w ' that they are not in the m i d d l e of the liver. In a n y case, w h a t e v e r the local b e h a v i o u r a l r u l e s m a y b e t h a t d e t e r m i n e t h e o v e r a l l s h a p e a n d size o f a termite m o u n d ,
they are presumably subject to genetic variation in
the
population at large. It is entirely plausible, indeed almost inevitable, that b o t h the s h a p e a n d size o f c o m p a s s termite m o u n d s h a v e e v o l v e d b y natural selection, just like a n y feature of bodily m o r p h o l o g y . T h i s can only have c o m e a b o u t t h r o u g h t h e s e l e c t i o n o f m u t a t i o n s a c t i n g a t t h e l o c a l l e v e l o n the building b e h a v i o u r of individual worker termites. N o w o u r s p e c i a l p r o b l e m arises, w h i c h w o u l d n o t arise i n t h e o r d i n a r y e m b r y o g e n e s i s of a m u l t i c e l l u l a r b o d y , nor in the e x a m p l e of m i x i n g light a n d d a r k m u d s . U n l i k e the cells of a m u l t i c e l l u l a r b o d y , the w o r k e r s are not
T h e Genetical Evolution of A n i m a l Artefacts
205
g e n e t i c a l l y identical. In the e x a m p l e of the d a r k a n d light m u d , it w a s easy to
suppose
that
a
genetically
heterogeneous
work-force
would
simply
construct a m o u n d of m i x e d m u d . But a work-force w h i c h w a s genetically heterogeneous w i t h respect to o n e of the b e h a v i o u r a l rules that affected overall m o u n d s h a p e m i g h t p r o d u c e curious results. B y a n a l o g y w i t h o u r simple M e n d e l i a n m o d e l of m u d selection, a c o l o n y m i g h t contain workers f a v o u r i n g t w o d i f f e r e n t r u l e s for d e t e r m i n i n g t h e b o u n d a r y o f t h e m o u n d , s a y in the ratio three to one. It is p l e a s i n g to i m a g i n e that such a b i m o d a l c o l o n y might produce a m o u n d with a strange double wall and a m o a t b e t w e e n ! M o r e p r o b a b l y , t h e r u l e s o b e y e d b y i n d i v i d u a l s w o u l d i n c l u d e p r o v i s i o n for the m i n o r i t y t o a l l o w t h e m s e l v e s t o b e o v e r r u l e d b y m a j o r i t y d e c i s i o n s , s o that only one clean-cut w a l l w o u l d e m e r g e . T h i s c o u l d w o r k in a similar w a y t o t h e ' d e m o c r a t i c ' c h o i c e o f a n e w nest site i n h o n e y b e e s w a r m s , o b s e r v e d by Lindauer (1961). S c o u t b e e s l e a v e t h e s w a r m h a n g i n g i n a t r e e , a n d p r o s p e c t for s u i t a b l e n e w p e r m a n e n t sites s u c h a s h o l l o w trees. E a c h s c o u t r e t u r n s a n d d a n c e s o n the s u r f a c e o f t h e s w a r m , u s i n g t h e w e l l - k n o w n v o n F r i s c h c o d e t o i n d i c a t e the
direction
investigated.
and The
distance 'vigour'
of
the
prospective
of the d a n c e
indicates
site the
that
she
has
individual
just
scout's
assessment o f t h e v i r t u e s o f t h e site. N e w b e e s a r e r e c r u i t e d t o g o o u t a n d e x a m i n e i t for t h e m s e l v e s , a n d i f t h e y ' a p p r o v e ' t h e y t o o d a n c e ' i n its f a v o u r ' on returning. After some hours, then, the scouts h a v e formed themselves into a few ' p a r t i e s ' , e a c h o n e ' a d v o c a t i n g ' a d i f f e r e n t n e s t site. F i n a l l y , m i n o r i t y 'opinions' b e c o m e even smaller minorities, as allegiances are transferred to m a j o r i t y d a n c e s . W h e n a n o v e r w h e l m i n g m a j o r i t y h a s b e e n a c h i e v e d for o n e site, t h e w h o l e s w a r m t a k e s o f f a n d flies t h e r e t o set u p h o m e . L i n d a u e r o b s e r v e d this p r o c e d u r e for n i n e t e e n d i f f e r e n t s w a r m s , a n d i n o n l y t w o o f t h e s e c a s e s w a s a c o n s e n s u s n o t s o o n r e a c h e d . I q u o t e his a c c o u n t of one of these: I n the first c a s e t w o g r o u p s o f m e s s e n g e r s h a d g o t i n t o c o m p e t i t i o n ; one g r o u p a n n o u n c e d a nesting place to the northwest, the other to the northeast. N e i t h e r o f the t w o w i s h e d t o y i e l d . T h e s w a r m then f i n a l l y f l e w off a n d I c o u l d s c a r c e l y b e l i e v e m y e y e s — i t s o u g h t t o d i v i d e itself. T h e o n e h a l f w a n t e d t o f l y t o t h e n o r t h w e s t , t h e o t h e r t o the northeast.
A p p a r e n t l y each g r o u p of scouting bees w a n t e d
to
a b d u c t t h e s w a r m t o t h e n e s t i n g p l a c e o f its o w n c h o i c e . B u t t h a t w a s n a t u r a l l y n o t p o s s i b l e , for o n e g r o u p w a s a l w a y s w i t h o u t t h e q u e e n , a n d t h e r e r e s u l t e d a r e m a r k a b l e t u g o f w a r i n t h e a i r , o n c e 100 m e t e r s to the northwest, then a g a i n 150 meters to the northeast, until finally after h a l f a n h o u r t h e s w a r m g a t h e r e d t o g e t h e r a t t h e o l d l o c a t i o n . I m m e d i a t e l y both groups b e g a n again with their soliciting dances,
206
The Genetical Evolution of Animal Artefacts
a n d i t w a s n o t u n t i l t h e n e x t d a y t h a t t h e n o r t h e a s t g r o u p finally y i e l d e d ; they e n d e d their d a n c e and thus an a g r e e m e n t w a s reached on the nesting p l a c e in the northwest [ L i n d a u e r 1 9 6 1 , p. 4 3 ] . T h e r e is no suggestion here that the t w o s u b g r o u p s of bees w e r e genetically d i f f e r e n t , t h o u g h t h e y m a y h a v e b e e n . W h a t m a t t e r s for the p o i n t I a m m a k i n g is that e a c h i n d i v i d u a l follows local b e h a v i o u r a l rules, the c o m b i n e d effect o f w h i c h n o r m a l l y g i v e s rise t o c o o r d i n a t e d s w a r m b e h a v i o u r . T h e s e e v i d e n t l y i n c l u d e r u l e s for r e s o l v i n g ' d i s p u t e s ' i n f a v o u r o f the m a j o r i t y . D i s a g r e e m e n t s o v e r t h e p r e f e r r e d l o c a t i o n for t h e o u t e r w a l l o f a t e r m i t e m o u n d m i g h t b e j u s t a s s e r i o u s for c o l o n y s u r v i v a l a s d i s a g r e e m e n t o v e r n e s t i n g sites a m o n g L i n d a u e r ' s b e e s ( c o l o n y s u r v i v a l m a t t e r s , b e c a u s e o f its effects o n t h e s u r v i v a l o f t h e g e n e s c a u s i n g i n d i v i d u a l s t o r e s o l v e d i s p u t e s ) . A s a w o r k i n g h y p o t h e s i s we m i g h t e x p e c t that disputes resulting from genetic h e t e r o g e n e i t y i n t e r m i t e s w o u l d b e r e s o l v e d b y s i m i l a r r u l e s . I n this w a y the e x t e n d e d p h e n o t y p e c o u l d take up a discrete a n d regular shape, despite being built by genetically heterogeneous workers. The
analysis
of artefacts g i v e n
in
this
chapter seems,
at first sight,
v u l n e r a b l e to reductio ad absurdum. I s n ' t t h e r e a sense, it m a y be a s k e d , in w h i c h e v e r y effect
that an a n i m a l has upon
the w o r l d is an extended
p h e n o t y p e ? W h a t a b o u t t h e f o o t p r i n t s left i n t h e m u d b y a n o y s t e r c a t c h e r , the paths w o r n t h r o u g h the grass by sheep, the l u x u r i a n t tussock that marks t h e site of a last y e a r ' s c o w p a t ? A p i g e o n ' s nest is an a r t e f a c t w i t h o u t a d o u b t , b u t in g a t h e r i n g the sticks the bird also c h a n g e s the a p p e a r a n c e of the g r o u n d w h e r e t h e y h a d l a i n . I f t h e nest i s c a l l e d e x t e n d e d p h e n o t y p e , w h y s h o u l d n ' t w e s o c a l l t h e b a r e p a t c h o f g r o u n d w h e r e t h e sticks u s e d t o l i e ? To
answer
this
we
must
recall
the fundamental
reason
why
we are
i n t e r e s t e d i n t h e p h e n o t y p i c e x p r e s s i o n o f g e n e s i n the f i r s t p l a c e . O f a l l the m a n y p o s s i b l e r e a s o n s , t h e o n e w h i c h c o n c e r n s u s i n this b o o k i s a s f o l l o w s . We
are
fundamentally
interested
in
natural
selection,
therefore
in
the
differential s u r v i v a l of r e p l i c a t i n g entities such as genes. G e n e s are favoured or disfavoured relative to their alleles as a c o n s e q u e n c e of their p h e n o t y p i c effects u p o n t h e w o r l d . S o m e o f t h e s e p h e n o t y p i c effects m a y b e i n c i d e n t a l c o n s e q u e n c e s o f others, a n d h a v e n o b e a r i n g o n the survival c h a n c e s , one w a y or the other, of the genes c o n c e r n e d . A genetic m u t a t i o n that changes t h e s h a p e o f a n o y s t e r c a t c h e r ' s foot w i l l d o u b t l e s s t h e r e b y i n f l u e n c e t h e o y s t e r c a t c h e r ' s s u c c e s s i n p r o p a g a t i n g it. I t m a y , for i n s t a n c e , s l i g h t l y r e d u c e t h e b i r d ' s risk o f s i n k i n g i n t o m u d , w h i l e a t t h e s a m e t i m e i t s l i g h t l y s l o w s h i m d o w n w h e n h e i s r u n n i n g o n firm g r o u n d . S u c h effects a r e l i k e l y t o b e o f d i r e c t r e l e v a n c e to n a t u r a l selection. B u t the m u t a t i o n will also h a v e an effect o n t h e s h a p e o f t h e f o o t p r i n t s left b e h i n d i n the m u d — a r g u a b l y a n e x t e n d e d p h e n o t y p i c effect. If, a s i s p e r f e c t l y l i k e l y , this h a s n o i n f l u e n c e o n the success of the g e n e c o n c e r n e d (Williams 1966, p p . 1 2 - 1 3 ) , it is of no
The Genetical Evolution of A n i m a l Artefacts
207
interest t o t h e s t u d e n t o f n a t u r a l s e l e c t i o n , a n d t h e r e i s n o p o i n t i n b o t h e r i n g t o discuss i t u n d e r t h e h e a d i n g o f t h e e x t e n d e d p h e n o t y p e , t h o u g h i t w o u l d b e f o r m a l l y c o r r e c t t o d o s o . If, o n t h e o t h e r h a n d , t h e c h a n g e d f o o t p r i n t d i d i n f l u e n c e s u r v i v a l o f t h e o y s t e r c a t c h e r , s a y b y m a k i n g i t h a r d e r for p r e d a t o r s to
track the
bird,
I
would
w a n t to regard
it
as
part
of the
extended
p h e n o t y p e o f t h e g e n e . P h e n o t y p i c effects o f g e n e s , w h e t h e r a t t h e l e v e l o f intracellular b i o c h e m i s t r y , gross b o d i l y m o r p h o l o g y or e x t e n d e d p h e n o t y p e , are
potentially
generation,
devices
or barriers
by
which
genes
lever
t o t h e i r d o i n g so.
themselves
into
the
next
I n c i d e n t a l side-effects are not
a l w a y s effective as tools or barriers, a n d we do not b o t h e r to r e g a r d t h e m as
phenotypic
expressions
of genes,
either
at
the
conventional
or
the
extended phenotype level. I t i s u n f o r t u n a t e t h a t this c h a p t e r h a s h a d t o b e r a t h e r h y p o t h e t i c a l . T h e r e h a v e been o n l y a few studies of the genetics of b u i l d i n g b e h a v i o u r in a n y animal
(e.g. D i l g e r
genetics'
will
be
1962), but there is no reason to think that 'artefact
any
different,
in
principle,
from
behaviour
genetics
g e n e r a l l y ( H a n s e l l i n p r e s s ) . T h e i d e a o f t h e e x t e n d e d p h e n o t y p e i s still sufficiently u n f a m i l i a r t h a t i t m i g h t n o t i m m e d i a t e l y o c c u r t o a g e n e t i c i s t t o study termite m o u n d s as a p h e n o t y p e , even if it w e r e p r a c t i c a l l y easy to do so—and
it
wouldn't
be
easy.
Yet
we
must
acknowledge
at
least
the
theoretical validity of such a b r a n c h of genetics if we are to c o u n t e n a n c e the Darwinian evolution of beaver dams and termite mounds. A n d w h o can d o u b t t h a t , i f t e r m i t e m o u n d s fossilized p l e n t i f u l l y , w e w o u l d see g r a d e d e v o l u t i o n a r y series w i t h t r e n d s a s s m o o t h (or a s p u n c t u a t e d ! ) a s a n y t h a t w e find in vertebrate skeletal palaeontology (Schmidt 1 9 5 5 ; Hansell in press)? Permit me one further speculation to lead us into the next c h a p t e r . I h a v e spoken as if the genes inside a termite m o u n d w e r e all enclosed in the nuclei o f cells o f t e r m i t e b o d i e s . T h e ' e m b r y o l o g i c a l ' f o r c e s b e a r i n g o n t h e e x t e n d e d phenotype have been assumed termites.
Yet
the
chapter on
to originate from the genes of individual arms races and manipulation should h a v e
a l e r t e d u s t o a n o t h e r w a y o f l o o k i n g a t it. I f a l l t h e D N A c o u l d b e d i s t i l l e d out of a termite m o u n d , perhaps as m u c h as one-quarter of it w o u l d not h a v e originated from termite nuclei at all. S o m e such p r o p o r t i o n of the b o d y weight of each individual termite is typically m a d e up of symbiotic cellulosedigesting m i c r o o r g a n i s m s in the g u t — f l a g e l l a t e s or b a c t e r i a . T h e s y m b i o n t s are o b l i g a t e l y d e p e n d e n t o n the termites, a n d the termites o n t h e m . T h e proximal p h e n o t y p i c p o w e r of the s y m b i o n t genes is exerted v i a protein synthesis i n s y m b i o n t c y t o p l a s m . B u t j u s t a s t e r m i t e g e n e s r e a c h o u t b e y o n d the cells t h a t e n c l o s e t h e m a n d m a n i p u l a t e t h e d e v e l o p m e n t o f w h o l e t e r m i t e bodies a n d h e n c e of the m o u n d , is it not almost i n e v i t a b l e that the s y m b i o n t genes
will
have
surroundings? termite cells
And and
been will hence
selected this
to
exert
phenotypic
power
not include exerting p h e n o t y p i c
bodies,
on
termite
behaviour
and
on
their
power on
even
termite
208
T h e Genetical Evolution of Animal Artefacts
m o u n d s ? A l o n g t h e s e l i n e s , c o u l d t h e e v o l u t i o n o f e u s o c i a l i t y i n the I s o p t e r a be e x p l a i n e d as an a d a p t a t i o n of the m i c r o s c o p i c s y m b i o n t s rather than of the termites themselves? T h i s c h a p t e r h a s e x p l o r e d t h e i d e a o f t h e e x t e n d e d p h e n o t y p e , first o f g e n e s in a single i n d i v i d u a l , then of genes from different but closely related i n d i v i d u a l s , m e m b e r s of a k i n - g r o u p . T h e logic of the a r g u m e n t n o w seems to c o m p e l us to c o n t e m p l a t e the possibility of an extended phenotype's being j o i n t l y m a n i p u l a t e d , not necessarily c o o p e r a t i v e l y , b y genes from distantly related i n d i v i d u a l s , i n d i v i d u a l s of different species, e v e n different k i n g d o m s . T h i s i s t h e d i r e c t i o n i n w h i c h o u r n e x t o u t w a r d s t e p m u s t t a k e us.
1 2 Host Phenotypes of Parasite Genes
L e t us briefly take stock of w h e r e we h a v e r e a c h e d in o u r o u t w a r d march. T h e phenotypic expression of a gene can extend outside the cell in w h i c h t h e g e n e s e x e r t t h e i r i m m e d i a t e b i o c h e m i c a l i n f l u e n c e , t o affect g r o s s features o f a w h o l e m u l t i c e l l u l a r b o d y . T h i s i s c o m m o n p l a c e , a n d w e a r e c o n v e n t i o n a l l y used to the i d e a of a g e n e ' s p h e n o t y p i c expression b e i n g e x t e n d e d this far. In the previous c h a p t e r we took the small further step of e x t e n d i n g the phenotype to artefacts, built by individual b e h a v i o u r w h i c h is subject to g e n e t i c v a r i a t i o n , for i n s t a n c e c a d d i s h o u s e s . N e x t w e s a w t h a t a n e x t e n d e d phenotype can be built under the joint influence of genes in m o r e than one individual body. B e a v e r d a m s and termite m o u n d s are collectively built by the b e h a v i o u r a l efforts o f m o r e t h a n o n e i n d i v i d u a l . A g e n e t i c m u t a t i o n i n one i n d i v i d u a l b e a v e r c o u l d s h o w itself in p h e n o t y p i c c h a n g e in the shared artefact. If the p h e n o t y p i c c h a n g e in the artefact h a d an influence on the success o f r e p l i c a t i o n o f t h e n e w g e n e , n a t u r a l s e l e c t i o n w o u l d a c t , p o s i t i v e l y or negatively, to c h a n g e the probability of similar artefacts existing in the future. T h e g e n e ' s e x t e n d e d p h e n o t y p i c effect, s a y a n i n c r e a s e i n t h e h e i g h t o f the d a m , affects its c h a n c e s o f s u r v i v a l i n p r e c i s e l y t h e s a m e s e n s e a s i n t h e c a s e o f a g e n e w i t h a n o r m a l p h e n o t y p i c effect, s u c h a s a n i n c r e a s e i n t h e l e n g t h o f the t a i l . T h e f a c t t h a t t h e d a m i s t h e s h a r e d p r o d u c t o f t h e b u i l d i n g behaviour of several beavers does not alter the principle: genes that tend to m a k e beavers build h i g h d a m s will themselves, on a v e r a g e , tend to r e a p the benefits (or costs) o f h i g h d a m s , e v e n t h o u g h e v e r y d a m m a y b e j o i n t l y b u i l t b y several beavers. I f t w o b e a v e r s w o r k i n g o n the s a m e d a m h a v e different g e n e s for d a m h e i g h t , interaction interactions.
between
the resulting e x t e n d e d p h e n o t y p e will reflect the
the genes,
There could
in the s a m e w a y as
be extended genetic
bodies reflect g e n e
a n a l o g u e s o f epistasis,
of
modifier genes, even of d o m i n a n c e a n d recessiveness. Finally, at the end of the c h a p t e r , we s a w that genes ' s h a r i n g ' a g i v e n e x t e n d e d p h e n o t y p i c trait m i g h t c o m e from different species, e v e n different 209
Host Phenotypes of Parasite Genes
2IO
p h y l a a n d different k i n g d o m s . T h i s c h a p t e r will d e v e l o p t w o further ideas. O n e is that p h e n o t y p e s that extend outside the body do not h a v e to be i n a n i m a t e a r t e f a c t s : t h e y c a n t h e m s e l v e s b e b u i l t o f l i v i n g tissue. T h e o t h e r idea is that w h e r e v e r there are 'shared' genetic influences on an extended p h e n o t y p e , the shared influences m a y be in conflict with e a c h other rather t h a n c o o p e r a t i v e . T h e r e l a t i o n s h i p s w e s h a l l b e c o n c e r n e d w i t h a r e those o f parasites a n d their hosts. I shall s h o w that it is l o g i c a l l y sensible to regard parasite g e n e s as h a v i n g p h e n o t y p i c expression in host bodies a n d b e h a v i o u r . T h e c a d d i s l a r v a rides inside the stone house that it built. It therefore s e e m s a p p r o p r i a t e t o r e g a r d t h e h o u s e a s t h e o u t e r w a l l o f the g e n e v e h i c l e , t h e c a s i n g o f t h e s u r v i v a l m a c h i n e . I t i s e v e n e a s i e r t o r e g a r d the shell o f a s n a i l a s p a r t o f t h e p h e n o t y p i c e x p r e s s i o n o f s n a i l g e n e s s i n c e , a l t h o u g h the s h e l l i s i n o r g a n i c a n d ' d e a d ' , its c h e m i c a l s u b s t a n c e w a s d i r e c t l y s e c r e t e d b y s n a i l c e l l s . V a r i a t i o n s i n , s a y , shell t h i c k n e s s w o u l d b e c a l l e d g e n e t i c i f g e n e s in snail
cells
affected
'environmental'.
shell
thickness.
Otherwise
they
B u t there are reports o f snails w i t h
would
be
called
t r e m a t o d e parasites
h a v i n g t h i c k e r shells t h a n u n p a r a s i t i z e d snails ( C h e n g 1 9 7 3 ) . F r o m t h e p o i n t o f v i e w o f s n a i l g e n e t i c s , this a s p e c t o f shell v a r i a t i o n i s u n d e r ' e n v i r o n m e n t a l ' c o n t r o l — t h e f l u k e i s p a r t o f t h e e n v i r o n m e n t o f t h e s n a i l — b u t from the p o i n t of v i e w of fluke genetics it m i g h t w e l l be u n d e r genetic control: it m i g h t , i n d e e d , be an e v o l v e d a d a p t a t i o n of the fluke. It is a d m i t t e d l y also p o s s i b l e t h a t t h e t h i c k e n e d s h e l l is a p a t h o l o g i c a l r e s p o n s e of t h e s n a i l , a d u l l b y p r o d u c t o f i n f e c t i o n . B u t let m e e x p l o r e t h e p o s s i b i l i t y t h a t i t i s a fluke a d a p t a t i o n , b e c a u s e i t i s a n i n t e r e s t i n g i d e a t o use i n f u r t h e r d i s c u s s i o n . I f w e c o n s i d e r s n a i l s h e l l v a r i a t i o n as, i n p a r t , p h e n o t y p i c e x p r e s s i o n o f s n a i l g e n e s , w e m i g h t r e c o g n i z e a n o p t i m u m s h e l l t h i c k n e s s i n the f o l l o w i n g s e n s e . S e l e c t i o n p r e s u m a b l y p e n a l i z e s s n a i l g e n e s t h a t m a k e shells t o o t h i c k , a s w e l l a s t h o s e t h a t m a k e shells t o o t h i n . T h i n shells p r o v i d e i n a d e q u a t e protection.
Genes
for
too-thin
shells
therefore
endanger
their
germ-line
copies, w h i c h are thus not favoured by natural selection. Shells that are too t h i c k p r e s u m a b l y p r o t e c t t h e i r s n a i l s ( a n d t h e e n c l o s e d g e r m - l i n e g e n e s for extra thickness)
s u p e r l a t i v e l y , b u t t h e e x t r a c o s t o f m a k i n g a t h i c k shell
d e t r a c t s f r o m t h e s n a i l ' s s u c c e s s i n s o m e o t h e r w a y . I n t h e e c o n o m y o f the body,
r e s o u r c e s t h a t a r e c o n s u m e d i n m a k i n g e x t r a - t h i c k shells,
c a r r y i n g the e x t r a w e i g h t a r o u n d , making, say,
larger gonads.
and in
m i g h t better h a v e b e e n diverted into
C o n t i n u i n g with the hypothetical example,
t h e r e f o r e , g e n e s for e x t r a - t h i c k shells w i l l t e n d t o i n d u c e i n t h e i r b o d i e s s o m e compensating disadvantage such as relatively small gonads, and they will therefore not be passed on to the next generation so effectively. E v e n if there is, i n f a c t , n o t r a d e - o f f b e t w e e n s h e l l t h i c k n e s s a n d g o n a d s i z e , t h e r e i s b o u n d t o b e s o m e k i n d o f a n a l o g o u s trade-off, a n d a c o m p r o m i s e w i l l b e r e a c h e d a t a n i n t e r m e d i a t e t h i c k n e s s . G e n e s t h a t t e n d t o m a k e s n a i l shells e i t h e r t o o thick or too thin w i l l not prosper in the snail g e n e p o o l .
Host Phenotypes of Parasite Genes
2 1 1
B u t this w h o l e a r g u m e n t p r e s u p p o s e s t h a t t h e o n l y g e n e s t h a t h a v e p o w e r over variation in shell thickness are snail genes. W h a t if s o m e of the c a u s a l factors t h a t a r e , b y d e f i n i t i o n , e n v i r o n m e n t a l f r o m t h e s n a i l ' s p o i n t o f v i e w , turn o u t to be g e n e t i c from s o m e o t h e r p o i n t of v i e w , say t h a t of the fluke? Suppose we a d o p t the suggestion m a d e a b o v e that some fluke genes are c a p a b l e , t h r o u g h a n i n f l u e n c e o n s n a i l p h y s i o l o g y , o f e x e r t i n g a n effect o n snail shell t h i c k n e s s . I f shell t h i c k n e s s i n f l u e n c e s t h e r e p l i c a t i o n s u c c e s s o f such fluke genes, n a t u r a l selection is b o u n d to w o r k on their frequencies relative to their alleles in the fluke g e n e - p o o l . C h a n g e s in snail shell thickness m a y b e r e g a r d e d , t h e n , a t l e a s t i n p a r t , a s p o t e n t i a l a d a p t a t i o n s for t h e benefit o f f l u k e g e n e s . N o w , the o p t i m u m shell thickness from the point of v i e w of the fluke genes is h a r d l y likely to be the s a m e as the o p t i m u m from the p o i n t of v i e w of snail g e n e s . F o r i n s t a n c e , s n a i l g e n e s w i l l b e s e l e c t e d for t h e i r b e n e f i c i a l effects o n snail
reproduction
as
well
as snail survival,
but
(except
under special
c i r c u m s t a n c e s w h i c h w e s h a l l c o m e o n to) f l u k e g e n e s m a y v a l u e s n a i l survival b u t they will not v a l u e snail r e p r o d u c t i o n at all. In the i n e v i t a b l e trade-off b e t w e e n
the d e m a n d s
of snail
survival
and
snail
reproduction,
therefore, snail genes w i l l be selected to p r o d u c e an o p t i m a l c o m p r o m i s e , while fluke genes will
be selected
to d e v a l u e snail r e p r o d u c t i o n to the
a d v a n t a g e of snail s u r v i v a l , a n d h e n c e to t h i c k e n the shell. A t h i c k e n i n g of the shell
in
parasitized
snails
is,
it will
be
remembered,
the
observed
phenomenon with which we began. It m a y be objected here that, a l t h o u g h a fluke has no direct stake in the r e p r o d u c t i o n o f its o w n s n a i l h o s t , i t d o e s h a v e a s t a k e i n t h e r e b e i n g a n e w g e n e r a t i o n o f snails a t l a r g e . T h i s i s t r u e , b u t w e m u s t b e v e r y c a r e f u l b e f o r e w e use t h e f a c t t o p r e d i c t t h a t s e l e c t i o n w o u l d f a v o u r f l u k e a d a p t a t i o n s t o e n h a n c e s n a i l r e p r o d u c t i o n . T h e q u e s t i o n w e h a v e t o ask i s t h i s . G i v e n t h a t the f l u k e g e n e - p o o l w a s d o m i n a t e d b y g e n e s t h a t a i d e d s n a i l r e p r o d u c t i o n a t the e x p e n s e o f s n a i l s u r v i v a l , w o u l d s e l e c t i o n f a v o u r a selfish f l u k e g e n e t h a t s a c r i f i c e d t h e r e p r o d u c t i o n o f its p a r t i c u l a r s n a i l h o s t ,
even
parasitically
c a s t r a t e d t h e s n a i l , i n t h e i n t e r e s t o f p r o l o n g i n g t h e life o f t h a t h o s t , a n d h e n c e o f p r o m o t i n g its o w n s u r v i v a l a n d r e p r o d u c t i o n ? E x c e p t u n d e r s p e c i a l circumstances the a n s w e r is surely y e s ; such a rare g e n e w o u l d i n v a d e the fluke gene-pool,
since
it
could
exploit
the
free
supply
of n e w
snails
encouraged by the public-spirited majority of the fluke p o p u l a t i o n . In other words, f a v o u r i n g snail r e p r o d u c t i o n at the e x p e n s e of snail s u r v i v a l w o u l d n o t b e a f l u k e E S S . F l u k e g e n e s t h a t m a n a g e t o shift t h e s n a i l ' s i n v e s t m e n t o f resources a w a y from r e p r o d u c t i o n a n d into s u r v i v a l w i l l tend to be f a v o u r e d in the fluke g e n e - p o o l .
It is entirely plausible, therefore, that the extra
t h i c k n e s s of shells o b s e r v e d in p a r a s i t i z e d s n a i l s is a fluke a d a p t a t i o n . O n this h y p o t h e s i s , t h e s h e l l p h e n o t y p e i s a s h a r e d p h e n o t y p e , i n f l u e n c e d by fluke genes as w e l l as by snail genes, j u s t as the b e a v e r d a m is a p h e n o t y p e
2 1 2
shared
Host Phenotypes o f Parasite Genes
by genes in more than one individual beaver.
A c c o r d i n g t o the
hypothesis, there are t w o o p t i m u m thicknesses of snail shells: a relatively thick fluke o p t i m u m , a n d a s o m e w h a t thinner snail o p t i m u m . T h e observed t h i c k n e s s i n p a r a s i t i z e d snails w i l l p r o b a b l y b e s o m e w h e r e b e t w e e n the t w o o p t i m a , since snail genes a n d fluke genes are both in a position to exert p o w e r , a n d they are e x e r t i n g their p o w e r in opposite directions. A s for p a r a s i t e - f r e e s n a i l s , i t m i g h t b e e x p e c t e d t h a t t h e i r shells w o u l d h a v e the s n a i l - o p t i m a l thickness, since there are no fluke genes to exert p o w e r . T h i s is too simple, h o w e v e r . If the population at large has a high incidence of fluke infestation,
the g e n e - p o o l will p r o b a b l y contain genes that tend to
c o m p e n s a t e for t h e t h i c k e n i n g effect o f f l u k e g e n e s . T h i s w o u l d l e a d t o uninfected thinner
snails
even
thicknesses
in
having
than
the
fluke-free
over-compensating snail
optimum.
areas should
be
phenotypes,
I
therefore
shells
predict
intermediate
that that
between
are shell
those o f
i n f e c t e d s n a i l s a n d u n i n f e c t e d snails i n f l u k e - i n f e s t e d a r e a s . I d o n o t k n o w o f a n y e v i d e n c e b e a r i n g o n this p r e d i c t i o n , b u t i t w o u l d b e i n t e r e s t i n g t o l o o k . N o t e t h a t this p r e d i c t i o n d o e s n o t d e p e n d o n a n y a d hoc a s s u m p t i o n a b o u t snails ' w i n n i n g ' o r f l u k e s ' w i n n i n g ' . I t a s s u m e s t h a t b o t h s n a i l g e n e s a n d f l u k e g e n e s e x e r t some p o w e r o v e r t h e s n a i l p h e n o t y p e . T h e p r e d i c t i o n w i l l follow regardless of the q u a n t i t a t i v e details of that p o w e r . F l u k e s l i v e i n s i d e s n a i l shells in a sense t h a t is n o t t o o far r e m o v e d from the sense i n w h i c h s n a i l s l i v e i n s i d e s n a i l shells, a n d c a d d i s l a r v a e l i v e i n s i d e t h e i r stone houses. H a v i n g a c c e p t e d the idea that the form a n d c o l o u r of a caddis house
might
constitute
phenotypic
expression
of caddis genes,
it is not
d i f f i c u l t t o a c c e p t t h e i d e a o f t h e f o r m a n d c o l o u r o f a s n a i l shell b e i n g phenotypic
expression of genes in a fluke inside the snail.
If we could
fancifully i m a g i n e a fluke g e n e a n d a snail g e n e intelligently discussing with a c a d d i s g e n e t h e p r o b l e m s o f m a k i n g a h a r d o u t e r w a l l for p r o t e c t i o n , I d o u b t i f t h e c o n v e r s a t i o n w o u l d m a k e a n y r e f e r e n c e t o t h e fact t h a t the f l u k e w a s a parasite w h i l e the c a d d i s a n d the snail w e r e not. T h e rival merits of s e c r e t i n g c a l c i u m c a r b o n a t e , r e c o m m e n d e d b y the f l u k e a n d t h e s n a i l g e n e s , versus p i c k i n g up stones, preferred by the caddis g e n e , w o u l d be discussed. T h e r e m i g h t be s o m e reference to the fact that a c o n v e n i e n t a n d e c o n o m i c a l w a y o f s e c r e t i n g c a l c i u m c a r b o n a t e i n v o l v e s t h e use o f a s n a i l . B u t , from the gene's-eye viewpoint,
I
suspect that the c o n c e p t of parasitism w o u l d be
treated as irrelevant. A l l three genes m i g h t regard themselves as parasitic, or alternatively
as
using
comparable
levers
of power
to
influence
their
respective w o r l d s so as to s u r v i v e . T h e l i v i n g cells of the snail w o u l d be regarded
by the snail gene and
t h e f l u k e g e n e a s useful o b j e c t s t o b e
m a n i p u l a t e d i n t h e o u t s i d e w o r l d , i n e x a c t l y t h e s a m e sense a s t h e stones o n the b o t t o m o f the stream w o u l d b e r e g a r d e d b y the c a d d i s g e n e . B y d i s c u s s i n g i n o r g a n i c s n a i l shells, I h a v e r e t a i n e d c o n t i n u i t y w i t h the caddis houses a n d o t h e r n o n - l i v i n g artefacts of the previous c h a p t e r , thereby
Host Phenotypes of Parasite Genes
213
pursuing my policy of sustaining credulity by e x t e n d i n g the c o n c e p t of the p h e n o t y p e g r a d u a l l y by insensible degrees. B u t n o w it is time to grasp the l i v i n g s n a i l f i r m l y b y t h e h o r n s . F l u k e s o f t h e g e n u s Leucochloridium i n v a d e t h e h o r n s o f snails w h e r e t h e y c a n b e s e e n t h r o u g h t h e s k i n ,
conspicuously
p u l s a t i n g . T h i s t e n d s t o m a k e b i r d s , w h o a r e t h e n e x t h o s t i n t h e life c y c l e o f the f l u k e , b i t e off t h e t e n t a c l e s m i s t a k i n g t h e m , W i c k l e r ( 1 9 6 8 ) s u g g e s t s , for insects. W h a t i s i n t e r e s t i n g h e r e i s t h a t t h e f l u k e s s e e m a l s o t o m a n i p u l a t e t h e behaviour o f t h e s n a i l s . W h e t h e r i t i s b e c a u s e t h e s n a i l ' s e y e s a r e a t t h e e n d s o f the h o r n s , o r w h e t h e r t h r o u g h s o m e m o r e i n d i r e c t p h y s i o l o g i c a l r o u t e , t h e fluke m a n a g e s to c h a n g e the snail's b e h a v i o u r w i t h respect to light. T h e n o r m a l n e g a t i v e p h o t o t a x i s i s r e p l a c e d i n i n f e c t e d snails b y p o s i t i v e l i g h t s e e k i n g . T h i s c a r r i e s t h e m u p t o o p e n sites w h e r e t h e y a r e p r e s u m a b l y m o r e l i k e l y t o b e e a t e n b y b i r d s , a n d this b e n e f i t s t h e f l u k e . O n c e a g a i n , i f this i s t o b e r e g a r d e d a s a p a r a s i t i c a d a p t a t i o n , a n d i n d e e d it is widely so regarded (Wickler 1968; H o l m e s & Bethel 1 9 7 2 ) , we are forced to postulate the s o m e t i m e existence of genes in the parasite g e n e - p o o l that influenced
the
b e h a v i o u r o f hosts,
since all D a r w i n i a n adaptations
e v o l v e d by the selection of genes. By definition such genes w e r e genes 'for' snail b e h a v i o u r , a n d t h e s n a i l b e h a v i o u r h a s t o b e r e g a r d e d a s p a r t o f t h e phenotypic expression of fluke genes. T h e genes in one organism's cells, then, c a n h a v e e x t e n d e d p h e n o t y p i c i n f l u e n c e o n t h e l i v i n g b o d y o f a n o t h e r o r g a n i s m ; i n this c a s e a p a r a s i t e ' s genes
find
phenotypic
expression
in
the
behaviour
o f its
host.
The
p a r a s i t o l o g y l i t e r a t u r e i s full o f i n t e r e s t i n g e x a m p l e s w h i c h a r e n o w u s u a l l y i n t e r p r e t e d a s a d a p t i v e m a n i p u l a t i o n o f hosts b y p a r a s i t e s ( e . g . H o l m e s & Bethel 1 9 7 2 ; L o v e 1980). It has not, to be sure, a l w a y s b e e n f a s h i o n a b l e a m o n g parasitologists to m a k e such interpretations explicit. For instance, an important review of parasitic castration in C r u s t a c e a
(Reinhard
1956)
is
packed with detailed information and speculation on the precise physiologic a l r o u t e s b y w h i c h p a r a s i t e s c a s t r a t e t h e i r hosts, b u t i s a l m o s t d e v o i d o f discussion o n w h y t h e y m i g h t h a v e b e e n selected t o d o so, o r w h e t h e r , instead, castration is s i m p l y a fortuitous b y p r o d u c t of parasitization. It m a y be an interesting indication of c h a n g i n g scientific fashions that a m o r e recent review (Baudoin 1975) extensively considers the functional significance of parasitic castration from the i n d i v i d u a l parasite's point o f v i e w . B a u d o i n c o n c l u d e s : ' T h e m a i n theses o f this p a p e r a r e ( 1 ) t h a t p a r a s i t i c c a s t r a t i o n c a n b e v i e w e d a s a p a r a s i t e ' s a d a p t a t i o n a n d (2) t h a t a d v a n t a g e s d e r i v e d f r o m this a d a p t a t i o n a r e a r e s u l t o f r e d u c t i o n i n h o s t r e p r o d u c t i v e effort; w h i c h i n t u r n g i v e s rise t o i n c r e a s e d h o s t s u r v i v o r s h i p , i n c r e a s e d h o s t g r o w t h and/or increased e n e r g y a v a i l a b l e to the parasite t h e r e b y i n c r e a s i n g the p a r a s i t e ' s D a r w i n i a n f i t n e s s . ' T h i s is, o f c o u r s e , v e r y m u c h t h e a r g u m e n t I h a v e just followed in discussing parasite-induced t h i c k e n i n g of snail shells. A g a i n , a b e l i e f that parasitic castration is a parasite a d a p t a t i o n l o g i c a l l y
Host Phenotypes of Parasite Genes
214
i m p l i e s t h a t t h e r e m u s t b e , o r a t least m u s t h a v e b e e n , p a r a s i t e g e n e s 'for' changes
in
host
physiology.
T h e symptoms of parasitic
castration,
sex-
c h a n g e , increased size, or w h a t e v e r they m a y be, are properly regarded as extended phenotypic manifestations of parasite genes. The
alternative
physiology
and
pathological
to
Baudoin's
interpretation
is
that
changes
b e h a v i o u r are not parasite adaptations,
byproducts
of
infection.
Consider
the
in
host
but simply dull
parasitic
barnacle
( t h o u g h in its a d u l t s t a g e it l o o k s m o r e l i k e a f u n g u s ) Sacculina. It m i g h t be said t h a t Sacculina d o e s n o t d i r e c t l y b e n e f i t f r o m t h e c a s t r a t i o n o f its c r a b host, but s i m p l y sucks n u t r i m e n t from all t h r o u g h the host's b o d y , and as a side-effect o f its d e v o u r i n g t h e tissues o f t h e g o n a d s t h e c r a b s h o w s t h e s y m p t o m s o f castration. I n support o f the a d a p t a t i o n hypothesis, h o w e v e r , B a u d o i n points to those cases in w h i c h parasites a c h i e v e the castration by synthesis of host h o r m o n e s , surely a specific a d a p t a t i o n rather than a b o r i n g b y p r o d u c t . E v e n in those cases w h e r e the castration is initially caused as a b y p r o d u c t o f t h e d e v o u r i n g o f g o n a d a l tissue, m y s u s p i c i o n i s t h a t s e l e c t i o n would
subsequently
act
on
parasites
to
modify
the
details
of
their
p h y s i o l o g i c a l effects o n hosts, m o d i f y t h e m i n a w a y f a v o u r a b l e t o t h e p a r a s i t e ' s w e l l - b e i n g . Sacculina p r e s u m a b l y h a s s o m e o p t i o n s o v e r w h i c h p a r t s o f t h e c r a b ' s b o d y its r o o t s y s t e m i n v a d e s f i r s t . N a t u r a l s e l e c t i o n i s s u r e l y l i k e l y t o f a v o u r g e n e s i n Sacculina t h a t c a u s e i t t o i n v a d e g o n a d a l tissue before i n v a d i n g v i t a l o r g a n s o n w h i c h t h e c r a b ' s s u r v i v a l d e p e n d s . A p p l y i n g this k i n d o f a r g u m e n t a t a m o r e d e t a i l e d l e v e l , s i n c e g o n a d a l d e s t r u c t i o n has m u l t i p l e a n d c o m p l e x effects o n c r a b p h y s i o l o g y , a n a t o m y a n d b e h a v i o u r , i t is entirely reasonable to guess that selection w o u l d act on parasites to finetune
their
initially
castration
fortuitous
t e c h n i q u e so
consequences
as to increase
of castration.
p a r a s i t o l o g i s t s w o u l d a g r e e w i t h this f e e l i n g
their benefit from
I
(P.
believe O.
many
Lawrence,
the
modern personal
c o m m u n i c a t i o n ) . A l l that I am a d d i n g , then, is the l o g i c a l point that the c o m m o n b e l i e f t h a t p a r a s i t i c c a s t r a t i o n i s a n a d a p t a t i o n i m p l i e s t h a t the m o d i f i e d host p h e n o t y p e i s p a r t o f t h e e x t e n d e d p h e n o t y p e o f p a r a s i t e g e n e s . P a r a s i t e s often s t u n t t h e g r o w t h of t h e i r hosts, a n d it is e a s y to see this as a b o r i n g b y p r o d u c t o f i n f e c t i o n . M o r e i n t e r e s t t h e r e f o r e a t t a c h e s t o those r a r e r c a s e s i n w h i c h p a r a s i t e s e n h a n c e host g r o w t h , a n d I h a v e a l r e a d y m e n t i o n e d t h e c a s e o f t h e t h i c k e n e d s n a i l s h e l l s . C h e n g ( 1 9 7 3 , p . 22) b e g i n s his a c c o u n t of such cases w i t h a r e v e a l i n g sentence: ' A l t h o u g h one generally considers p a r a s i t e s t o b e d e t r i m e n t a l t o t h e i r hosts a n d c a u s e t h e loss o f e n e r g y a n d poor health, instances are k n o w n w h e r e the o c c u r r e n c e of parasites actually i n d u c e s e n h a n c e d g r o w t h o f t h e h o s t . ' B u t C h e n g i s h e r e s o u n d i n g like a medical doctor rather than
like a
Darwinian
biologist.
If 'detriment'
is
defined in terms of r e p r o d u c t i v e success rather than survival a n d 'health', it i s p r o b a b l e t h a t g r o w t h - e n h a n c e m e n t i s i n d e e d d e t r i m e n t a l t o t h e host, for t h e r e a s o n s g i v e n i n m y d i s c u s s i o n o f s n a i l shells.
N a t u r a l s e l e c t i o n has
Host P h e n o t y p e s o f P a r a s i t e G e n e s
215
p r e s u m a b l y f a v o u r e d an o p t i m a l host size, a n d if a parasite causes the host to d e v i a t e f r o m this size in either direction it is p r o b a b l y h a r m i n g t h e h o s t ' s r e p r o d u c t i v e success, e v e n if it is at the s a m e time p r o m o t i n g host s u r v i v a l . A l l the e x a m p l e s o f g r o w t h - e n h a n c e m e n t g i v e n b y C h e n g c a n b e easily understood as parasite-induced switches of resources a w a y from investment i n host r e p r o d u c t i o n , w h i c h i s o f n o i n t e r e s t t o t h e p a r a s i t e , t o t h e g r o w t h and survival of the host's o w n b o d y , w h i c h is of g r e a t interest to the parasite (again we must b e w a r e of the group-selectionist p l e a that the existence of a n e w g e n e r a t i o n o f hosts i s o f i m p o r t a n c e t o t h e p a r a s i t e species). M i c e i n f e c t e d b y l a r v a e o f t h e t a p e w o r m Spirometra mansanoides g r o w faster t h a n u n i n f e c t e d m i c e . I t h a s b e e n s h o w n t h a t t h e t a p e w o r m s a c h i e v e this b y secreting a substance resembling a mouse g r o w t h h o r m o n e . M o r e d r a m a t i c a l l y , b e e t l e l a r v a e o f t h e g e n u s Tribolium, w h e n i n f e c t e d b y t h e s p o r o z o a n Nosema, u s u a l l y fail t o m e t a m o r p h o s e i n t o a d u l t s . I n s t e a d t h e y c o n t i n u e t o g r o w t h r o u g h a s m a n y a s six e x t r a l a r v a l m o u l t s , e n d i n g u p a s g i a n t l a r v a e weighing more than twice as m u c h as non-parasitized controls. Evidence suggests
that
this
m a j o r shift
in
beetle
priorities,
from
reproduction
to
i n d i v i d u a l g r o w t h , i s d u e t o t h e s y n t h e s i s o f j u v e n i l e h o r m o n e , o r its c l o s e a n a l o g u e , b y t h e p r o t o z o a n p a r a s i t e . A g a i n this i s o f i n t e r e s t b e c a u s e , a s a l r e a d y s u g g e s t e d for t h e c a s e o f p a r a s i t i c c a s t r a t i o n o f Crustacea, i t m a k e s the
boring
special
byproduct
molecules
theory
ordinarily
all
but
untenable. Juvenile
synthesized
by
insects,
not
hormones protozoa.
are The
synthesis o f a n i n s e c t h o r m o n e b y a p r o t o z o a n p a r a s i t e h a s t o b e r e g a r d e d a s a specific a n d r a t h e r e l a b o r a t e a d a p t a t i o n . T h e e v o l u t i o n o f t h e c a p a c i t y t o s y n t h e s i z e j u v e n i l e h o r m o n e b y Nosema m u s t h a v e c o m e a b o u t t h r o u g h t h e s e l e c t i o n o f g e n e s i n t h e Nosema g e n e - p o o l . T h e p h e n o t y p i c effect o f t h e s e g e n e s , w h i c h led t o t h e i r s u r v i v a l i n t h e Nosema g e n e - p o o l , w a s a n e x t e n d e d p h e n o t y p i c effect, a n effect w h i c h m a n i f e s t e d i t s e l f i n b e e t l e b o d i e s . O n c e a g a i n t h e p r o b l e m o f i n d i v i d u a l b e n e f i t v e r s u s g r o u p b e n e f i t arises, and in an a c u t e form. A p r o t o z o a n is so small in c o m p a r i s o n w i t h a beetle l a r v a t h a t a s i n g l e p r o t o z o a n , o n its o w n , c o u l d n o t m u s t e r a s u f f i c i e n t d o s e o f h o r m o n e t o affect the b e e t l e . H o r m o n e m a n u f a c t u r e m u s t b e a g r o u p effort by large n u m b e r s of i n d i v i d u a l p r o t o z o a . It benefits all i n d i v i d u a l parasites i n the b e e t l e , b u t i t m u s t a l s o cost e a c h i n d i v i d u a l s o m e t h i n g t o a d d his t i n y c o n t r i b u t i o n t o t h e g r o u p c h e m i c a l effort. I f t h e i n d i v i d u a l p r o t o z o a w e r e genetically heterogeneous, consider w h a t would happen. A s s u m e a majority of protozoa cooperating in synthesizing hormone. An individual with a rare g e n e t h a t m a d e h i m o p t o u t o f t h e g r o u p effort w o u l d s a v e h i m s e l f t h e c o s t o f synthesis. S u c h a s a v i n g w o u l d be of i m m e d i a t e benefit to h i m , a n d to the selfish g e n e t h a t m a d e h i m o p t o u t . T h e loss o f his c o n t r i b u t i o n t o t h e g r o u p synthesis w o u l d h u r t his r i v a l s j u s t a s m u c h a s i t h u r t h i m . I n a n y c a s e t h e loss t o t h e g r o u p ' s
productivity would
be very small,
though
it w o u l d
represent a major s a v i n g to him. T h e r e f o r e , e x c e p t u n d e r special conditions,
216
Host Phenotypes of Parasite Genes
taking part in a c o o p e r a t i v e g r o u p synthesis together w i t h genetic rivals is n o t a n e v o l u t i o n a r i l y s t a b l e s t r a t e g y . W e m u s t t h e r e f o r e p r e d i c t t h a t all the Nosema i n a g i v e n b e e t l e w i l l b e f o u n d t o b e c l o s e r e l a t i v e s , p r o b a b l y a n identical c l o n e . I d o n ' t k n o w of a n y direct e v i d e n c e here, but the expectation i s i n l i n e w i t h t h e t y p i c a l s p o r o z o a n life c y c l e . Baudoin
properly
emphasizes
the
analogous
point
in
connection with
p a r a s i t i c c a s t r a t i o n . H e h a s a s e c t i o n e n t i t l e d ' K i n s h i p o f c a s t r a t o r s i n the same
individual
invariably
host',
produced
offspring . . . parasitic
in
which
he
either
by
single
castration
is
says
'Parasitic
parasites
usually
or
castration by
produced
their either
is
almost
immediate by
single
g e n o t y p e s or by v e r y closely related g e n o t y p e s . M e t a c e r c a r i a l infections in snails a r e e x c e p t i o n s . . . I n t h e s e c a s e s , h o w e v e r , p a r a s i t i c c a s t r a t i o n m a y b e i n c i d e n t a l . ' B a u d o i n i s f u l l y a w a r e o f t h e s i g n i f i c a n c e o f these f a c t s : ' . . . the g e n e t i c r e l a t i o n s h i p o f c a s t r a t o r s w i t h i n i n d i v i d u a l hosts i s s u c h t h a t n a t u r a l s e l e c t i o n a t t h e l e v e l o f i n d i v i d u a l g e n o t y p e s c a n a c c o u n t for t h e o b s e r v e d effects'. M a n y f a s c i n a t i n g e x a m p l e s o f p a r a s i t e s m a n i p u l a t i n g the b e h a v i o u r o f t h e i r hosts c a n b e g i v e n . F o r n e m a t o m o r p h l a r v a e w h o n e e d t o b r e a k o u t o f t h e i r i n s e c t hosts a n d g e t i n t o w a t e r w h e r e t h e y l i v e a s a d u l t s , ' . . . a m a j o r d i f f i c u l t y i n t h e p a r a s i t e ' s life i s t h e r e t u r n t o w a t e r .
I t is, t h e r e f o r e , o f
p a r t i c u l a r i n t e r e s t t h a t t h e p a r a s i t e a p p e a r s t o affect t h e b e h a v i o u r o f its h o s t , a n d " e n c o u r a g e s " i t t o r e t u r n t o w a t e r . T h e m e c h a n i s m b y w h i c h this i s a c h i e v e d i s o b s c u r e , b u t t h e r e a r e sufficient i s o l a t e d r e p o r t s t o certify t h a t t h e p a r a s i t e d o e s i n f l u e n c e its h o s t , a n d often s u i c i d a l l y for t h e host . . . O n e of the m o r e d r a m a t i c reports describes an infected bee flying o v e r a pool and, w h e n a b o u t s i x feet o v e r it, d i v i n g s t r a i g h t i n t o t h e w a t e r . I m m e d i a t e l y o n i m p a c t the g o r d i a n w o r m burst out and s w a m into the w a t e r , the m a i m e d b e e b e i n g left t o d i e ' ( C r o l l 1 9 6 6 ) . P a r a s i t e s t h a t h a v e a life c y c l e i n v o l v i n g a n i n t e r m e d i a t e host, from w h i c h t h e y h a v e t o m o v e t o a d e f i n i t i v e h o s t , o f t e n m a n i p u l a t e t h e b e h a v i o u r o f the i n t e r m e d i a t e h o s t t o m a k e i t m o r e l i k e l y t o b e e a t e n b y t h e d e f i n i t i v e host. W e h a v e a l r e a d y s e e n a n e x a m p l e o f this, t h e c a s e o f Leucochloridium i n snail tentacles. H o l m e s and Bethel
(1972)
have reviewed many examples, and
they h a v e t h e m s e l v e s p r o v i d e d us w i t h o n e of the most t h o r o u g h l y researched cases (Bethel & H o l m e s 1 9 7 3 ) . T h e y studied t w o species of a c a n t h o c e p h a l a n w o r m s , Polymorphus paradoxus a n d P. marilis.
Both
use a f r e s h w a t e r
'shrimp'
( r e a l l y a n a m p h i p o d ) , Gammarus lacustris, a s a n i n t e r m e d i a t e host, a n d b o t h use d u c k s as t h e d e f i n i t i v e h o s t . P. paradoxus, h o w e v e r , s p e c i a l i z e s in the m a l l a r d , w h i c h is a s u r f a c e - d a b b l i n g d u c k , w h i l e P. marilis s p e c i a l i z e s in d i v i n g d u c k s . I d e a l l y t h e n , P . paradoxus m i g h t b e n e f i t b y m a k i n g its s h r i m p s s w i m to the surface, w h e r e they are likely to be eaten by m a l l a r d s , w h i l e P. marilis m i g h t b e n e f i t b y m a k i n g its s h r i m p s a v o i d t h e s u r f a c e . U n i n f e c t e d Gammarus lacustris t e n d to a v o i d l i g h t , a n d s t a y c l o s e to the l a k e
Host Phenotypes of Parasite Genes
217
bottom. Bethel and H o l m e s noticed striking differences in the b e h a v i o u r of s h r i m p s i n f e c t e d w i t h c y s t a c a n t h s o f P . paradoxus. T h e y s t a y e d c l o s e t o t h e surface, and c l u n g tenaciously to surface plants a n d e v e n to the hairs on the researchers' legs. T h i s s u r f a c e - h u g g i n g b e h a v i o u r w o u l d p r e s u m a b l y m a k e them v u l n e r a b l e to predation by d a b b l i n g m a l l a r d s , a n d also by muskrats w h i c h a r e a n a l t e r n a t i v e d e f i n i t i v e host o f P . paradoxus. B e t h e l a n d H o l m e s believe
that
the
habit
of
clinging
to
weeds
makes
infected
shrimps
particularly vulnerable to muskrats, w h o gather floating vegetation and take it h o m e to feed off it. L a b o r a t o r y tests c o n f i r m e d t h a t s h r i m p s i n f e c t e d w i t h c y s t a c a n t h s o f P . paradoxus seek t h e l i g h t e d h a l f o f a t a n k , a n d a l s o p o s i t i v e l y a p p r o a c h t h e source of light. T h i s is the opposite of the b e h a v i o u r s h o w n by uninfected s h r i m p s . I n c i d e n t a l l y , i t i s n o t t h a t t h e i n f e c t e d s h r i m p s w e r e g e n e r a l l y sick and floated passively to the surface, as in the c o m p a r a b l e case of C r o w d e n a n d B r o o m ' s ( 1 9 8 0 ) fish. T h e s e s h r i m p s fed a c t i v e l y , o f t e n l e a v i n g t h e s u r f a c e l a y e r t o d o so, b u t w h e n t h e y c a p t u r e d a m o r s e l o f f o o d t h e y p r o m p t l y t o o k i t to the surface to eat it w h e r e a s a n o r m a l s h i m p w o u l d h a v e t a k e n it to the bottom. A n d w h e n startled in mid water, instead of d i v i n g to the b o t t o m as a n o r m a l s h r i m p w o u l d , t h e y h e a d e d for t h e s u r f a c e . S h r i m p s i n f e c t e d b y c y s t a c a n t h s o f t h e o t h e r s p e c i e s , P . marilis, h o w e v e r , d o n o t h u g t h e s u r f a c e . I n l a b o r a t o r y tests t h e y a d m i t t e d l y s o u g h t t h e l i g h t e d h a l f o f a n a q u a r i u m i n p r e f e r e n c e t o t h e d a r k half, b u t t h e y d i d n o t o r i e n t positively t o w a r d s the source of l i g h t : they distributed themselves r a n d o m l y i n the l i g h t e d half, r a t h e r t h a n a t t h e s u r f a c e . W h e n s t a r t l e d , t h e y w e n t t o the b o t t o m r a t h e r t h a n t o t h e s u r f a c e . B e t h e l a n d H o l m e s s u g g e s t t h a t t h e t w o s p e c i e s o f p a r a s i t e m o d i f y t h e b e h a v i o u r o f t h e i r i n t e r m e d i a t e host i n different w a y s , c a l c u l a t e d t o m a k e t h e s h r i m p s m o r e v u l n e r a b l e t o p r e d a t i o n b y t h e i r d e f i n i t i v e hosts, s u r f a c e - f e e d i n g a n d d i v i n g p r e d a t o r s r e s p e c t i v e l y . A later p a p e r (Bethel & H o l m e s 1977) p r o v i d e s partial c o n f i r m a t i o n of this
hypothesis.
Captive
mallards
and
muskrats
in
the
laboratory
took
s h r i m p s i n f e c t e d w i t h P. paradoxus at a h i g h e r r a t e t h a n t h e y t o o k u n i n f e c t e d s h r i m p s . S h r i m p s i n f e c t e d w i t h P . marilis, h o w e v e r , w e r e n o t t a k e n a n y m o r e often t h a n u n i n f e c t e d o n e s , e i t h e r b y m a l l a r d s o r b y m u s k r a t s .
It would
obviously
a
predator,
be
desirable
predicting
to
that
do
the
shrimps
reciprocal infected
experiment
with
with
cystacanths
of P.
diving marilis
w o u l d , i n this c a s e , b e r e l a t i v e l y m o r e v u l n e r a b l e . T h i s e x p e r i m e n t d o e s n o t appear to have been done. Let us provisionally accept Bethel and Holmes's hypothesis, and rephrase i t i n the l a n g u a g e o f t h e e x t e n d e d p h e n o t y p e . T h e a l t e r e d b e h a v i o u r o f t h e shrimp is r e g a r d e d as an a d a p t a t i o n on the part of the a c a n t h o c e p h a l a n p a r a s i t e . I f this h a s c o m e a b o u t t h r o u g h n a t u r a l s e l e c t i o n , t h e r e m u s t h a v e been
genetic
variation
'for'
shrimp
behaviour
in
the
worm
gene-pool,
o t h e r w i s e t h e r e w o u l d h a v e b e e n n o t h i n g for n a t u r a l s e l e c t i o n t o w o r k o n .
2l8
Host Phenotypes of Parasite Genes
We m a y , therefore, talk of w o r m genes h a v i n g phenotypic expression in s h r i m p b o d i e s , i n j u s t t h e s a m e sense a s w e a r e a c c u s t o m e d t o t a l k i n g o f h u m a n genes h a v i n g phenotypic expression in h u m a n bodies. T h e c a s e o f t h e f l u k e ( ' b r a i n w o r m ' ) Dicrocoelium dendriticum i s often q u o t e d a s a n o t h e r e l e g a n t e x a m p l e o f a p a r a s i t e m a n i p u l a t i n g a n i n t e r m e d i a t e host t o i n c r e a s e its c h a n c e s o f e n d i n g u p i n its d e f i n i t i v e h o s t ( W i c k l e r 1 9 7 6 ; L o v e 1980).
The
definitive
host
is
an
ungulate
such
as
a
sheep,
and
the
i n t e r m e d i a t e hosts a r e f i r s t a s n a i l a n d t h a n a n a n t . T h e n o r m a l life c y c l e c a l l s for t h e a n t t o b e a c c i d e n t a l l y e a t e n b y t h e s h e e p . I t s e e m s t h a t t h e f l u k e cercaria
achieves
this
in
a way
analogous
to
t h a t o f the Leucochloridium
m e n t i o n e d a b o v e . B y b u r r o w i n g i n t o t h e s u b o e s o p h a g e a l g a n g l i o n , the a p t l y n a m e d ' b r a i n w o r m ' c h a n g e s the ant's behaviour. W h e r e a s an uninfected a n t w o u l d n o r m a l l y r e t r e a t i n t o its nest w h e n i t b e c a m e c o l d , i n f e c t e d ants c l i m b to the top of grass stems, c l a m p their j a w s in the plant and remain i m m o b i l e as if asleep. H e r e they are v u l n e r a b l e to b e i n g eaten by the w o r m ' s d e f i n i t i v e h o s t . T h e i n f e c t e d a n t , l i k e a n o r m a l a n t , d o e s r e t r e a t d o w n the g r a s s s t e m t o a v o i d d e a t h f r o m t h e m i d d a y h e a t — w h i c h w o u l d b e b a d for t h e p a r a s i t e — b u t i t r e t u r n s t o its a e r i a l r e s t i n g p o s i t i o n i n t h e c o o l o f the afternoon ( L o v e 1980). W i c k l e r (1976) says that of the a p p r o x i m a t e l y fifty c e r c a r i a e t h a t i n f e c t a g i v e n a n t , o n l y o n e b u r r o w s i n t o t h e b r a i n a n d i t dies in the process:
' I t s a c r i f i c e s i t s e l f for t h e b e n e f i t o f t h e o t h e r c e r c a r i a e . '
U n d e r s t a n d a b l y , W i c k l e r therefore predicts that the g r o u p of cercariae in an ant will be found to be a p o l y e m b r y o n i c clone. A n e v e n m o r e e l a b o r a t e e x a m p l e i s t h e c a s e o f c r o w n g a l l , o n e o f t h e few k n o w n p l a n t c a n c e r s ( K e r r 1 9 7 8 ; S c h e l l e t al. 1 9 7 9 ) . E x c e p t i o n a l l y for a c a n c e r i t i s i n d u c e d b y a b a c t e r i u m , Agrobacterium. T h e s e b a c t e r i a i n d u c e t h e c a n c e r in the p l a n t o n l y if they themselves c o n t a i n a Ti plasmid, a small ring of extrachromosomal
DNA.
The
Ti
plasmid
may
be
regarded
as
an
a u t o n o m o u s r e p l i c a t o r ( C h a p t e r 9 ) a l t h o u g h , like a n y other D N A replicator, i t c a n n o t s u c c e e d a p a r t f r o m t h e c e l l u l a r m a c h i n e r y p u t t o g e t h e r u n d e r the i n f l u e n c e o f o t h e r D N A r e p l i c a t o r s , i n this c a s e t h o s e o f t h e host. T i g e n e s a r e t r a n s f e r r e d f r o m b a c t e r i a l t o p l a n t c e l l s , a n d t h e i n f e c t e d p l a n t cells a r e i n d u c e d to m u l t i p l y u n c o n t r o l l a b l y , w h i c h is w h y the c o n d i t i o n is called a c a n c e r . T h e T i genes also c a u s e the p l a n t cells t o synthesize large quantities of substances called opines, w h i c h the plants w o u l d not normally make, and w h i c h they c a n n o t use. T h e interesting point is that, in an e n v i r o n m e n t rich in opines, Ti-infected bacteria survive and reproduce m u c h better than noninfected b a c t e r i a . T h i s is b e c a u s e the Ti p l a s m i d provides the b a c t e r i u m with a set o f g e n e s w h i c h e n a b l e t h e b a c t e r i u m t o use t h e o p i n e s a s a s o u r c e o f energy
and
chemicals.
The
Ti
plasmids
could
almost
be
regarded
as
practising artificial selection in favour of infected bacteria, hence in favour of copies of themselves. T h e opines also function as bacterial 'aphrodisiacs', as K e r r p u t s it, p r o m o t i n g b a c t e r i a l c o n j u g a t i o n a n d t h e r e f o r e p l a s m i d transfer.
Host Phenotypes of Parasite Genes
Kerr
(1978)
concludes:
'It
is
a
very
elegant
example
219
of biological
e v o l u t i o n ; it e v e n d e m o n s t r a t e s a p p a r e n t altruism in b a c t e r i a l g e n e s . . . T h e D N A w h i c h is transferred from b a c t e r i u m to p l a n t has no future; it dies w h e n the p l a n t c e l l d i e s . H o w e v e r , b y a l t e r i n g t h e p l a n t c e l l t o p r o d u c e a n o p i n e , i t e n s u r e s (a) p r e f e r e n t i a l s e l e c t i o n o f t h e s a m e D N A i n b a c t e r i a l c e l l s and
(b)
transfer o f t h a t
DNA
to other bacterial
cells.
It demonstrates
evolution a t the level o f genes, not organisms, w h i c h m a y o n l y b e g e n e carriers.' (Such statements are, of course, music to my ears, b u t I h o p e K e r r will forgive my p u b l i c l y w o n d e r i n g at the gratuitous c a u t i o n of ' m a y o n l y b e ' g e n e carriers. It is a bit like s a y i n g ' T h e eyes m a y be the w i n d o w s of the soul' or ' O , my L u v e m a y be like a red red rose'. It m a y h a v e b e e n the w o r k of an editorial hand!) K e r r continues: 'In n a t u r a l l y - i n d u c e d c r o w n galls o n m a n y ( b u t n o t all) hosts, v e r y f e w b a c t e r i a s u r v i v e i n t h e g a l l . . . A t f i r s t s i g h t , i t w o u l d appear that pathogenicity is conferring no biological a d v a n t a g e . It is o n l y w h e n o n e c o n s i d e r s o p i n e p r o d u c t i o n b y t h e h o s t a n d its effect o n bacteria living at the surface of the g a l l , that the strong selective a d v a n t a g e o f g e n e s for p a t h o g e n i c i t y b e c o m e s c l e a r . ' M a y r (1963, pp.
1 9 6 - 1 9 7 ) discusses t h e p h e n o m e n o n o f p l a n t s m a k i n g
g a l l s t o h o u s e i n s e c t s , i n t e r m s s o f a v o u r a b l e t o m y thesis t h a t I c a n q u o t e him verbatim almost without c o m m e n t : W h y . . . s h o u l d a p l a n t m a k e t h e g a l l s u c h a p e r f e c t d o m i c i l e for a n i n s e c t t h a t i s its e n e m y ? A c t u a l l y w e a r e d e a l i n g h e r e w i t h t w o selection pressures. On the o n e h a n d , selection w o r k s on a p o p u l a t i o n of gall
insects
and
favors
those
whose
gall-inducing
chemicals
stimulate the p r o d u c t i o n of galls g i v i n g m a x i m u m p r o t e c t i o n to the y o u n g l a r v a . T h i s , o b v i o u s l y , i s a m a t t e r o f life o r d e a t h for t h e g a l l insect
and
thus
constitutes
a
very
high
selection
pressure.
The
o p p o s i n g selection pressure on the p l a n t is in most cases quite small b e c a u s e h a v i n g a few galls will depress v i a b i l i t y of the plant host only v e r y s l i g h t l y . T h e ' c o m p r o m i s e ' i n this c a s e i s a l l i n f a v o r o f t h e g a l l insect. T o o h i g h a density of the g a l l insect is u s u a l l y p r e v e n t e d by d e n s i t y - d e p e n d e n t factors not related to the p l a n t host.
M a y r is here i n v o k i n g the e q u i v a l e n t of the i i f e / d i n n e r p r i n c i p l e ' to e x p l a i n w h y the p l a n t d o e s n o t f i g h t b a c k a g a i n s t t h e r e m a r k a b l e m a n i p u l a t i o n b y the i n s e c t . I t i s n e c e s s a r y for m e t o a d d o n l y t h i s . I f M a y r i s r i g h t t h a t t h e g a l l i s a n a d a p t a t i o n for t h e b e n e f i t o f t h e i n s e c t a n d n o t t h e p l a n t , i t c a n h a v e e v o l v e d o n l y t h r o u g h the n a t u r a l selection of genes in the insect g e n e pool. L o g i c a l l y , we h a v e to r e g a r d these as genes w i t h p h e n o t y p i c expression i n p l a n t tissue, i n t h e s a m e sense a s s o m e o t h e r g e n e o f t h e i n s e c t , s a y o n e for e y e c o l o u r , c a n b e s a i d t o h a v e p h e n o t y p i c e x p r e s s i o n i n i n s e c t tissue. C o l l e a g u e s w i t h w h o m I discuss the d o c t r i n e of the e x t e n d e d p h e n o t y p e
220
Host Phenotypes of Parasite Genes
repeatedly c o m e up with the same entertaining speculations. Is it just an a c c i d e n t t h a t w e s n e e z e w h e n g e t t i n g a c o l d , o r c o u l d i t b e a result o f m a n i p u l a t i o n by viruses to increase their c h a n c e s of infecting another host? Do a n y v e n e r e a l diseases increase the libido, e v e n if o n l y b y i n d u c i n g an itch, like e x t r a c t o f S p a n i s h f l y ? D o the b e h a v i o u r a l s y m p t o m s o f rabies infection increase the c h a n c e of the virus b e i n g passed on
(Bacon &
Macdonald
1 9 8 0 ) ? ' W h e n a d o g g e t s r a b i e s , its t e m p e r c h a n g e s q u i c k l y . I t i s often m o r e a f f e c t i o n a t e for a d a y o r t w o , a n d g i v e n t o l i c k i n g its h u m a n c o n t a c t s , a d a n g e r o u s p r a c t i c e , for t h e v i r u s i s a l r e a d y i n its s a l i v a . S o o n i t g r o w s restless a n d w a n d e r s off, r e a d y t o b i t e a n y o n e t h a t g e t s i n its w a y ' Britannica
1977).
E v e n non-carnivorous animals are driven
(Encyclopaedia by the rabies
virus to v i c i o u s biting, and there are recorded cases of h u m a n s contracting t h e d i s e a s e f r o m t h e b i t e s o f n o r m a l l y h a r m l e s s f r u i t - e a t i n g b a t s . A p a r t from the
obvious
wandering'
power
of biting
to
might very well serve
(Hamilton &
May
spread
a
saliva-borne
to spread
virus,
'restless
the virus m o r e effectively
1 9 7 7 ) . T h a t the w i d e s p r e a d a v a i l a b i l i t y o f c h e a p air
t r a v e l h a s h a d a d r a m a t i c i m p a c t o n the s p r e a d o f h u m a n d i s e a s e i s o b v i o u s : dare we w o n d e r w h e t h e r the phrase 'travel b u g ' might have a more than metaphorical significance? T h e reader will p r o b a b l y , like me, f i n d such speculations far-fetched. T h e y a r e i n t e n d e d o n l y a s l i g h t - h e a r t e d i l l u s t r a t i o n s o f t h e kind o f t h i n g t h a t m i g h t g o o n (see a l s o E w a l d , 1 9 8 0 , w h o d r a w s a t t e n t i o n t o t h e m e d i c a l s i g n i f i c a n c e o f this k i n d o f t h i n k i n g ) . A l l I r e a l l y n e e d t o e s t a b l i s h i s t h a t i n some e x a m p l e s h o s t s y m p t o m s c a n p r o p e r l y b e r e g a r d e d a s p a r a s i t i c a d a p t a t i o n ; s a y , for instance,
the
Peter
Pan
syndrome
in
Tribolium
induced
by
protozoan-
synthesized j u v e n i l e h o r m o n e . G i v e n such an admitted parasite adaptation, t h e c o n c l u s i o n I w i s h t o d r a w i s n o t r e a l l y d i s p u t a b l e . I f host b e h a v i o u r o r p h y s i o l o g y is a parasite a d a p t a t i o n , there must be (have been) parasite genes ' f o r ' m o d i f y i n g t h e h o s t , a n d t h e h o s t m o d i f i c a t i o n s a r e t h e r e f o r e p a r t o f the phenotypic
expression
of those
parasite genes.
The
extended
phenotype
r e a c h e s o u t o f t h e b o d y i n w h o s e c e l l s the g e n e s lie, r e a c h e s o u t t o t h e l i v i n g tissues o f o t h e r o r g a n i s m s . T h e r e l a t i o n s h i p o f Sacculina g e n e t o c r a b b o d y i s n o t i n p r i n c i p l e different f r o m t h e r e l a t i o n s h i p o f c a d d i s g e n e t o s t o n e , n o r i n d e e d different from the r e l a t i o n s h i p o f h u m a n g e n e t o h u m a n s k i n . T h i s i s the f i r s t o f the p o i n t s t h a t I i n t e n d e d t o e s t a b l i s h i n this c h a p t e r . I t h a s t h e c o r o l l a r y , w h i c h I h a v e a l r e a d y e m p h a s i z e d in other terms in C h a p t e r 4, that the b e h a v i o u r of an i n d i v i d u a l m a y n o t a l w a y s b e i n t e r p r e t a b l e a s d e s i g n e d t o m a x i m i z e its o w n g e n e t i c w e l f a r e : i t m a y b e m a x i m i z i n g s o m e b o d y else's g e n e t i c w e l f a r e , i n this c a s e t h a t o f a p a r a s i t e i n s i d e it. I n t h e n e x t c h a p t e r w e s h a l l g o further, a n d see t h a t s o m e o f t h e a t t r i b u t e s o f a n i n d i v i d u a l m a y b e r e g a r d e d a s p h e n o t y p i c expression of genes in other individuals w h o need not necessarily be parasites inside.
Host Phenotypes o f Parasite Genes
2 2 1
T h e s e c o n d p o i n t o f this p r e s e n t c h a p t e r i s t h a t t h e g e n e s t h a t b e a r u p o n any given
extended
phenotypic
trait m a y
be
in
conflict
rather
than
in
concert with one another. I could talk in terms of a n y of the e x a m p l e s g i v e n a b o v e , b u t I shall stick to one, the case of the snail shell t h i c k e n e d by the influence of a fluke. To r e c a p i t u l a t e that story in slightly different terms, a student of snail genetics a n d a student of fluke g e n e t i c s m i g h t e a c h look at the s a m e p h e n o t y p i c v a r i a t i o n , v a r i a t i o n i n s n a i l s h e l l t h i c k n e s s . T h e s n a i l g e n e t i c i s t w o u l d p a r t i t i o n t h e v a r i a n c e between a g e n e t i c a n d a n e n v i r o n mental c o m p o n e n t , by c o r r e l a t i n g the thickness of shells in p a r e n t snails a n d their offspring. T h e f l u k e geneticist w o u l d i n d e p e n d e n t l y p a r t i t i o n the s a m e o b s e r v e d v a r i a n c e i n t o a g e n e t i c a n d a n e n v i r o n m e n t a l c o m p o n e n t , i n his c a s e b y c o r r e l a t i n g t h e shell t h i c k n e s s o f s n a i l s c o n t a i n i n g p a r t i c u l a r f l u k e s w i t h t h e shell t h i c k n e s s o f s n a i l s c o n t a i n i n g t h e o f f s p r i n g o f t h o s e s a m e f l u k e s . As far as the snail g e n e t i c i s t is c o n c e r n e d , t h e fluke c o n t r i b u t i o n is p a r t of w h a t he calls the ' e n v i r o n m e n t a l ' variation.
R e c i p r o c a l l y , for t h e f l u k e
geneticist, v a r i a t i o n d u e to snail genes is ' e n v i r o n m e n t a l ' v a r i a t i o n . An
'extended
geneticist'
would
acknowledge
both
sources
of genetic
variation. He w o u l d h a v e to w o r r y a b o u t the form of their i n t e r a c t i o n — i s it additive, multiplicative, 'epistatic', etc.?—but in principle such worries are a l r e a d y familiar to b o t h the snail geneticist a n d the fluke geneticist. W i t h i n a n y o r g a n i s m , different g e n e s i n f l u e n c e t h e s a m e p h e n o t y p i c t r a i t s , a n d t h e f o r m o f the i n t e r a c t i o n i s a p r o b l e m w i t h r e s p e c t t o g e n e s w i t h i n o n e n o r m a l g e n o m e j u s t a s m u c h a s i t i s for g e n e s i n a n ' e x t e n d e d ' g e n o m e . I n t e r a c t i o n s b e t w e e n t h e effects o f s n a i l g e n e a n d f l u k e g e n e a r e , i n p r i n c i p l e , n o d i f f e r e n t f r o m i n t e r a c t i o n s b e t w e e n t h e effects o f o n e s n a i l g e n e a n d a n o t h e r s n a i l gene. A n d yet, it m a y be said, is there not a rather i m p o r t a n t difference? S n a i l gene m a y interact w i t h snail g e n e in a d d i t i v e , m u l t i p l i c a t i v e , or a n y other w a y s , b u t d o they not b o t h h a v e the s a m e interests a t h e a r t ? B o t h h a v e b e e n s e l e c t e d i n t h e p a s t b e c a u s e t h e y w o r k e d for t h e s a m e e n d , t h e s u r v i v a l a n d r e p r o d u c t i o n o f t h e snails t h a t b o r e t h e m . F l u k e g e n e a n d f l u k e g e n e , t o o , a r e w o r k i n g for t h e s a m e e n d , t h e r e p r o d u c t i v e s u c c e s s o f t h e f l u k e . B u t s n a i l gene and fluke g e n e do not h a v e the s a m e interests at heart. O n e is selected to p r o m o t e snail r e p r o d u c t i o n , the other to p r o m o t e fluke r e p r o d u c t i o n . T h e r e i s t r u t h i n t h e p r o t e s t a t i o n s o f the last p a r a g r a p h , b u t i t i s i m p o r t a n t t o b e c l e a r a b o u t e x a c t l y w h e r e t h a t t r u t h lies. I t i s n o t t h a t t h e r e i s s o m e o b v i o u s t r a d e - u n i o n spirit u n i t i n g f l u k e g e n e s a g a i n s t a r i v a l u n i o n o f s n a i l g e n e s . T o persist w i t h this h a r m l e s s a n t h r o p o m o r p h i s m , e a c h g e n e i s f i g h t i n g o n l y its a l l e l e s a t t h e s a m e l o c u s , a n d i t w i l l ' u n i t e ' w i t h g e n e s a t o t h e r l o c i o n l y insofar as d o i n g so assists it in its selfish w a r a g a i n s t its o w n a l l e l e s . A f l u k e g e n e m a y ' u n i t e ' w i t h o t h e r f l u k e g e n e s i n this w a y b u t , e q u a l l y , i f i t w a s c o n v e n i e n t t o d o so, i t m i g h t u n i t e w i t h p a r t i c u l a r s n a i l g e n e s . A n d i f i t remains true that snail genes are in p r a c t i c e selected to w o r k t o g e t h e r w i t h
Host Phenotypes of Parasite Genes
222
e a c h other a n d against an o p p o s i n g g a n g of fluke genes, the reason is only that snail g e n e s tend to g a i n from the s a m e events in the w o r l d as do other snail g e n e s . F l u k e genes stand to g a i n from other events. A n d the real reason w h y snail genes stand to g a i n from the s a m e events as e a c h other, w h i l e fluke g e n e s s t a n d t o g a i n f r o m a different set o f e v e n t s , i s s i m p l y t h i s : a l l s n a i l g e n e s share
the same
route into
the
next generation—snail
gametes.
All fluke
g e n e s , o n t h e o t h e r h a n d , m u s t use a different r o u t e , f l u k e c e r c a r i a e , t o g e t i n t o t h e n e x t g e n e r a t i o n . I t i s this f a c t a l o n e t h a t ' u n i t e s ' s n a i l g e n e s against fluke genes and v i c e versa. If it w e r e the case that the parasite genes passed out of the host's b o d y inside the host's g a m e t e s , things m i g h t be v e r y d i f f e r e n t . T h e i n t e r e s t s o f host g e n e s a n d p a r a s i t e g e n e s m i g h t n o t b e q u i t e identical, but they w o u l d then be v e r y m u c h closer than in the case of fluke a n d snail. I t f o l l o w s f r o m t h e e x t e n d e d p h e n o t y p e v i e w o f life, t h e n , t h a t c r u c i a l i m p o r t a n c e a t t a c h e s t o the m e a n s b y w h i c h parasites p r o p a g a t e their genes out of a g i v e n host into a n e w host. If the parasite's m e a n s of genetic exit f r o m t h e h o s t ' s b o d y i s t h e s a m e a s t h e h o s t ' s , n a m e l y t h e host's g a m e t e s o r s p o r e s , t h e r e w i l l b e r e l a t i v e l y little c o n f l i c t b e t w e e n t h e ' i n t e r e s t s ' o f p a r a s i t e and
host
genes.
For
example,
both
would
'agree'
about
the
optimum
t h i c k n e s s o f t h e h o s t ' s s h e l l . B o t h w i l l b e s e l e c t e d t o w o r k n o t o n l y for host s u r v i v a l b u t for host r e p r o d u c t i o n a s w e l l , w i t h a l l t h a t t h a t e n t a i l s . T h i s m i g h t i n c l u d e host s u c c e s s i n c o u r t s h i p a n d e v e n , i f t h e p a r a s i t e s a s p i r e t o b e ' i n h e r i t e d ' b y t h e h o s t ' s o w n o f f s p r i n g , host s u c c e s s i n p a r e n t a l c a r e . U n d e r s u c h c i r c u m s t a n c e s t h e i n t e r e s t s o f p a r a s i t e a n d host w o u l d
be likely to
c o i n c i d e t o s u c h a n e x t e n t t h a t i t m i g h t b e c o m e difficult for u s t o d e t e c t t h a t a
separate
parasite
existed
at
all.
It
is
clearly
of g r e a t
interest
for
parasitologists a n d 'symbiologists' to study such v e r y intimate parasites or s y m b i o n t s , s y m b i o n t s w i t h an interest in the success of their host's g a m e t e s as w e l l as in the s u r v i v a l of their host's b o d y . S o m e lichens m i g h t be promisi n g e x a m p l e s , a n d s o m i g h t b a c t e r i a l e n d o s y m b i o n t s o f insects w h i c h a r e t r a n s m i t t e d t r a n s o v a r i a l l y a n d i n s o m e c a s e s s e e m t o i n f l u e n c e t h e host sex ratio (Peleg & Norris 1972). Mitochondria,
chloroplasts,
and
other
cell
organelles
with
their o w n
r e p l i c a t i n g D N A m i g h t a l s o b e g o o d c a n d i d a t e s for s t u d y i n this c o n n e c t i o n . A f a s c i n a t i n g a c c o u n t o f c e l l o r g a n e l l e s a n d m i c r o o r g a n i s m s seen a s s e m i autonomous
symbionts
proceedings
of a
inhabiting
symposium
Richmond and Smith
a
entitled
cellular The
ecology
Cell
as
a
is
given
Habitat,
in
the
edited
by
(1979). T h e closing words of Smith's introductory
chapter are particularly m e m o r a b l e and apposite: 'In non-living habitats, an organism
either
exists
or it does
not.
In
the
cell
habitat,
an
invading
o r g a n i s m c a n p r o g r e s s i v e l y lose p i e c e s o f itself, s l o w l y b l e n d i n g i n t o t h e general
background,
Indeed,
one is
its
reminded
former
existence
of Alice
in
betrayed
Wonderland's
only
by
some
relic.
encounter with
the
Host P h e n o t y p e s o f P a r a s i t e G e n e s
223
C h e s h i r e C a t . A s she w a t c h e d it, " i t v a n i s h e d q u i t e s l o w l y , b e g i n n i n g w i t h the tail, a n d e n d i n g w i t h t h e g r i n , w h i c h r e m a i n e d s o m e t i m e after t h e rest o f it had g o n e " ' (Smith 1979). M a r g u l i s (1976) gives an interesting survey of all t h e d e g r e e s o f v a n i s h i n g o f t h e g r i n . R i c h m o n d ' s (1979) chapter, too, is very c o n g e n i a l to the present thesis: 'It is c o n v e n t i o n a l to regard cells as units of b i o l o g i c a l function. A n o t h e r v i e w , p a r t i c u l a r l y a p p o s i t e t o this s y m p o s i u m , i s t h a t t h e c e l l i s t h e m i n i m a l u n i t capable o f replicating D N A . . . S u c h a c o n c e p t places D N A a t the centre o f biology. T h u s D N A is not r e g a r d e d s i m p l y as a h e r e d i t a r y m e a n s of ensuring the l o n g t e r m s u r v i v a l o f t h e o r g a n i s m s o f w h i c h i t f o r m s p a r t . R a t h e r , i t stresses t h a t t h e p r i m a r y r o l e o f cells i s t o m a x i m i z e t h e a m o u n t a n d d i v e r s i t y o f D N A i n t h e b i o s p h e r e . . . ' T h i s last r e m a r k , i n c i d e n t a l l y , i s u n f o r t u n a t e . M a x i m i z i n g the a m o u n t and diversity of D N A in the biosphere is the concern of nobody and nothing. Rather, each small piece of D N A is selected for its p o w e r t o m a x i m i z e its own s u r v i v a l a n d r e p l i c a t i o n . R i c h m o n d g o e s o n : ' I f t h e c e l l i s c o n s i d e r e d a s a u n i t for t h e r e p l i c a t i o n o f D N A , i t f o l l o w s t h a t D N A a d d i t i o n a l t o t h a t r e q u i r e d for t h e d u p l i c a t i o n o f t h e c e l l m a y a l s o be carried; m o l e c u l a r parasitism, symbiosis and m u t u a l i s m m a y o c c u r at the D N A level, as it does at higher organizational levels in b i o l o g y . ' We h a v e arrived
back
at
the
c o n c e p t o f 'selfish
DNA'
which
was
a subject of
C h a p t e r 9. It is interesting to speculate on whether mitochondria, chloroplasts, and other
DNA-bearing
(Margulis 1970,
organelles
originated
from
parasitic
prokaryotes
1981). But, important as that question is as a m a t t e r of
history, it does not bear, o n e w a y or the other, on my present c o n c e r n . I am h e r e i n t e r e s t e d i n w h e t h e r m i t o c h o n d r i a l D N A i s l i k e l y t o w o r k for t h e s a m e phenotypic ends as nuclear D N A , or whether it is likely to be in conflict with it. T h i s s h o u l d d e p e n d n o t o n t h e h i s t o r i c o r i g i n s o f m i t o c h o n d r i a b u t o n their p r e s e n t m e t h o d o f p r o p a g a t i n g t h e i r D N A . M i t o c h o n d r i a l g e n e s a r e passed o u t o f o n e m e t a z o a n b o d y i n t o a b o d y o f t h e n e x t g e n e r a t i o n i n e g g c y t o p l a s m . A n o p t i m a l female p h e n o t y p e from the p o i n t o f v i e w o f the female's o w n nuclear genes is likely to be v e r y m u c h the s a m e as an o p t i m a l female p h e n o t y p e from the point o f v i e w o f her m i t o c h o n d r i a l D N A . B o t h h a v e an interest in her successfully s u r v i v i n g ,
reproducing, and rearing
offspring. A t least, t h a t i s t r u e a s far a s f e m a l e o f f s p r i n g a r e c o n c e r n e d . M i t o c h o n d r i a p r e s u m a b l y h a v e n o ' w i s h ' for t h e i r b o d i e s t o h a v e s o n s : a m a l e b o d y r e p r e s e n t s t h e e n d o f t h e l i n e a s far a s m i t o c h o n d r i a l d e s c e n t i s concerned. A l l mitochondria in existence h a v e spent the vast majority of their a n c e s t r a l c a r e e r s i n f e m a l e b o d i e s , a n d t h e y m i g h t t e n d t o h a v e w h a t i t takes t o persist i n i n h a b i t i n g f e m a l e b o d i e s .
In birds the interests of
mitochondrial D N A will b e closely similar t o those o f Y - c h r o m o s o m a l D N A , and slightly d i v e r g e n t from those o f a u t o s o m a l a n d X - c h r o m o s o m a l D N A . A n d i f m i t o c h o n d r i a l D N A c o u l d exert p h e n o t y p i c p o w e r i n the e g g o f a
224
Host Phenotypes of Parasite Genes
m a m m a l , i t i s p e r h a p s n o t t o o f a n c i f u l t o i m a g i n e i t f r a n t i c a l l y f i g h t i n g off t h e kiss o f d e a t h o f Y - b e a r i n g s p e r m s ( E b e r h a r d 1 9 8 0 ; C o s m i d e s & T o o b y 1981). B u t i n a n y case, i f the interests o f m i t o c h o n d r i a l D N A a n d n u c l e a r D N A a r e n o t a l w a y s i d e n t i c a l , t h e y a r e v e r y c l o s e , c e r t a i n l y m u c h closer than the interests o f fluke D N A a n d snail D N A . T h e m e s s a g e o f t h e p r e s e n t s e c t i o n i s this. T h e f a c t t h a t s n a i l g e n e s c o n f l i c t w i t h f l u k e g e n e s m o r e t h a n t h e y c o n f l i c t w i t h o t h e r s n a i l g e n e s a t different l o c i i s n o t t h e o b v i o u s f o r e g o n e c o n c l u s i o n i t m i g h t a p p e a r t o b e . I t results s i m p l y f r o m t h e f a c t t h a t a n y t w o g e n e s i n a s n a i l n u c l e u s a r e o b l i g e d t o use the s a m e exit route from the present b o d y into the future. B o t h h a v e the s a m e stake in the success of the present snail in m a n u f a c t u r i n g gametes, g e t t i n g t h e m f e r t i l i z e d , a n d s e c u r i n g t h e s u r v i v a l a n d r e p r o d u c t i o n o f the offspring so formed. F l u k e genes conflict w i t h snail genes in their influence on t h e s h a r e d p h e n o t y p e , s i m p l y b e c a u s e t h e i r d e s t i n y i s s h a r e d for o n l y a short p a r t o f t h e f u t u r e : t h e i r c o m m o n c a u s e i s l i m i t e d t o t h e life o f t h e p r e s e n t host b o d y , a n d d o e s n o t c a r r y o v e r i n t o t h e g a m e t e s a n d o f f s p r i n g o f the present host. T h e role of m i t o c h o n d r i a in the a r g u m e n t is to e x e m p l i f y cases w h e r e p a r a s i t e a n d h o s t g e n e s s h a r e t h e s a m e g a m e t i c d e s t i n y , a t least i n p a r t . I f n u c l e a r genes do not conflict with nuclear genes at other loci, it is only b e c a u s e meiosis is e v e n - h a n d e d : meiosis does not n o r m a l l y favour some loci o v e r others, nor some alleles over others, but scrupulously puts one gene at r a n d o m from
each
diploid
pair
in
every gamete.
Of course
there are
i n s t r u c t i v e e x c e p t i o n s , a n d for m y thesis t h e y a r e s u f f i c i e n t l y i m p o r t a n t t o h a v e d o m i n a t e d t h e t w o c h a p t e r s o n ' o u t l a w s ' a n d 'selfish D N A ' . T h e r e , a s here, an i m p o r t a n t message is that replicating entities will tend to w o r k a g a i n s t e a c h o t h e r t o t h e e x t e n t t h a t t h e y e m p l o y different m e t h o d s o f egress from v e h i c l e to v e h i c l e . Returning symbiotic
to
the
main
relationships
can
subject be
of the
classified
present in
chapter,
various
ways
parasitic for
and
different
purposes. T h e classifications d e v e l o p e d by parasitologists and doctors are no doubt
useful
for
their
purposes,
but
I
want
to
develop
a
particular
classification based on the concept of gene p o w e r . It should be r e m e m b e r e d t h a t , f r o m this p o i n t o f v i e w , t h e n o r m a l r e l a t i o n s h i p b e t w e e n different g e n e s in the same nucleus, e v e n on the same c h r o m o s o m e , is just one extreme on the c o n t i n u u m of parasitic or symbiotic relationships. T h e first d i m e n s i o n o f m y c l a s s i f i c a t i o n h a s a l r e a d y b e e n stressed.
It
c o n c e r n s t h e d e g r e e o f s i m i l a r i t y o r d i f f e r e n c e i n t h e m e t h o d s o f egress from hosts, a n d p r o p a g a t i o n o f host genes a n d parasite genes. A t one e x t r e m e will b e p a r a s i t e s t h a t use t h e h o s t ' s p r o p a g u l e s for their o w n r e p r o d u c t i o n . F o r s u c h p a r a s i t e s a n o p t i m u m host p h e n o t y p e f r o m t h e p a r a s i t e ' s p o i n t o f v i e w i s l i k e l y t o c o i n c i d e w i t h t h e o p t i m u m f r o m t h e p o i n t o f v i e w o f t h e host's o w n g e n e s . T h i s i s n o t t o s a y t h a t t h e host g e n e s w o u l d n o t ' p r e f e r ' t o b e rid
Host Phenotypes of Parasite Genes
225
o f the p a r a s i t e a l t o g e t h e r . B u t b o t h h a v e a n i n t e r e s t i n m a s s - p r o d u c i n g t h e same propagules, a n d both h a v e an interest in d e v e l o p i n g a p h e n o t y p e that i s g o o d for m a s s - p r o d u c i n g t h o s e s a m e p r o p a g u l e s : t h e r i g h t b e a k l e n g t h , w i n g shape, courtship b e h a v i o u r , clutch size, etc., d o w n to m i n u t e details of all a s p e c t s o f t h e p h e n o t y p e . A t the o t h e r e x t r e m e w i l l b e p a r a s i t e s w h o s e g e n e s a r e p a s s e d o n n o t i n t h e host's r e p r o d u c t i v e p r o p a g u l e s b u t , s a y , i n t h e h o s t ' s e x h a l e d b r e a t h , o r i n the host's d e a d b o d y . I n t h e s e c a s e s t h e o p t i m u m h o s t p h e n o t y p e f r o m t h e parasite genes' point of v i e w is likely to be v e r y different from the o p t i m u m host p h e n o t y p e f r o m t h e host g e n e s ' p o i n t o f v i e w . T h e p h e n o t y p e w h i c h emerges will be a c o m p r o m i s e . T h i s , then, is one dimension of classification of host-parasite relationships.
I shall call it the d i m e n s i o n of ' p r o p a g u l e
overlap'. A second dimension of classification concerns the time of action of parasite g e n e s d u r i n g host d e v e l o p m e n t . A g e n e , w h e t h e r a h o s t g e n e o r a p a r a s i t e gene, c a n exert a m o r e f u n d a m e n t a l influence on the final host p h e n o t y p e if i t a c t s e a r l y i n t h e d e v e l o p m e n t o f t h e host e m b r y o t h a n i f i t a c t s l a t e . A radical c h a n g e such as the d e v e l o p m e n t of two heads c o u l d be a c h i e v e d by a s i n g l e m u t a t i o n (in host o r p a r a s i t e g e n o m e ) p r o v i d e d t h e m u t a t i o n a c t e d sufficiently e a r l y i n t h e e m b r y o n i c d e v e l o p m e n t o f t h e h o s t . A l a t e - a c t i n g m u t a n t ( a g a i n , i n host o r p a r a s i t e g e n o m e ) — a m u t a n t t h a t d o e s n o t b e g i n t o a c t u n t i l t h e host b o d y h a s r e a c h e d a d u l t h o o d — i s l i k e l y t o h a v e o n l y a s m a l l effect, s i n c e t h e g e n e r a l a r c h i t e c t u r e o f t h e b o d y w i l l , b y t h e n , h a v e b e e n l a i d d o w n . T h e r e f o r e a p a r a s i t e t h a t e n t e r s its h o s t after t h e h o s t h a s r e a c h e d a d u l t h o o d is less l i k e l y to h a v e a r a d i c a l effect on t h e h o s t ' s p h e n o t y p e t h a n a parasite that gets in early. T h e r e are n o t a b l e e x c e p t i o n s , h o w e v e r , such as the p a r a s i t i c c a s t r a t i o n o f C r u s t a c e a a l r e a d y m e n t i o n e d . M y third d i m e n s i o n o f classification o f h o s t - p a r a s i t e relations c o n c e r n s the c o n t i n u u m from w h a t m a y be c a l l e d close i n t i m a c y to a c t i o n at a d i s t a n c e . A l l g e n e s e x e r t p o w e r p r i m a r i l y b y s e r v i n g a s t e m p l a t e s for t h e s y n t h e s i s o f p r o t e i n s . T h e l o c u s o f p r i m a r y g e n e p o w e r is, t h e r e f o r e , t h e c e l l , i n p a r t i c u l a r the c y t o p l a s m s u r r o u n d i n g t h e n u c l e u s i n w h i c h t h e g e n e sits. M e s s e n g e r R N A streams t h r o u g h the n u c l e a r m e m b r a n e a n d m e d i a t e s g e n e t i c control over cytoplasmic biochemistry. T h e phenotypic expression of a gene is then, i n the f i r s t p l a c e , its i n f l u e n c e o n c y t o p l a s m i c b i o c h e m i s t r y . I n its t u r n , this i n f l u e n c e s t h e f o r m a n d s t r u c t u r e o f t h e w h o l e c e l l , a n d t h e n a t u r e o f its c h e m i c a l a n d p h y s i c a l i n t e r a c t i o n s w i t h n e i g h b o u r i n g c e l l s . T h i s affects t h e b u i l d - u p o f m u l t i c e l l u l a r tissues, a n d i n t u r n t h e d i f f e r e n t i a t i o n o f a v a r i e t y o f tissues i n t h e d e v e l o p i n g b o d y . F i n a l l y e m e r g e t h e a t t r i b u t e s o f t h e w h o l e organism
t h a t gross a n a t o m i s t s a n d
ethologists identify at
their level as
phenotypic expressions of genes. W h e r e p a r a s i t e g e n e s e x e r t s h a r e d p o w e r w i t h host g e n e s o v e r t h e s a m e host p h e n o t y p i c c h a r a c t e r i s t i c , t h e c o n f l u e n c e o f t h e t w o p o w e r s m a y o c c u r
226
Host Phenotypes of Parasite Genes
a t a n y s t a g e i n t h e c h a i n j u s t d e s c r i b e d . S n a i l g e n e s , a n d t h e g e n e s o f the fluke that parasitizes the snail, exert their p o w e r s e p a r a t e l y from e a c h other a t t h e c e l l u l a r a n d e v e n t h e tissue l e v e l . T h e y i n f l u e n c e t h e c y t o p l a s m i c c h e m i s t r y of their r e s p e c t i v e cells separately, b e c a u s e they do not share cells. T h e y i n f l u e n c e tissue f o r m a t i o n s e p a r a t e l y ,
b e c a u s e s n a i l tissues a r e n o t
i n t i m a t e l y i n f i l t r a t e d b y f l u k e tissues i n t h e w a y t h a t , s a y , t h e a l g a l a n d f u n g a l tissues o f a l i c h e n a r e i n t i m a t e . S n a i l g e n e s a n d f l u k e g e n e s i n f l u e n c e the d e v e l o p m e n t of o r g a n systems, indeed of w h o l e organisms, separately, b e c a u s e all the fluke cells are g a t h e r e d t o g e t h e r in one mass rather than being interspersed
a m o n g snail cells.
I f f l u k e g e n e s i n f l u e n c e s n a i l shell
t h i c k n e s s , t h e y d o s o b y first c o l l a b o r a t i n g w i t h o t h e r f l u k e g e n e s t o m a k e a whole fluke. O t h e r p a r a s i t e s a n d s y m b i o n t s m o r e i n t i m a t e l y i n f i l t r a t e t h e s y s t e m s o f the host. A t t h e e x t r e m e a r e t h e p l a s m i d s a n d o t h e r f r a g m e n t s o f D N A w h i c h , a s w e s a w i n C h a p t e r 9 , l i t e r a l l y i n s e r t t h e m s e l v e s i n t h e host c h r o m o s o m e s . I t i s i m p o s s i b l e t o i m a g i n e a m o r e i n t i m a t e p a r a s i t e . ' S e l f i s h D N A ' itself i s n o t more intimate, and indeed we m a y never k n o w h o w m a n y of our genes, w h e t h e r 'junk' or 'useful', originated as inserted plasmids. It seems to follow f r o m t h e thesis o f this b o o k t h a t t h e r e i s n o i m p o r t a n t d i s t i n c t i o n b e t w e e n o u r ' o w n ' genes a n d parasitic or symbiotic insertion sequences. W h e t h e r they c o n f l i c t o r c o o p e r a t e w i l l d e p e n d n o t o n t h e i r h i s t o r i c a l o r i g i n s b u t o n the circumstances from w h i c h they stand to gain now. V i r u s e s h a v e t h e i r o w n p r o t e i n j a c k e t , b u t t h e y i n s e r t t h e i r D N A i n t o the host's cell. T h e y are therefore in a position to influence the cellular chemistry of the host at an intimate level, if not quite such an intimate level as an insertion s e q u e n c e in the host c h r o m o s o m e .
I n t r a c e l l u l a r p a r a s i t e s i n the
c y t o p l a s m , too, m a y be presumed to be in a position to exert considerable p o w e r o v e r host p h e n o t y p e s . S o m e p a r a s i t e s d o n o t i n f i l t r a t e t h e host a t t h e c e l l u l a r l e v e l , b u t a t t h e tissue l e v e l . E x a m p l e s a r e Sacculina, a n d m a n y f u n g a l a n d p l a n t p a r a s i t e s , w h e r e parasite cells and host cells are distinct, but w h e r e the parasite invades t h e h o s t ' s tissues b y m e a n s o f a n i n t r i c a t e a n d finely d i v i d e d r o o t s y s t e m . T h e s e p a r a t e c e l l s o f p a r a s i t i c b a c t e r i a a n d p r o t o z o a m a y i n f i l t r a t e t h e h o s t tissues w i t h s i m i l a r l y c o m p r e h e n s i v e i n t i m a c y . T o a s l i g h t l y lesser e x t e n t t h a n a c e l l p a r a s i t e , s u c h a 'tissue p a r a s i t e ' is in a s t r o n g p o s i t i o n to i n f l u e n c e o r g a n development
and
gross
p h e n o t y p i c form
and
behaviour.
O t h e r internal
p a r a s i t e s , s u c h a s t h e f l u k e s w e h a v e b e e n d i s c u s s i n g , d o n o t m i x t h e i r tissues w i t h t h o s e o f t h e h o s t , b u t k e e p t h e i r tissues t o t h e m s e l v e s a n d e x e r t p o w e r only at the level of the w h o l e organism. B u t w e h a v e not yet r e a c h e d the end o f our c o n t i n u u m o f p r o x i m i t y . N o t a l l p a r a s i t e s l i v e p h y s i c a l l y i n s i d e t h e i r hosts. T h e y m a y e v e n s e l d o m c o m e into c o n t a c t w i t h their hosts. A c u c k o o is a parasite in v e r y m u c h the same w a y a s a f l u k e . B o t h a r e w h o l e - o r g a n i s m p a r a s i t e s r a t h e r t h a n tissue p a r a s i t e s
H o s t P h e n o t y p e s of P a r a s i t e G e n e s
227
o r c e l l p a r a s i t e s . I f fluke g e n e s c a n b e s a i d t o h a v e p h e n o t y p i c e x p r e s s i o n i n a snail's b o d y , there is no sensible reason w h y c u c k o o g e n e s should not be said to h a v e p h e n o t y p i c expression in a reed w a r b l e r ' s b o d y . T h e difference is a practical one, a n d a rather smaller one than the difference b e t w e e n , say, a c e l l u l a r p a r a s i t e a n d a tissue p a r a s i t e . T h e p r a c t i c a l d i f f e r e n c e i s t h a t t h e c u c k o o d o e s n o t l i v e i n s i d e t h e r e e d w a r b l e r ' s b o d y , s o h a s less o p p o r t u n i t y for m a n i p u l a t i n g t h e h o s t ' s i n t e r n a l b i o c h e m i s t r y .
It has to rely on other
m e d i a for its m a n i p u l a t i o n , for i n s t a n c e s o u n d w a v e s a n d l i g h t w a v e s . A s d i s c u s s e d in C h a p t e r 4, it uses a s u p e r n o r m a l l y b r i g h t g a p e to i n j e c t its control into the reed w a r b l e r ' s n e r v o u s system v i a the
eyes.
I t uses a n
especially loud b e g g i n g c r y to control the reed w a r b l e r ' s n e r v o u s system v i a the ears. C u c k o o genes, i n e x e r t i n g their d e v e l o p m e n t a l p o w e r o v e r host phenotypes, h a v e to rely on action at a distance. T h e concept of genetic action at a distance pushes our idea of the extended p h e n o t y p e o u t t o its l o g i c a l c u l m i n a t i o n . T h a t i s w h e r e w e m u s t g o i n t h e next chapter.
13 Action at a Distance
Snail
shells
coil
either
to
the
right
or
to
the
left.
Usually
all
i n d i v i d u a l s i n o n e s p e c i e s c o i l t h e s a m e w a y , b u t a f e w p o l y m o r p h i c species are to be found. In the Pacific island l a n d snail
Partula
suturalis s o m e l o c a l
populations are right-handed, others are left-handed, and others are mixed in various proportions.
It is therefore possible to study the genetics of
d i r e c t i o n a l i t y o f c o i l i n g ( M u r r a y & C l a r k e 1 9 6 6 ) . W h e n snails from r i g h t h a n d e d p o p u l a t i o n s w e r e c r o s s e d w i t h snails f r o m l e f t - h a n d e d p o p u l a t i o n s , e v e r y o f f s p r i n g c o i l e d t h e s a m e w a y a s its ' m o t h e r ' (the p a r e n t t h a t p r o v i d e d the e g g : the snails are h e r m a p h r o d i t e s ) . T h i s m i g h t be thought to indicate a n o n - g e n e t i c m a t e r n a l i n f l u e n c e . B u t w h e n M u r r a y a n d C l a r k e crossed F 1 snails w i t h e a c h o t h e r t h e y o b t a i n e d a c u r i o u s r e s u l t . A l l t h e p r o g e n y w e r e left-handed,
regardless of the direction of c o i l i n g of either parent. T h e i r
i n t e r p r e t a t i o n o f t h e results i s t h a t c o i l i n g i s g e n e t i c a l l y d e t e r m i n e d , w i t h left-handedness phenotype
is
dominant controlled
to not
right-handedness, by
its
own
but
genotype
that but
by
an its
animal's mother's
g e n o t y p e . T h u s the F1 i n d i v i d u a l s d i s p l a y e d the p h e n o t y p e s dictated by their m o t h e r s '
genotypes,
although
all
contained
the same h e t e r o z y g o u s
g e n o t y p e s since t h e y w e r e p r o d u c e d b y m a t i n g t w o p u r e strains. S i m i l a r l y , the F2 p r o g e n y of F1 m a t i n g s all d i s p l a y e d the p h e n o t y p e a p p r o p r i a t e to an F1 g e n o t y p e — l e f t - h a n d e d since that is d o m i n a n t a n d the F1 g e n o t y p e w a s h e t e r o z y g o u s . T h e u n d e r l y i n g g e n o t y p e s o f the F 2 g e n e r a t i o n p r e s u m a b l y s e g r e g a t e d i n c l a s s i c 3 : 1 M e n d e l i a n f a s h i o n , b u t this d i d n o t s h o w itself i n their p h e n o t y p e s .
It w o u l d h a v e s h o w n itself in the p h e n o t y p e s of their
progeny. N o t e that it is the m o t h e r ' s g e n o t y p e , not her p h e n o t y p e , w h i c h controls her offspring's p h e n o t y p e . T h e F1 individuals themselves w e r e left-handed or right-handed
in
equal
proportion,
yet
all
had
the
same
heterozygous
g e n o t y p e , a n d a l l t h e r e f o r e p r o d u c e d l e f t - h a n d e d o f f s p r i n g . A s i m i l a r effect h a d b e e n o b t a i n e d e a r l i e r i n t h e f r e s h w a t e r s n a i l Limnaea peregra, t h o u g h i n t h a t c a s e r i g h t - h a n d e d n e s s w a s d o m i n a n t . O t h e r s u c h ' m a t e r n a l effects' h a v e 228
A c t i o n at a D i s t a n c e
229
l o n g b e e n k n o w n t o g e n e t i c i s t s . A s F o r d ( 1 9 7 5 ) p u t it, ' W e h a v e h e r e s i m p l e M e n d e l i a n inheritance the expression of w h i c h is constantly d e l a y e d one g e n e r a t i o n . ' T h e p h e n o m e n o n p e r h a p s arises w h e n t h e e m b r y o l o g i c a l e v e n t d e t e r m i n i n g t h e p h e n o t y p i c trait o c c u r s s o e a r l y i n d e v e l o p m e n t a s t o b e influenced b y m a t e r n a l messenger R N A from the e g g c y t o p l a s m , before the z y g o t e h a s b e g u n t o m a n u f a c t u r e its o w n m e s s e n g e r R N A . T h e d i r e c t i o n o f coiling in snails is d e t e r m i n e d by the initial d i r e c t i o n of spiral c l e a v a g e , w h i c h occurs before the e m b r y o ' s o w n D N A has b e g u n t o w o r k ( C o h e n 1977)T h i s k i n d o f effect p r o v i d e s a s p e c i a l o p p o r t u n i t y for t h e k i n d o f m a t e r n a l m a n i p u l a t i o n of offspring that we discussed in C h a p t e r 4. M o r e g e n e r a l l y , it is a s p e c i a l e x a m p l e of g e n e t i c ' a c t i o n at a d i s t a n c e ' .
It i l l u s t r a t e s , in a
particularly clear a n d simple m a n n e r , that the p o w e r of a g e n e m a y e x t e n d b e y o n d t h e b o u n d a r i e s o f t h e b o d y i n w h o s e c e l l s i t sits ( H a l d a n e 1 9 3 2 b ) . W e c a n n o t h o p e that all g e n e t i c a c t i o n at a distance w i l l r e v e a l itself in so elegant
a
Mendelian
manner
as
in
the
case
of the
snails. Just
as,
in
c o n v e n t i o n a l genetics, the M e n d e l i a n m a j o r genes of the s c h o o l r o o m are the tip o f t h e i c e b e r g o f r e a l i t y , s o w e m a y m a k e c o n j e c t u r e s a b o u t a p o l y g e n i c ' e x t e n d e d g e n e t i c s ' , a g e n e t i c s in w h i c h a c t i o n at a d i s t a n c e is rife b u t in w h i c h t h e effects o f t h e g e n e s a r e c o m p l e x a n d i n t e r a c t i n g , a n d t h e r e f o r e difficult t o sort o u t . A g a i n a s i n c o n v e n t i o n a l g e n e t i c s , w e d o n o t n e c e s s a r i l y h a v e to do g e n e t i c e x p e r i m e n t s in o r d e r to infer the p r e s e n c e of g e n e t i c influence
on
variation.
Once
we
have
satisfied
c h a r a c t e r i s t i c is a D a r w i n i a n a d a p t a t i o n this,
ourselves
that
a
given
in itself, is t a n t a m o u n t to
satisfying ourselves that v a r i a t i o n in that c h a r a c t e r m u s t at o n e t i m e h a v e had a genetic basis. If it h a d not, selection c o u l d not h a v e preserved the a d v a n t a g e o u s a d a p t a t i o n in the p o p u l a t i o n . O n e p h e n o m e n o n t h a t l o o k s l i k e a n a d a p t a t i o n a n d w h i c h , i n s o m e sense, involves action at a distance, is the ' B r u c e Effect'. A f e m a l e m o u s e w h o has just been inseminated by one m a l e has her p r e g n a n c y b l o c k e d by exposure to c h e m i c a l i n f l u e n c e f r o m a s e c o n d m a l e . T h e effect s e e m s a l s o t o o c c u r i n a variety of species of m i c e a n d voles in nature. S c h w a g m e y e r (1980) considers three m a i n hypotheses of the a d a p t i v e significance of the B r u c e Effect, b u t for t h e s a k e o f a r g u m e n t
I shall not, here, a d v o c a t e the hypothesis that
S c h w a g m e y e r attributes to m e — t h a t the B r u c e Effect represents a k i n d of female a d a p t a t i o n . Instead I shall look at it from the m a l e point of v i e w , a n d simply
assume
that
the
second
male
benefits
himself by
p r e v e n t i n g the
female's p r e g n a n c y , t h e r e b y e l i m i n a t i n g the offspring of a m a l e r i v a l , w h i l e a t t h e s a m e t i m e b r i n g i n g the f e m a l e q u i c k l y i n t o o e s t r u s s o t h a t h e c a n m a t e with her himself. I h a v e expressed the hypothesis in the l a n g u a g e of C h a p t e r 4, the l a n g u a g e of individual m a n i p u l a t i o n . But it c a n e q u a l l y well be expressed in the l a n g u a g e of the e x t e n d e d p h e n o t y p e a n d genetic a c t i o n at a d i s t a n c e . G e n e s
230
A c t i o n at a D i s t a n c e
i n m a l e m i c e h a v e p h e n o t y p i c e x p r e s s i o n i n f e m a l e b o d i e s , i n j u s t the s a m e sense a s g e n e s i n m o t h e r s n a i l s h a v e p h e n o t y p i c e x p r e s s i o n i n t h e b o d i e s o f their c h i l d r e n . In the snail case, the m e d i u m of the action at a distance w a s assumed to be m a t e r n a l messenger R N A . In the mouse case it is apparently a m a l e p h e r o m o n e . M y thesis i s t h a t t h e d i f f e r e n c e b e t w e e n t h e t w o cases i s n o t a fundamental one. Consider how an
'extended geneticist'
m i g h t talk a b o u t
the genetical
e v o l u t i o n of the B r u c e Effect. A m u t a n t g e n e arose w h i c h , w h e n present in the b o d y of a m a l e m o u s e , h a d p h e n o t y p i c expression in the bodies of female m i c e w i t h w h o m h e c a m e i n c o n t a c t . T h e r o u t e o f a c t i o n o f the g e n e o n its final p h e n o t y p e w a s l o n g a n d c o m p l e x , b u t n o t n o t i c e a b l y m o r e s o t h a n routes of genetic action w i t h i n
bodies
customarily are.
In
conventional
w i t h i n - b o d y g e n e t i c s , the c h a i n of c a u s a t i o n l e a d i n g from g e n e to observed p h e n o t y p e m a y h a v e m a n y links. T h e f i r s t link i s a l w a y s R N A , the second i s p r o t e i n . A b i o c h e m i s t m a y d e t e c t t h e p h e n o t y p e t h a t interests h i m a t this second link stage. Physiologists or anatomists w i l l not pick up the p h e n o t y p e that interests
them
until m o r e stages h a v e
been
passed.
T h e y will
not
c o n c e r n t h e m s e l v e s w i t h t h e d e t a i l s o f these e a r l i e r l i n k s i n t h e c h a i n , b u t w i l l t a k e t h e m for g r a n t e d . W h o l e - o r g a n i s m g e n e t i c i s t s f i n d i t sufficient t o d o b r e e d i n g e x p e r i m e n t s l o o k i n g o n l y a t w h a t , for t h e m , i s t h e f i n a l l i n k i n the c h a i n , e y e c o l o u r , c r i n k l i n e s s o f h a i r , o r w h a t e v e r i t is. T h e b e h a v i o u r geneticist looks at an even more distant l i n k — w a l t z i n g in mice, creepingthrough m a n i a in sticklebacks, h y g i e n e in h o n e y b e e s , etc. He arbitrarily chooses to r e g a r d a b e h a v i o u r pattern as the end link in the c h a i n , but he k n o w s that the a b n o r m a l b e h a v i o u r of a m u t a n t is caused by, say, a b n o r m a l n e u r o a n a t o m y , or a b n o r m a l endocrine physiology. He knows that he could h a v e l o o k e d w i t h a m i c r o s c o p e a t t h e n e r v o u s s y s t e m i n o r d e r t o d e t e c t his mutants, but he preferred to look at b e h a v i o u r instead (Brenner 1974). He m a d e a n a r b i t r a r y d e c i s i o n t o r e g a r d o b s e r v e d b e h a v i o u r a s t h e e n d link i n the c h a i n o f c a u s a t i o n . Whichever
link
in
the
chain
a
geneticist
chooses
to
regard
as
the
' p h e n o t y p e ' of interest, he k n o w s that the decision w a s an arbitrary one. He m i g h t h a v e chosen an earlier stage, and he m i g h t h a v e chosen a later one. S o , a student of the g e n e t i c s of the B r u c e Effect c o u l d assay m a l e p h e r o m o n e s b i o c h e m i c a l l y i n o r d e r t o d e t e c t t h e v a r i a t i o n u p o n w h i c h t o b a s e his g e n e t i c study.
Or
he
could
look
further
back
in
the
chain,
ultimately
to
the
i m m e d i a t e p o l y p e p t i d e products o f the genes c o n c e r n e d . O r h e could look later in the c h a i n . W h a t i s t h e n e x t l a t e r l i n k i n t h e c h a i n after t h e m a l e p h e r o m o n e ? I t i s o u t s i d e t h e m a l e b o d y . T h e c h a i n o f c a u s a t i o n e x t e n d s a c r o s s a g a p i n t o the female b o d y . It goes t h r o u g h a n u m b e r of stages in the female b o d y , a n d o n c e a g a i n o u r geneticist does not h a v e to b o t h e r himself w i t h the details. He
A c t i o n at a D i s t a n c e
231
c h o o s e s , for c o n v e n i e n c e , t o e n d his c o n c e p t u a l c h a i n a t t h e p o i n t w h e r e t h e g e n e causes p r e g n a n c y b l o c k a g e in females. T h a t is the p h e n o t y p i c g e n e p r o d u c t w h i c h h e finds m o s t e a s y t o a s s a y , a n d i t i s t h e p h e n o t y p e w h i c h i s o f direct interest to h i m as a student of a d a p t a t i o n in nature.
A b o r t i o n in
f e m a l e m i c e , a c c o r d i n g t o this h y p o t h e s i s , i s a p h e n o t y p i c effect o f a g e n e i n male mice. H o w , then, w o u l d the ' e x t e n d e d geneticist' visualize the e v o l u t i o n o f the Bruce Effect? T h e m u t a n t gene w h i c h ,
w h e n present in males,
has
the
p h e n o t y p i c effect i n f e m a l e b o d i e s o f c a u s i n g t h e m t o a b o r t , i s f a v o u r e d b y n a t u r a l s e l e c t i o n o v e r its a l l e l e s . I t i s f a v o u r e d b e c a u s e i t t e n d s t o b e c a r r i e d i n t h e b o d i e s o f t h e o f f s p r i n g w h i c h t h e f e m a l e b e a r s after b l o c k i n g h e r previous p r e g n a n c y . But, following the h a b i t of C h a p t e r 4, we n o w guess that females w o u l d be u n l i k e l y to s u b m i t to such m a n i p u l a t i o n w i t h o u t resistance, and that a kind of arms r a c e m i g h t d e v e l o p . In the l a n g u a g e of i n d i v i d u a l advantage,
selection
would
favour
mutant
females
that
resisted
the
p h e r o m o n a l m a n i p u l a t i o n o f the males. H o w w o u l d the ' e x t e n d e d geneticist' t h i n k a b o u t this r e s i s t a n c e ? B y i n v o k i n g t h e c o n c e p t o f t h e m o d i f i e r g e n e . O n c e again, we turn first to conventional w i t h i n - b o d y genetics to remind ourselves of a principle, then carry that principle o v e r into the r e a l m of extended genetics. In w i t h i n - b o d y genetics we are quite used to the idea of more than one g e n e affecting variation in a n y g i v e n p h e n o t y p i c character. S o m e t i m e s i t i s c o n v e n i e n t t o d e s i g n a t e o n e l o c u s a s h a v i n g t h e ' m a j o r ' effect o n t h e c h a r a c t e r , t h e o t h e r s h a v i n g ' m o d i f y i n g ' effects. A t o t h e r t i m e s n o o n e locus p r e d o m i n a t e s o v e r the others sufficiently to be c a l l e d major. A l l the g e n e s m a y b e t h o u g h t o f a s m o d i f y i n g t h e effects o f e a c h o t h e r .
In the
chapter o n ' O u t l a w s a n d M o d i f i e r s ' , w e s a w that t w o loci b e a r i n g o n the same phenotypic c h a r a c t e r m a y be subject to conflicting selection pressures. T h e e n d result m a y b e s t a l e m a t e , c o m p r o m i s e , o r o u t r i g h t v i c t o r y for o n e side o r t h e o t h e r . T h e p o i n t i s t h a t c o n v e n t i o n a l w i t h i n - b o d y g e n e t i c s i s already a c c u s t o m e d to t h i n k i n g of the n a t u r a l selection of genes at different loci b e a r i n g u p o n t h e s a m e p h e n o t y p i c c h a r a c t e r b u t i n o p p o s i t e d i r e c t i o n s . A p p l y t h e lesson i n t h e e x t e n d e d g e n e t i c s d o m a i n . T h e p h e n o t y p i c t r a i t o f interest i s a b o r t i o n i n f e m a l e m i c e . T h e g e n e s b e a r i n g u p o n i t n o d o u b t i n c l u d e a set o f g e n e s i n t h e f e m a l e ' s o w n b o d y , a n d a l s o a n o t h e r set o f g e n e s i n the m a l e ' s b o d y . I n t h e c a s e o f t h e m a l e g e n e s t h e l i n k s i n t h e c h a i n o f c a u s a t i o n i n c l u d e p h e r o m o n a l a c t i o n a t a d i s t a n c e , a n d this m a y m a k e t h e influence of the m a l e genes seem v e r y indirect. B u t the causal links in the c a s e o f the f e m a l e g e n e s a r e l i k e l y t o b e n e a r l y a s i n d i r e c t , a l b e i t t h e y a r e confined
inside
her body.
P r o b a b l y t h e y m a k e use
of various chemical
secretions flowing in her b l o o d s t r e a m , w h e r e a s the m a l e g e n e s m a k e use, in a d d i t i o n , o f c h e m i c a l s e c r e t i o n s f l o w i n g i n t h e a i r . T h e p o i n t i s t h a t b o t h sets of genes, by l o n g a n d indirect causal links, b e a r u p o n the s a m e p h e n o t y p i c
232
A c t i o n at a D i s t a n c e
c h a r a c t e r , a b o r t i o n i n t h e f e m a l e , a n d e i t h e r set o f g e n e s m a y b e r e g a r d e d a s m o d i f i e r s o f t h e o t h e r set, j u s t a s s o m e g e n e s w i t h i n e a c h set m a y b e r e g a r d e d a s m o d i f i e r s o f o t h e r s w i t h i n t h e s a m e set. M a l e genes influence the female p h e n o t y p e . F e m a l e genes influence the female p h e n o t y p e , a n d also modify the influence o f m a l e genes. F o r all w e k n o w , female genes influence the m a l e p h e n o t y p e in counter-manipulation, in w h i c h case we e x p e c t the selection of modifiers a m o n g genes in males. T h i s w h o l e s t o r y c o u l d h a v e b e e n t o l d i n t h e l a n g u a g e o f C h a p t e r 4 , the l a n g u a g e of individual manipulation. T h e l a n g u a g e of extended genetics is not d e m o n s t r a b l y m o r e c o r r e c t . It is a different w a y of s a y i n g the same thing. T h e N e c k e r C u b e h a s f l i p p e d . R e a d e r s m u s t d e c i d e for t h e m s e l v e s w h e t h e r they like the n e w v i e w better than the old.
I suggest that the w a y the
e x t e n d e d g e n e t i c i s t tells t h e s t o r y o f t h e B r u c e Effect i s m o r e e l e g a n t a n d p a r s i m o n i o u s t h a n t h e w a y t h e c o n v e n t i o n a l g e n e t i c i s t w o u l d h a v e told it. Both geneticists potentially h a v e to contend with a formidably long and c o m p l e x c h a i n of causation, l e a d i n g from g e n e to p h e n o t y p e . B o t h admit that their c h o i c e of w h i c h link in the c h a i n to d e s i g n a t e as the p h e n o t y p i c c h a r a c t e r of interest—earlier links b e i n g consigned to the e m b r y o l o g i s t — i s arbitrary. T h e c o n v e n t i o n a l geneticist m a k e s the further arbitrary decision to cut off all c h a i n s at the p o i n t w h e r e they r e a c h the outer w a l l of the b o d y . G e n e s affect p r o t e i n s , a n d p r o t e i n s affect X w h i c h affects Y w h i c h affects Z w h i c h . . . affects t h e p h e n o t y p i c c h a r a c t e r o f i n t e r e s t . B u t t h e c o n v e n t i o n a l g e n e t i c i s t d e f i n e s ' p h e n o t y p i c effect' i n s u c h a w a y t h a t X , Y a n d Z m u s t all be
confined
inside
one
individual
body
wall.
The
extended
geneticist
r e c o g n i z e s t h a t this c u t - o f f i s a r b i t r a r y , a n d h e i s q u i t e h a p p y t o a l l o w his X , Y a n d Z to leap the g a p b e t w e e n one individual b o d y and another. T h e c o n v e n t i o n a l g e n e t i c i s t t a k e s i n his s t r i d e t h e b r i d g i n g o f g a p s b e t w e e n cells w i t h i n b o d i e s . H u m a n r e d b l o o d c e l l s , for i n s t a n c e , h a v e n o n u c l e i , a n d m u s t express the p h e n o t y p e s of genes in other cells. So w h y should we not, w h e n t h e o c c a s i o n w a r r a n t s it, c o n c e i v e o f t h e b r i d g i n g o f g a p s b e t w e e n cells i n d i f f e r e n t b o d i e s ? A n d w h e n w i l l t h e o c c a s i o n w a r r a n t i t ? W h e n e v e r w e find i t c o n v e n i e n t , a n d this w i l l t e n d t o b e i n a n y o f t h o s e c a s e s w h e r e , i n conventional l a n g u a g e , one organism appears to be manipulating another. T h e e x t e n d e d geneticist w o u l d , i n fact, b e quite h a p p y t o rewrite the w h o l e o f C h a p t e r 4 , f i x i n g his g a z e o n t h e n e w f a c e o f t h e N e c k e r C u b e . I s h a l l s p a r e t h e r e a d e r a n y s u c h r e w r i t i n g , a l t h o u g h i t w o u l d b e a n i n t e r e s t i n g task to u n d e r t a k e . I shall not pile e x a m p l e on e x a m p l e of genetic action at a d i s t a n c e , b u t i n s t e a d w i l l d i s c u s s t h e c o n c e p t , a n d p r o b l e m s t h a t i t raises, more generally. In the c h a p t e r on a r m s races a n d m a n i p u l a t i o n I said that an o r g a n i s m ' s l i m b s m i g h t b e a d a p t e d t o w o r k for t h e g e n e s o f a n o t h e r o r g a n i s m , a n d I a d d e d t h a t this i d e a c o u l d n o t b e m a d e f u l l y m e a n i n g f u l u n t i l l a t e r i n the book. I m e a n t that it could be m a d e meaningful in terms of genetic action at
A c t i o n at a D i s t a n c e
233
a d i s t a n c e . S o , w h a t d o e s it m e a n to s a y t h a t a f e m a l e ' s m u s c l e s w o r k for a m a l e ' s g e n e s , or t h a t a p a r e n t ' s l i m b s w o r k for its o f f s p r i n g ' s g e n e s , or t h a t a reed w a r b l e r ' s l i m b s w o r k for a c u c k o o ' s g e n e s ? I t w i l l b e r e m e m b e r e d t h a t the
'central
theorem'
of the
selfish
organism
claims
that
an
animal's
b e h a v i o u r t e n d s t o m a x i m i z e its o w n ( i n c l u s i v e ) fitness. W e s a w t h a t t o t a l k o f a n i n d i v i d u a l b e h a v i n g s o a s t o m a x i m i z e its i n c l u s i v e fitness i s e q u i v a l e n t to talking of the g e n e or genes 'for' that b e h a v i o u r p a t t e r n m a x i m i z i n g their s u r v i v a l . W e h a v e n o w a l s o s e e n t h a t , i n p r e c i s e l y t h e s a m e sense a s i t i s e v e r p o s s i b l e to t a l k of a g e n e ' f o r ' a b e h a v i o u r p a t t e r n , it is p o s s i b l e to t a l k of a
gene,
in
one
organism,
'for'
a
behaviour
pattern
(or
other
pheno-
typic characteristic) in a n o t h e r o r g a n i s m . P u t t i n g these three things together we
arrive
An
animal's
at
our
own
behaviour
'central
tends
to
theorem'
maximize
the
of
the
survival
extended of the
phenotype:
genes
'for'
that
behaviour, whether or not those genes happen to be in the body of the particular animal performing
it.
A n d h o w far afield c a n t h e p h e n o t y p e e x t e n d ? I s t h e r e a n y l i m i t t o a c t i o n a t a d i s t a n c e , a s h a r p cut-off, a n i n v e r s e s q u a r e l a w ? T h e f a r t h e s t a c t i o n a t a distance I c a n think of is a m a t t e r of several miles, the distance s e p a r a t i n g the e x t r e m e m a r g i n s o f a b e a v e r l a k e f r o m t h e g e n e s for w h o s e s u r v i v a l i t i s a n a d a p t a t i o n . I f b e a v e r l a k e s c o u l d fossilize, w e w o u l d p r e s u m a b l y see a t r e n d t o w a r d s i n c r e a s e d l a k e s i z e i f w e a r r a n g e d t h e fossils i n c h r o n o l o g i c a l order. T h e increase i n size w a s doubtless a n a d a p t a t i o n p r o d u c e d b y n a t u r a l s e l e c t i o n , i n w h i c h c a s e w e h a v e t o infer t h a t t h e e v o l u t i o n a r y t r e n d c a m e about by allele r e p l a c e m e n t . In the terms of the e x t e n d e d p h e n o t y p e , alleles for l a r g e r l a k e s r e p l a c e d a l l e l e s for s m a l l e r l a k e s . I n t h e s a m e t e r m s , b e a v e r s c a n b e said t o c a r r y w i t h i n t h e m s e l v e s g e n e s w h o s e p h e n o t y p i c e x p r e s s i o n extends m a n y miles a w a y from the genes themselves. W h y not hundreds of miles, thousands of miles? C o u l d an ectoparasite w h i c h stayed b e h i n d in E n g l a n d inject a s w a l l o w w i t h a d r u g w h i c h affected t h a t s w a l l o w ' s b e h a v i o u r o n its a r r i v a l i n A f r i c a , a n d c o u l d t h e c o n s e q u e n c e i n A f r i c a b e u s e f u l l y r e g a r d e d a s the p h e n o t y p i c e x p r e s s i o n o f p a r a s i t e g e n e s in E n g l a n d ? T h e logic of the e x t e n d e d p h e n o t y p e m i g h t s e e m to f a v o u r the idea, but I think in p r a c t i c e it is unlikely, at least if we are t a l k i n g a b o u t p h e n o t y p i c e x p r e s s i o n as adaptation. I see a c r u c i a l p r a c t i c a l d i f f e r e n c e f r o m the c a s e o f the b e a v e r d a m . A g e n e i n a b e a v e r w h i c h , w h e n c o m p a r e d w i t h its a l l e l e s , c a u s e s a l a r g e r l a k e t o c o m e i n t o e x i s t e n c e , c a n d i r e c t l y b e n e f i t itself b y m e a n s o f its l a k e . A l l e l e s c a u s i n g s m a l l e r l a k e s a r e less l i k e l y t o s u r v i v e , a s a d i r e c t c o n s e q u e n c e o f t h e i r s m a l l e r p h e n o t y p e s . I t is, h o w e v e r , h a r d t o see h o w a g e n e i n a n E n g l i s h e c t o p a r a s i t e c o u l d b e n e f i t itself, a t t h e e x p e n s e o f its a l l e l e s i n E n g l a n d , a s a d i r e c t r e s u l t o f its A f r i c a n p h e n o t y p i c e x p r e s s i o n . A f r i c a i s p r o b a b l y t o o far a w a y for t h e c o n s e q u e n c e s o f t h e g e n e ' s a c t i o n t o feed b a c k a n d affect t h e w e l f a r e o f t h e g e n e itself. By the s a m e token, b e y o n d a certain size of b e a v e r lakes, it w o u l d b e c o m e
234
A c t i o n at a D i s t a n c e
h a r d to r e g a r d further increases in size as a d a p t a t i o n s . T h e reason is that, b e y o n d a c e r t a i n s i z e , o t h e r b e a v e r s t h a n the b u i l d e r s o f t h e d a m a r e j u s t a s likely to benefit from e a c h increase in size as the d a m - b u i l d e r s themselves. A b i g lake benefits all the beavers in the area, w h e t h e r they created it or w h e t h e r t h e y j u s t f o u n d i t a n d e x p l o i t e d it. S i m i l a r l y , e v e n i f a g e n e i n a n E n g l i s h a n i m a l c o u l d e x e r t s o m e p h e n o t y p i c effect o n A f r i c a w h i c h d i r e c t l y benefited the survival of the gene's ' o w n ' a n i m a l , other English animals of the s a m e kind w o u l d almost certainly benefit just as m u c h . We must not f o r g e t t h a t n a t u r a l s e l e c t i o n i s a l l a b o u t relative s u c c e s s . It is a d m i t t e d l y p o s s i b l e
to s p e a k of
a g e n e as h a v i n g a p a r t i c u l a r
p h e n o t y p i c e x p r e s s i o n , e v e n w h e n its o w n s u r v i v a l i s n o t i n f l u e n c e d b y t h a t p h e n o t y p i c e x p r e s s i o n . I n this sense, t h e n , a g e n e i n E n g l a n d m i g h t i n d e e d h a v e p h e n o t y p i c e x p r e s s i o n i n a r e m o t e c o n t i n e n t w h e r e its c o n s e q u e n c e s d o n o t f e e d b a c k u p o n its o w n s u c c e s s i n t h e E n g l i s h g e n e - p o o l . B u t I h a v e a l r e a d y a r g u e d t h a t i n t h e w o r l d o f t h e e x t e n d e d p h e n o t y p e this i s n o t a profitable w a y of speaking.
I
used the e x a m p l e of footprints in m u d as
p h e n o t y p i c e x p r e s s i o n o f g e n e s for foot s h a p e , a n d I g a v e m y i n t e n t i o n o f using extended
p h e n o t y p e l a n g u a g e only w h e n the character concerned
m i g h t c o n c e i v a b l y i n f l u e n c e , p o s i t i v e l y o r n e g a t i v e l y , t h e r e p l i c a t i o n success of the g e n e or genes c o n c e r n e d . It is n o t p l a u s i b l e , b u t it h e l p s to m a k e t h e p o i n t if I c o n s t r u c t a t h o u g h t e x p e r i m e n t i n w h i c h i t w o u l d i n d e e d b e useful t o s p e a k o f a g e n e a s h a v i n g p h e n o t y p i c expression e x t e n d i n g to another continent. S w a l l o w s return, each year,
to e x a c t l y the s a m e nest.
It follows that an ectoparasite, waiting
d o r m a n t i n a s w a l l o w ' s nest i n E n g l a n d , c a n e x p e c t t o see t h e v e r y s a m e s w a l l o w b o t h b e f o r e a n d after t h e s w a l l o w ' s j o u r n e y t o A f r i c a . I f t h e p a r a s i t e c o u l d engineer some c h a n g e in the s w a l l o w ' s b e h a v i o u r in Africa, it might indeed r e a p the c o n s e q u e n c e s on the s w a l l o w ' s return to E n g l a n d . Suppose, for i n s t a n c e , t h a t t h e p a r a s i t e n e e d s a r a r e t r a c e e l e m e n t w h i c h i s n o t f o u n d i n E n g l a n d , b u t w h i c h o c c u r s i n t h e fat o f a p a r t i c u l a r A f r i c a n fly. S w a l l o w s n o r m a l l y h a v e n o p r e f e r e n c e for this f l y , b u t t h e p a r a s i t e , b y i n j e c t i n g a d r u g i n t o t h e s w a l l o w b e f o r e i t l e a v e s for A f r i c a , s o c h a n g e s its d i e t a r y p r e f e r e n c e s a s t o i n c r e a s e t h e l i k e l i h o o d o f its e a t i n g s p e c i m e n s o f this f l y . W h e n the s w a l l o w r e t u r n s t o E n g l a n d , its b o d y c o n t a i n s e n o u g h o f t h e t r a c e e l e m e n t t o b e n e f i t t h e i n d i v i d u a l p a r a s i t e (or its c h i l d r e n ) w a i t i n g i n t h e o r i g i n a l nest, benefit t h e m at the e x p e n s e of rivals w i t h i n the parasite species. O n l y in c i r c u m s t a n c e s such as these w o u l d I wish to speak of a g e n e in one continent as h a v i n g phenotypic expression in another continent. T h e r e i s a risk, w h i c h I h a d b e t t e r f o r e s t a l l , t h a t s u c h t a l k o f a d a p t a t i o n o n a g l o b a l s c a l e m a y c a l l t o t h e r e a d e r ' s m i n d t h e f a s h i o n a b l e i m a g e o f the e c o l o g i c a l ' w e b ' , of w h i c h the most e x t r e m e manifestation is the ' G a i a ' hypothesis of L o v e l o c k (1979). My w e b of interlocking extended phenotypic i n f l u e n c e s b e a r s a superficial r e s e m b l a n c e t o the w e b s o f m u t u a l d e p e n d e n c e
A c t i o n at a D i s t a n c e
235
and symbiosis that bulk so largely in the p o p - e c o l o g y literature (e.g.
The
Ecologist) a n d i n L o v e l o c k ' s b o o k . T h e c o m p a r i s o n c o u l d h a r d l y b e m o r e misleading.
Since Lovelock's G a i a
hypothesis
has
been
enthusiastically
e s p o u s e d b y n o less a scientist t h e n M a r g u l i s ( 1 9 8 1 ) , a n d e x t r a v a g a n t l y praised by M e l l a n b y (1979) as the w o r k of a genius, it c a n n o t be i g n o r e d , and I must digress in order c a t e g o r i c a l l y to d i s c l a i m a n y c o n n e c t i o n w i t h the extended phenotype. Lovelock
rightly
regards
homeostatic
self-regulation
as
one
of
the
c h a r a c t e r i s t i c a c t i v i t i e s o f l i v i n g o r g a n i s m s , a n d this l e a d s h i m t o t h e d a r i n g hypothesis that the w h o l e E a r t h is e q u i v a l e n t to a single l i v i n g o r g a n i s m . W h e r e a s T h o m a s ' s ( 1 9 7 4 ) l i k e n i n g of the w o r l d to a l i v i n g cell c a n be accepted
as
a
throwaway
poetic
line,
Lovelock
clearly
takes
his
E a r t h / o r g a n i s m c o m p a r i s o n s e r i o u s l y e n o u g h t o d e v o t e a w h o l e b o o k t o it. H e r e a l l y m e a n s it. H i s e x p l a n a t i o n s o f t h e n a t u r e o f t h e a t m o s p h e r e a r e r e p r e s e n t a t i v e o f his i d e a s . T h e E a r t h h a s m u c h m o r e o x y g e n t h a n i s t y p i c a l of c o m p a r a b l e planets. It has l o n g been w i d e l y suggested that g r e e n plants are p r o b a b l y a l m o s t e n t i r e l y r e s p o n s i b l e for this h i g h o x y g e n c o n t e n t . M o s t people would regard o x y g e n production as a byproduct of plant activity, and a f o r t u n a t e o n e for t h o s e o f u s w h o n e e d t o b r e a t h e o x y g e n ( p r e s u m a b l y , t o o , we have been selected to breathe o x y g e n partly because there is so m u c h of it a b o u t ) . L o v e l o c k goes further, a n d regards o x y g e n p r o d u c t i o n by plants as a n a d a p t a t i o n o n t h e p a r t o f t h e E a r t h / o r g a n i s m o r ' G a i a ' ( n a m e d after t h e G r e e k E a r t h g o d d e s s ) : p l a n t s p r o d u c e o x y g e n because i t b e n e f i t s life a s a whole. H e uses the s a m e k i n d o f a r g u m e n t for o t h e r g a s e s t h a t o c c u r i n s m a l l amounts: W h a t , then, is the purpose of m e t h a n e a n d h o w does it relate to o x y g e n ? O n e obvious function is to m a i n t a i n the integrity of the a n a e r o b i c z o n e s o f its o r i g i n [ p . 7 3 ] . A n o t h e r p u z z l i n g atmospheric gas is nitrous o x i d e . .. We m a y be sure that
the
efficient
biosphere
is
unlikely
to
squander
the
energy
r e q u i r e d i n m a k i n g this o d d g a s u n l e s s i t h a s s o m e useful f u n c t i o n . T w o p o s s i b l e uses c o m e t o m i n d . . . [ p . 7 4 ] . A n o t h e r n i t r o g e n o u s g a s m a d e i n l a r g e v o l u m e s i n t h e soil a n d t h e s e a and released to the air is a m m o n i a . . . As w i t h m e t h a n e , the b i o s p h e r e uses a g r e a t d e a l o f e n e r g y i n p r o d u c i n g a m m o n i a , w h i c h i s n o w e n t i r e l y o f b i o l o g i c a l o r i g i n . Its f u n c t i o n i s a l m o s t c e r t a i n l y t o c o n t r o l the acidity o f the e n v i r o n m e n t . . . [p. 7 7 ] . T h e fatal f l a w i n L o v e l o c k ' s h y p o t h e s i s w o u l d h a v e i n s t a n t l y o c c u r r e d t o h i m i f h e h a d w o n d e r e d a b o u t the l e v e l o f n a t u r a l s e l e c t i o n p r o c e s s w h i c h
A c t i o n at a D i s t a n c e
236
w o u l d be r e q u i r e d in order to p r o d u c e the E a r t h ' s supposed adaptations. Homeostatic adaptations in individual bodies evolve because individuals w i t h i m p r o v e d h o m e o s t a t i c a p p a r a t u s pass o n t h e i r g e n e s m o r e e f f e c t i v e l y than i n d i v i d u a l s w i t h inferior homeostatic apparatuses. F o r the a n a l o g y to a p p l y s t r i c t l y , t h e r e w o u l d h a v e t o h a v e b e e n a set o f r i v a l G a i a s , p r e s u m a b l y o n d i f f e r e n t p l a n e t s . B i o s p h e r e s w h i c h d i d n o t d e v e l o p efficient h o m e o s t a t i c regulation of their p l a n e t a r y atmospheres tended to go extinct. T h e Universe w o u l d h a v e t o b e full o f d e a d p l a n e t s w h o s e h o m e o s t a t i c r e g u l a t i o n s y s t e m s had
failed,
with,
dotted
around,
a
handful of successful,
well-regulated
p l a n e t s o f w h i c h E a r t h i s o n e . E v e n this i m p r o b a b l e s c e n a r i o i s n o t sufficient to lead
to the
e v o l u t i o n of p l a n e t a r y a d a p t a t i o n s of the kind L o v e l o c k
proposes. In addition we w o u l d h a v e to postulate some kind of reproduction, w h e r e b y s u c c e s s f u l p l a n e t s s p a w n e d c o p i e s o f t h e i r life f o r m s o n n e w p l a n e t s . I a m n o t , o f c o u r s e , s u g g e s t i n g t h a t L o v e l o c k b e l i e v e s i t h a p p e n e d like that.
He
would
surely
consider
the
idea
of interplanetary
selection
as
l u d i c r o u s a s I d o . O b v i o u s l y h e s i m p l y d i d n o t see his h y p o t h e s i s a s e n t a i l i n g the h i d d e n assumptions that I think it entails. He m i g h t dispute that it does entail those assumptions, a n d m a i n t a i n that G a i a could e v o l v e her global a d a p t a t i o n s b y the o r d i n a r y processes o f D a r w i n i a n selection a c t i n g within the o n e p l a n e t . I v e r y m u c h d o u b t that a m o d e l of s u c h a selection process c o u l d b e m a d e t o w o r k : i t w o u l d h a v e a l l t h e n o t o r i o u s difficulties o f ' g r o u p s e l e c t i o n ' . F o r i n s t a n c e , i f p l a n t s a r e s u p p o s e d t o m a k e o x y g e n for t h e g o o d o f t h e b i o s p h e r e , i m a g i n e a m u t a n t p l a n t w h i c h s a v e d i t s e l f the costs o f o x y g e n manufacture.
Obviously
it
would
outreproduce
its
more
public-spirited
c o l l e a g u e s , a n d g e n e s for p u b l i c - s p i r i t e d n e s s w o u l d s o o n d i s a p p e a r . I t i s n o use p r o t e s t i n g t h a t o x y g e n m a n u f a c t u r e n e e d n o t h a v e c o s t s : i f i t d i d n o t h a v e costs,
the most p a r s i m o n i o u s e x p l a n a t i o n of o x y g e n production in plants
w o u l d be the o n e the scientific w o r l d accepts a n y w a y , that o x y g e n is a b y p r o d u c t o f s o m e t h i n g t h e p l a n t s d o for t h e i r o w n selfish g o o d . I d o not d e n y that s o m e b o d y m a y , one d a y , p r o d u c e a w o r k a b l e m o d e l of the evolution of G a i a ( p o s s i b l y a l o n g t h e lines o f ' M o d e l 2 ' b e l o w ) , a l t h o u g h I p e r s o n a l l y d o u b t it. B u t i f L o v e l o c k h a s s u c h a m o d e l i n m i n d h e d o e s n o t m e n t i o n it. I n d e e d , h e g i v e s n o i n d i c a t i o n t h a t t h e r e i s a difficult p r o b l e m h e r e . T h e G a i a h y p o t h e s i s i s a n e x t r e m e f o r m o f w h a t , for o l d t i m e s ' s a k e a l t h o u g h it is n o w rather unfair, I shall c o n t i n u e to call the ' B B C T h e o r e m ' . T h e B r i t i s h B r o a d c a s t i n g C o r p o r a t i o n i s r i g h t l y p r a i s e d for t h e e x c e l l e n c e o f its n a t u r e p h o t o g r a p h y , a n d i t u s u a l l y s t r i n g s t h e s e a d m i r a b l e v i s u a l i m a g e s t o g e t h e r w i t h a s e r i o u s c o m m e n t a r y . T h i n g s a r e c h a n g i n g n o w , b u t for y e a r s the d o m i n a n t message of these c o m m e n t a r i e s w a s o n e that h a d been elevated almost to the status of a religion by p o p ' e c o l o g y ' . T h e r e w a s something called the ' b a l a n c e of n a t u r e ' , an exquisitely fashioned m a c h i n e in w h i c h plants, h e r b i v o r e s , c a r n i v o r e s , parasites, and s c a v e n g e r s e a c h p l a y e d their a p p o i n t e d r o l e for t h e g o o d o f a l l . T h e o n l y t h i n g t h a t t h r e a t e n e d this d e l i c a t e
A c t i o n at a D i s t a n c e
ecological
china
shop
was
the
insensitive
bull
of h u m a n
progress,
237
the
bulldozer o f . . . , etc. T h e w o r l d needs the patient, toiling d u n g beetles a n d o t h e r s c a v e n g e r s , b u t for w h o s e selfless efforts a s t h e s a n i t a r y w o r k e r s o f t h e world . . . ,
etc.
Herbivores
need
their
predators,
but
for
whom
their
populations w o u l d soar out of control and threaten t h e m with extinction, just a s m a n ' s p o p u l a t i o n will unless . . . , etc. T h e B B C T h e o r e m i s often expressed i n t e r m s o f t h e p o e t r y o f w e b s a n d n e t w o r k s . T h e w h o l e w o r l d i s a finemeshed network of interrelationships, a w e b of connections w h i c h it has taken thousands of years to build up, and w o e betide m a n k i n d if we tear it d o w n . . . , etc. T h e r e is, n o d o u b t , m u c h m e r i t i n t h e m o r a l i s t i c e x h o r t a t i o n s t h a t s e e m t o f l o w f r o m t h e B B C T h e o r e m , b u t t h a t d o e s n o t m e a n its t h e o r e t i c a l b a s i s i s s o u n d . Its w e a k n e s s i s t h e o n e I h a v e a l r e a d y e x p o s e d i n t h e G a i a h y p o t h e s i s . A n e t w o r k o f r e l a t i o n s h i p s t h e r e m a y b e , b u t i t i s m a d e u p o f s m a l l , selfinterested c o m p o n e n t s .
E n t i t i e s t h a t p a y t h e costs o f f u r t h e r i n g t h e w e l l -
b e i n g o f the e c o s y s t e m a s a w h o l e w i l l t e n d t o r e p r o d u c e t h e m s e l v e s less successfully than contribute
rivals
nothing
to
that exploit their public-spirited the
general
welfare.
Hardin
colleagues,
(1968)
summed
and the
p r o b l e m u p i n his m e m o r a b l e p h r a s e ' T h e t r a g e d y o f t h e c o m m o n s ' , a n d m o r e r e c e n t l y ( H a r d i n 1 9 7 8 ) i n t h e a p h o r i s m , ' N i c e g u y s finish l a s t ' . I h a v e dealt w i t h the B B C T h e o r e m a n d the G a i a h y p o t h e s i s , b e c a u s e o f the d a n g e r t h a t m y o w n l a n g u a g e o f t h e e x t e n d e d p h e n o t y p e a n d a c t i o n a t a distance m a y sound like some o f the m o r e e x u b e r a n t l y e x t e n d e d n e t w o r k s a n d w e b s o f the T V ' e c o l o g i s t s ' . T o e m p h a s i z e t h e d i f f e r e n c e , t h e n , let m e b o r r o w t h e r h e t o r i c o f w e b s a n d n e t w o r k s , b u t use i t i n a v e r y d i f f e r e n t w a y , to explain the i d e a of the e x t e n d e d p h e n o t y p e a n d of g e n e t i c a c t i o n at a distance. L o c i in germ-line c h r o m o s o m e s are hotly contested pieces of p r o p e r t y . T h e contestants are a l l e l o m o r p h i c replicators. M o s t of the replicators in the w o r l d h a v e w o n their p l a c e i n i t b y d e f e a t i n g all a v a i l a b l e a l t e r n a t i v e alleles. T h e w e a p o n s w i t h w h i c h t h e y w o n , a n d t h e w e a p o n s w i t h w h i c h t h e i r r i v a l s lost, are
their
respective
phenotypic
consequences.
These
phenotypic
con-
s e q u e n c e s a r e c o n v e n t i o n a l l y t h o u g h t o f a s b e i n g r e s t r i c t e d t o a s m a l l field a r o u n d the r e p l i c a t o r itself, its b o u n d a r i e s b e i n g d e f i n e d b y t h e b o d y w a l l o f the i n d i v i d u a l o r g a n i s m i n w h o s e c e l l s t h e r e p l i c a t o r sits. B u t t h e n a t u r e o f the c a u s a l i n f l u e n c e o f g e n e o n p h e n o t y p e i s s u c h t h a t i t m a k e s n o s e n s e t o t h i n k o f the field o f i n f l u e n c e a s b e i n g l i m i t e d i n this a r b i t r a r y w a y , a n y m o r e t h a n i t m a k e s sense t o t h i n k o f i t a s l i m i t e d t o i n t r a c e l l u l a r b i o c h e m i s t r y . W e m u s t t h i n k o f e a c h r e p l i c a t o r a s t h e c e n t r e o f a field o f i n f l u e n c e o n t h e w o r l d a t l a r g e . C a u s a l i n f l u e n c e r a d i a t e s o u t f r o m t h e r e p l i c a t o r , b u t its p o w e r d o e s not d e c a y w i t h d i s t a n c e a c c o r d i n g t o a n y s i m p l e m a t h e m a t i c a l l a w . I t t r a v e l s w h e r e v e r i t c a n , far o r n e a r , a l o n g a v a i l a b l e a v e n u e s , a v e n u e s o f i n t r a c e l l u l a r biochemistry, of intercellular chemical and
physical interaction,
o f gross
238
A c t i o n at a D i s t a n c e
bodily form and physiology. T h r o u g h a variety Of physical and chemical m e d i a i t r a d i a t e s o u t b e y o n d the i n d i v i d u a l b o d y t o t o u c h o b j e c t s i n the w o r l d outside, i n a n i m a t e artefacts and even other living organisms. J u s t a s e v e r y g e n e i s t h e c e n t r e o f a r a d i a t i n g field o f i n f l u e n c e o n the w o r l d , so e v e r y p h e n o t y p i c c h a r a c t e r is the centre of c o n v e r g i n g influences from
many
genes,
both
within
and
outside
the
body
o f the
individual
o r g a n i s m . T h e w h o l e b i o s p h e r e — r e c o g n i z e t h e s u p e r f i c i a l affinity w i t h the B B C T h e o r e m — t h e w h o l e w o r l d o f p l a n t a n d a n i m a l m a t t e r i s criss-crossed w i t h a n i n t r i c a t e n e t w o r k o f fields o f g e n e t i c i n f l u e n c e , a w e b o f p h e n o t y p i c p o w e r . I c a n a l m o s t h e a r the t e l e v i s i o n c o m m e n t a r y : ' I m a g i n e b e i n g s h r u n k to the size of a
mitochondrion stationed
at a c o n v e n i e n t v a n t a g e point
outside the n u c l e a r m e m b r a n e of a h u m a n z y g o t e . W a t c h the molecules of messenger R N A a s they stream, b y the millions, out into the c y t o p l a s m o n t h e i r e r r a n d s o f p h e n o t y p i c p o w e r - p l a y . N o w g r o w t o t h e s i z e o f a c e l l i n the d e v e l o p i n g l i m b - b u d of a c h i c k e m b r y o . F e e l the wafts of c h e m i c a l inducers as they roll d o w n the gentle slopes of their axial g r a d i e n t s ! N o w g r o w again t o y o u r full s i z e , a n d s t a n d i n the m i d d l e o f a w o o d , a t d a w n i n s p r i n g . B i r d s o n g s u r g e s r o u n d y o u . M a l e s y r i n x e s p o u r o u t s o u n d , a n d a l l r o u n d the w o o d f e m a l e ovaries s w e l l . H e r e the influence travels in the form of pressure w a v e s i n t h e o p e n a i r , r a t h e r t h a n m o l e c u l e s i n c y t o p l a s m , b u t the p r i n c i p l e is the s a m e . At all three levels of the L i l l i p u t i a n / B r o b d i n g n a g i a n t h o u g h t experiment,
you
are
privileged
to
stand
in
the
midst
of uncountable
i n t e r l o c k i n g fields o f r e p l i c a t o r p o w e r . ' T h e r e a d e r w i l l g a t h e r t h a t i t w a s t h e message o f t h e B B C T h e o r e m t h a t I w a n t e d t o c r i t i c i z e , n o t its r h e t o r i c ! N e v e r t h e l e s s , a m o r e r e s t r a i n e d b r a n d o f eloquence
is
often
more
effective.
A
master of restrained
eloquence
in
b i o l o g i c a l w r i t i n g i s Ernst M a y r . H i s c h a p t e r o n ' T h e u n i t y o f the g e n o t y p e ' ( M a y r 1963) is often h e l d up to me in c o n v e r s a t i o n as d e e p l y antithetical to my
replicator-based
enthusiastically
viewpoint.
endorsing
almost
Since, every
on
the
word
contrary,
of that
I
find
chapter,
myself
something
must have been misunderstood, somewhere. M u c h the s a m e c o u l d b e said o f W r i g h t ' s (1980) e q u a l l y e l o q u e n t article on ' G e n i c and organismic selection', w h i c h purports to be a repudiation of t h e g e n i c s e l e c t i o n v i e w t h a t I h o l d , y e t a l m o s t n o n e o f w h i c h I find m y s e l f d i s a g r e e i n g w i t h . I t h i n k this is a v a l u a b l e p a p e r , e v e n t h o u g h its o s t e n s i b l e purpose is to a t t a c k the v i e w that ' w i t h respect to natural selection . . . it is the g e n e , not the i n d i v i d u a l or g r o u p , that is the unit'. W r i g h t c o n c l u d e s that ' T h e l i k e l i h o o d o f o r g a n i s m i c , i n s t e a d o f m e r e l y g e n i c , s e l e c t i o n g o e s far t o w a r d m e e t i n g o n e of the most serious objections to the theory of natural selection e n c o u n t e r e d by D a r w i n . ' He attributes the 'genie selection' v i e w to W i l l i a m s , M a y n a r d S m i t h a n d m e , a n d t r a c e s i t b a c k t o R . A . F i s h e r , I think c o r r e c t l y . A l l o f w h i c h m i g h t l e a d h i m t o b e s o m e w h a t b e m u s e d b y the following
accolade
from
Medawar
(1981):
'The
most
i m p o r t a n t single
A c t i o n at a D i s t a n c e
239
innovation in the m o d e r n synthesis w a s h o w e v e r the n e w c o n c e p t i o n that a population that was d e e m e d to u n d e r g o evolution c o u l d best be t h o u g h t of as a population of f u n d a m e n t a l r e p l i c a t i n g u n i t s — o f g e n e s — r a t h e r than as a population
of individual
animals
or
of cells.
Sewall
Wright . . . was
a
p r i n c i p a l i n n o v a t o r i n this n e w w a y o f t h i n k i n g — a p r i o r i t y for w h i c h R . A . F i s h e r , a n i m p o r t a n t b u t lesser f i g u r e , n e v e r f o r g a v e h i m I n t h e rest o f this c h a p t e r ,
I
hope to show that the version of 'genic
selectionism' that can be attacked as naively atomistic and reductionistic is a straw m a n ; that it is not the v i e w that I am a d v o c a t i n g ; a n d that if genes are c o r r e c t l y u n d e r s t o o d as b e i n g s e l e c t e d for their capacity to cooperate w i t h o t h e r genes in the g e n e - p o o l , we arrive at a theory of g e n i c selection w h i c h W r i g h t and M a y r will r e c o g n i z e a s fully c o m p a t i b l e w i t h their o w n v i e w s . N o t o n l y compatible but,
I w o u l d c l a i m , a truer a n d a clearer expression of their
v i e w s . I shall q u o t e k e y p a s s a g e s f r o m t h e s u m m a r y o f M a y r ' s c h a p t e r ( p p . 2 9 5 - 2 9 6 ) , s h o w i n g h o w they m a y b e a d a p t e d t o the w o r l d o f the e x t e n d e d phenotype. T h e p h e n o t y p e is the p r o d u c t of the h a r m o n i o u s i n t e r a c t i o n of all genes. T h e g e n o t y p e is a 'physiological t e a m ' in w h i c h a g e n e c a n m a k e a m a x i m u m c o n t r i b u t i o n t o fitness b y e l a b o r a t i n g its c h e m i c a l ' g e n e p r o d u c t ' in the n e e d e d q u a n t i t y a n d at the time w h e n it is needed in development [ M a y r 1963]. A n extended p h e n o t y p i c c h a r a c t e r i s t h e p r o d u c t o f t h e i n t e r a c t i o n o f m a n y genes w h o s e influence i m p i n g e s from b o t h inside a n d outside the o r g a n i s m . The
interaction
is
not
necessarily
harmonious—but
then
nor
are
gene
interactions within bodies necessarily harmonious, as we saw in C h a p t e r 8. T h e genes whose influences converge on a particular p h e n o t y p i c character a r e a ' p h y s i o l o g i c a l t e a m ' o n l y in a s p e c i a l a n d s u b t l e sense, a n d this is t r u e o f the c o n v e n t i o n a l w i t h i n - b o d y i n t e r a c t i o n s t o w h i c h M a y r refers, a s w e l l a s of extended interactions. I h a v e p r e v i o u s l y tried t o c o n v e y t h a t s p e c i a l sense w i t h t h e m e t a p h o r o f a rowing crew
(Dawkins
1976a,
pp.
91-92),
and
with
the
metaphor of
c o o p e r a t i o n b e t w e e n m y o p i c a n d n o r m a l - s i g h t e d p e o p l e ( D a w k i n s 1980, p p . 2 2 - 2 4 ) . T h e p r i n c i p l e m i g h t also b e l a b e l l e d t h e J a c k S p r a t p r i n c i p l e . T w o individuals with c o m p l e m e n t a r y appetites,
s a y for fat a n d
lean, or with
c o m p l e m e n t a r y skills, s a y i n g r o w i n g w h e a t a n d m i l l i n g it, f o r m n a t u r a l l y h a r m o n i o u s p a r t n e r s h i p s , a n d it is p o s s i b l e to r e g a r d a p a r t n e r s h i p as a higher-order unit. T h e interesting question is h o w such h a r m o n i o u s units come about. I w a n t to m a k e a general distinction b e t w e e n two models of selective processes,
both of w h i c h could,
in theory,
lead
to harmonious
cooperation and complementarity. T h e first m o d e l i n v o k e s s e l e c t i o n a t t h e l e v e l o f t h e h i g h e r - o r d e r u n i t s : i n a
240
A c t i o n at a D i s t a n c e
m e t a p o p u l a t i o n of h i g h e r - o r d e r units, h a r m o n i o u s units are favoured against d i s h a r m o n i o u s u n i t s . I t w a s a v e r s i o n o f this first m o d e l t h a t I s u g g e s t e d w a s implicit
in
the
Gaia
hypothesis—selection
among
planets
in
that case.
C o m i n g d o w n t o e a r t h , t h e first m o d e l m i g h t s u g g e s t t h a t g r o u p s o f a n i m a l s w h o s e m e m b e r s c o m p l e m e n t o n e a n o t h e r s ' skills, s a y g r o u p s c o n t a i n i n g b o t h farmers a n d millers, survive better than groups of farmers alone, or groups of m i l l e r s a l o n e . T h e s e c o n d m o d e l i s t h e o n e t h a t I find m o r e p l a u s i b l e . I t d o e s not need to postulate a m e t a p o p u l a t i o n of groups.
It is related to w h a t
p o p u l a t i o n geneticists call frequency-dependent selection. Selection goes on at the l o w e r level, the level of the c o m p o n e n t parts of a harmonious c o m p l e x . C o m p o n e n t s within a population are favoured by selection if they happen to interact h a r m o n i o u s l y w i t h the other c o m p o n e n t s that h a p p e n to be frequent in the p o p u l a t i o n . In a p o p u l a t i o n d o m i n a t e d by millers, i n d i v i d u a l farmers prosper, w h i l e in a p o p u l a t i o n d o m i n a t e d by farmers it p a y s to be a miller. B o t h kinds o f m o d e l l e a d t o a result w h i c h M a y r w o u l d call h a r m o n i o u s a n d c o o p e r a t i v e . B u t I am afraid that the c o n t e m p l a t i o n of h a r m o n y too o f t e n l e a d s b i o l o g i s t s t o t h i n k a u t o m a t i c a l l y i n t e r m s o f the first o f the t w o m o d e l s , a n d to forget the plausibility of the second. T h i s is true of genes w i t h i n a b o d y j u s t as it is true of farmers a n d millers in a c o m m u n i t y . T h e g e n o t y p e m a y be a ' p h y s i o l o g i c a l t e a m ' , b u t we do not h a v e to believe that that t e a m w a s necessarily selected as a harmonious unit in comparison with less h a r m o n i o u s r i v a l
units.
Rather,
each gene was selected
because it
p r o s p e r e d i n its e n v i r o n m e n t , a n d its e n v i r o n m e n t n e c e s s a r i l y i n c l u d e d t h e other genes w h i c h w e r e s i m u l t a n e o u s l y p r o s p e r i n g in the g e n e - p o o l . G e n e s w i t h c o m p l e m e n t a r y 'skills' prosper in e a c h others' presence. W h a t d o e s c o m p l e m e n t a r i n e s s m e a n for g e n e s ? T w o g e n e s m a y b e said t o b e c o m p l e m e n t a r y i f t h e s u r v i v a l o f e a c h , r e l a t i v e t o its a l l e l e s , i s e n h a n c e d w h e n t h e o t h e r i s a b u n d a n t i n t h e p o p u l a t i o n . T h e m o s t o b v i o u s r e a s o n for such m u t u a l assistance stems from the t w o genes performing a mutually c o m p l e m e n t a r y function w i t h i n individual bodies that they h a p p e n to share. T h e s y n t h e s i s o f c h e m i c a l s u b s t a n c e s o f b i o l o g i c a l i m p o r t a n c e often d e p e n d s u p o n a c h a i n of steps in a b i o c h e m i c a l p a t h w a y , e a c h o n e m e d i a t e d by a p a r t i c u l a r e n z y m e . T h e usefulness o f a n y o n e o f t h e s e e n z y m e s i s c o n d i t i o n a l u p o n the p r e s e n c e of the other e n z y m e s in the c h a i n . A g e n e - p o o l w h i c h is r i c h i n g e n e s for a l l e n z y m e s i n a g i v e n c h a i n e x c e p t o n e m a y set u p a s e l e c t i o n p r e s s u r e i n f a v o u r o f t h e g e n e for t h e m i s s i n g l i n k i n the c h a i n . I f there
are
alternative
pathways
to
the
same
biochemical
end
product,
selection m a y f a v o u r either p a t h w a y (but not both) d e p e n d i n g u p o n initial conditions. R a t h e r than r e g a r d the alternative p a t h w a y s as units b e t w e e n w h i c h selection chooses ( M o d e l 1), it is better to think as follows ( M o d e l 2 ) : selection will f a v o u r a g e n e that m a k e s a g i v e n e n z y m e , to the extent that g e n e s for m a k i n g t h e o t h e r e n z y m e s i n its p a t h w a y a r e a l r e a d y a b u n d a n t i n the g e n e - p o o l .
A c t i o n at a D i s t a n c e
241
But we do not h a v e to stay at a b i o c h e m i c a l level. I m a g i n e a species of m o t h w i t h stripes o n t h e w i n g s w h i c h r e s e m b l e g r o o v e s i n t r e e b a r k . S o m e i n d i v i d u a l s h a v e t r a n s v e r s e stripes w h i l e o t h e r s , i n a d i f f e r e n t a r e a , h a v e longitudinal stripes, the difference b e i n g d e t e r m i n e d at a single g e n e t i c locus. C l e a r l y a moth will be well c a m o u f l a g e d only if it points itself in the right d i r e c t i o n w h e n s i t t i n g o n t r e e b a r k ( S a r g e n t 1 9 6 9 b ) . S u p p o s e s o m e m o t h s sit vertically
and
others
horizontally,
the
behavioural
difference
being
c o n t r o l l e d a t a s e c o n d l o c u s . A n o b s e r v e r finds t h a t , f o r t u n a t e l y , a l l t h e m o t h s i n o n e a r e a h a v e l o n g i t u d i n a l stripes a n d sit v e r t i c a l l y ,
while in
a n o t h e r a r e a all t h e m o t h s h a v e t r a n s v e r s e stripes a n d sit h o r i z o n t a l l y . W e might
say,
between
then,
that
in
both
areas
there
t h e g e n e s for s t r i p e o r i e n t a t i o n
is
and
'harmonious
cooperation'
the genes d e t e r m i n i n g the
o r i e n t a t i o n o f s i t t i n g . H o w h a s this h a r m o n y c o m e a b o u t ? A g a i n w e i n v o k e o u r t w o m o d e l s . M o d e l 1 says that d i s h a r m o n i o u s g e n e c o m b i n a t i o n s — t r a n s v e r s e stripes w i t h v e r t i c a l r e s t i n g b e h a v i o u r , o r l o n g i t u dinal
stripes
with
horizontal
resting
harmonious gene combinations.
behaviour—died
Model
1
out,
leaving
only
i n v o k e s s e l e c t i o n a m o n g combi-
nations o f g e n e s . M o d e l 2 , o n t h e o t h e r h a n d , i n v o k e s s e l e c t i o n a t t h e l o w e r l e v e l o f t h e g e n e . If, for w h a t e v e r r e a s o n , t h e g e n e - p o o l i n a g i v e n a r e a h a p p e n s t o b e a l r e a d y d o m i n a t e d b y g e n e s for t r a n s v e r s e s t r i p e s , this w i l l a u t o m a t i c a l l y set u p a s e l e c t i o n p r e s s u r e a t t h e b e h a v i o u r a l l o c u s i n f a v o u r o f g e n e s for s i t t i n g h o r i z o n t a l l y . T h i s i n t u r n w i l l set u p a s e l e c t i o n p r e s s u r e t o increase the p r e d o m i n a n c e of transverse stripe genes at the striping locus w h i c h will, in turn, reinforce the selection in favour of sitting h o r i z o n t a l l y . T h e population will therefore rapidly c o n v e r g e on the e v o l u t i o n a r i l y stable c o m b i n a t i o n , t r a n s v e r s e stripes/sit h o r i z o n t a l l y . C o n v e r s e l y , a d i f f e r e n t set o f starting conditions w o u l d evolutionarily
stable
lead
state,
the p o p u l a t i o n
longitudinal
to converge
stripes/sit
on
vertically.
combination of starting frequencies at the t w o loci
the other
Any
given
will converge,
after
selection, on o n e or other of the t w o stable states. M o d e l 1 i s a p p l i c a b l e o n l y i f t h e p a i r s o r sets o f c o o p e r a t i n g g e n e s a r e e s p e c i a l l y l i k e l y t o find t h e m s e l v e s t o g e t h e r i n b o d i e s , for i n s t a n c e i f t h e y a r e closely linked into a ' s u p e r g e n e ' on one c h r o m o s o m e . T h e y m i g h t indeed be so linked (Ford 1 9 7 5 ) , b u t M o d e l 2 is particularly interesting b e c a u s e it enables us to visualize the evolution of harmonious gene c o m p l e x e s w i t h o u t such
linkage.
In
Model
2
the
cooperating genes
may
be
on
c h r o m o s o m e s , a n d f r e q u e n c y - d e p e n d e n t s e l e c t i o n w i l l still l e a d
different to popu-
lations b e i n g d o m i n a t e d by genes that interact h a r m o n i o u s l y w i t h the other genes
in
the
population,
as
a
result
of evolution
to
one
or
another
evolutionarily stable state ( L a w l o r & M a y n a r d S m i t h 1 9 7 6 ) . In p r i n c i p l e the s a m e k i n d o f r e a s o n i n g i s a p p l i c a b l e t o sets o f t h r e e l o c i ( s u p p o s e s t r i p e s o n the
hindwing
were
controlled
at
a
different
locus
from
stripes
on
the
f o r e w i n g ) , four loci . . . n l o c i . I f w e t r y t o m o d e l t h e i n t e r a c t i o n s i n d e t a i l t h e
242
A c t i o n at a D i s t a n c e
m a t h e m a t i c s b e c o m e d i f f i c u l t , b u t t h a t d o e s n o t m a t t e r for t h e p o i n t I w a n t to m a k e . A l l I am saying is that there are two general w a y s in w h i c h harmonious
cooperation
can
come
about.
One
way
is
for
harmonious
c o m p l e x e s to be favoured by selection over dis-harmonious complexes. T h e o t h e r i s for t h e s e p a r a t e parts o f c o m p l e x e s t o b e f a v o u r e d i n the p r e s e n c e , i n the p o p u l a t i o n , of other parts w i t h w h i c h they h a p p e n to h a r m o n i z e . H a v i n g u s e d M o d e l 2 for t h e k i n d o f w i t h i n - b o d y g e n e h a r m o n y t h a t M a y r had in mind, we now generalize it to between-body, 'extended', gene interactions.
We are going to be
talking about
genetic
interaction
at a
distance, rather t h a n the p h e n o t y p i c action at a distance w h i c h w a s the subject of the
e a r l i e r p a r t o f this c h a p t e r .
T h i s is
easy
to do,
because
frequency-dependent selection has classically been applied to between-body interactions,
from
Fisher's
(1930a)
t h e o r y o f t h e sex r a t i o o n .
p o p u l a t i o n s h a v e a b a l a n c e d sex ratio? M o d e l
W h y do
1 w o u l d suggest that it is
b e c a u s e p o p u l a t i o n s w i t h a n u n b a l a n c e d sex r a t i o h a v e g o n e e x t i n c t . F i s h e r ' s o w n h y p o t h e s i s is, o f c o u r s e , a v e r s i o n o f M o d e l 2 . I f a p o p u l a t i o n h a p p e n s t o h a v e a n u n b a l a n c e d s e x r a t i o , s e l e c t i o n within t h a t p o p u l a t i o n f a v o u r s g e n e s that tend to restore the b a l a n c e . T h e r e is no need to postulate a metap o p u l a t i o n of p o p u l a t i o n s , as in the case of M o d e l 1. Other examples geneticists
(e.g.
of frequency-dependent advantage Clarke
1979),
and
I
have
are well
previously
known to
discussed
their
r e l e v a n c e t o t h e c o n t r o v e r s y o v e r ' h a r m o n i o u s c o o p e r a t i o n ' ( D a w k i n s 1980, p p . 2 2 - 2 4 ) . T h e p o i n t I w a n t t o stress h e r e i s t h a t , f r o m t h e p o i n t o f v i e w o f each
replicating
entity,
complementariness relationships
within
between
its
relationships
genomes
genes
in
are
of harmony,
not,
different
in
cooperation
principle,
genomes.
The
different
gene
for
and from
sitting
vertically on tree-trunks is favoured in a gene-pool w h i c h h a p p e n s to be rich i n g e n e s for l o n g i t u d i n a l s t r i p e s , a n d v i c e v e r s a . H e r e , a s i n t h e b i o c h e m i c a l e x a m p l e o f the c h a i n o f e n z y m e s , the c o o p e r a t i o n takes p l a c e w i t h i n bodies: the s i g n i f i c a n c e o f t h e f a c t t h a t t h e g e n e - p o o l i s r i c h i n g e n e s for l o n g i t u d i n a l stripes i s t h a t a n y g i v e n g e n e a t t h e l o c u s d e t e r m i n i n g s i t t i n g b e h a v i o u r i s t h e r e f o r e s t a t i s t i c a l l y l i k e l y to be in a l o n g i t u d i n a l l y s t r i p e d b o d y . I s u g g e s t that
we
should
think
primarily
of genes
as
being selected
against
the
b a c k g r o u n d of the other genes that h a p p e n to be frequent in the gene-pool, and
only
secondarily
make
a
distinction
between
whether
the
salient
between-gene interactions h a p p e n to occur within bodies or between them. W i c k l e r ( 1 9 6 8 ) , i n his f a s c i n a t i n g r e v i e w o f a n i m a l m i m i c r y , p o i n t s o u t that
individuals
sometimes
appear
to
cooperate
in
achieving
mimetic
resemblance. He recounts an observation by K o e n i g of what appeared to be a sea a n e m o n e in an a q u a r i u m tank. T h e following d a y there w e r e t w o a n e m o n e s , e a c h h a l f t h e s i z e o f t h e o r i g i n a l o n e , a n d t h e d a y after t h a t the o r i g i n a l l a r g e a n e m o n e h a d a p p a r e n t l y r e c o n s t i t u t e d itself. T h e i m p o s s i b i l i t y
A c t i o n at a D i s t a n c e
243
o f this f i n a l l y led K o e n i g t o i n v e s t i g a t e i n d e t a i l , a n d h e d i s c o v e r e d t h a t t h e ' a n e m o n e ' w a s i n fact a f a k e , p u t t o g e t h e r b y n u m e r o u s c o o p e r a t i n g a n n e l i d worms. E a c h w o r m represented one tentacle, and they grouped themselves into a circle in the sand. Fish s e e m e d to be fooled by the d e c e p t i o n just as K o e n i g o r i g i n a l l y w a s , for t h e y g a v e t h e f a k e a n e m o n e t h e s a m e k i n d o f w i d e berth they w o u l d
a real one.
Each individual worm
presumably gained
p r o t e c t i o n f r o m fish p r e d a t o r s , b y j o i n i n g i n t h e c o o p e r a t i v e m i m i c r y r i n g . I s u g g e s t t h a t i t i s n o t h e l p f u l t o s p e a k o f groups o f w o r m s t h a t f o r m r i n g s a s being selected over groups that do not. R a t h e r , ring-joining i n d i v i d u a l s are favoured in populations of ring-joiners. In various insect species, e a c h i n d i v i d u a l m i m i c s o n e flower of a m a n y flowered inflorescence, and therefore a c o o p e r a t i n g c r o w d of t h e m is needed before a w h o l e inflorescence c a n be c o n v i n c i n g l y m i m i c k e d . ' I n East A f r i c a it
is
possible
to
find
a
particular
plant
with
extremely
beautiful
i n f l o r e s c e n c e s . . . t h e i n d i v i d u a l flowers a r e a b o u t h a l f a c e n t i m e t r e in h e i g h t , l o o k r a t h e r like b r o o m f l o w e r s , a n d a r e a r r a n g e d a r o u n d a v e r t i c a l s t e m l i k e the f l o w e r s o f t h e l u p i n .
E x p e r i e n c e d b o t a n i s t s h a v e t a k e n this p l a n t for
Tinnaea or Sesamopteris a n d f o u n d t h e m s e l v e s s u d d e n l y h o l d i n g a b a r e s t e m after p l u c k i n g the " f l o w e r " . T h e f l o w e r h a d n o t f a l l e n o f f — i t h a d f l o w n away!
The
nigritarsus In
"flower"
consists o f c i c a d a s ,
e i t h e r Ityraea gregorii o r
Oyarina
( W i c k l e r 1968, p. 6 1 ) .
order
to
develop
my
argument
I
need
to
make
certain
detailed
assumptions. S i n c e the details of the selection pressures b e a r i n g on these particular c i c a d a species are not k n o w n ,
it will
b e safest i f I
invent a
hypothetical c i c a d a w h i c h basically practises the same g r o u p - m i m i c r y trick as Ityraea a n d Oyarina. I a s s u m e t h a t my s p e c i e s o c c u r s in t w o c o l o u r m o r p h s , p i n k a n d b l u e , a n d t h a t the t w o m o r p h s m i m i c t w o d i f f e r e n t c o l o u r v a r i e t i e s of lupin. Pink a n d blue lupins are assumed to be e q u a l l y a b u n d a n t o v e r the w h o l e r a n g e of the c i c a d a species, b u t in a n y o n e l o c a l a r e a all the c i c a d a s are either pink or blue. together
near
the
' C o o p e r a t i o n ' occurs, in that individuals cluster
tips
of
plant
stems
and
together
resemble
lupin
inflorescences. It is ' h a r m o n i o u s ' in that m i x e d colour clusters do not o c c u r : I assume that a m i x e d c o l o u r cluster is especially likely to be spotted by predators as a fake, since real lupins do not h a v e t w o - t o n e inflorescences. H e r e i s h o w t h e h a r m o n y m i g h t h a v e c o m e a b o u t t h r o u g h M o d e l 2's frequency-dependent
selection.
In
any
given
area,
historical
accident
determined that there w a s an initial majority in f a v o u r of o n e c o l o u r t y p e or the o t h e r . I n a n a r e a t h a t h a p p e n e d t o b e d o m i n a t e d b y p i n k c i c a d a s , b l u e ones w e r e p e n a l i z e d .
In an area that h a p p e n e d to be d o m i n a t e d by blue
cicadas, pink one w e r e p e n a l i z e d . In both cases, simply b e i n g in the m i n o r i t y was disfavoured, b e c a u s e a m e m b e r of the m i n o r i t y t y p e w a s , by the l a w s of chance,
more
likely
than
a
m e m b e r of the
majority type
to
find
itself
244
A c t i o n at a D i s t a n c e
p a r t i c i p a t i n g in a m i x e d cluster. At the g e n e level we m a y say that pink genes are favoured in a gene-pool dominated by pink genes, and blue genes are favoured in a gene-pool dominated by blue genes. We n o w invent a n o t h e r insect, say a caterpillar, w h i c h is large e n o u g h to m i m i c a w h o l e lupin inflorescence, instead of a single flower. E a c h segment o f t h e c a t e r p i l l a r m i m i c s a different f l o w e r o f t h e i n f l o r e s c e n c e . T h e c o l o u r o f e a c h s e g m e n t i s c o n t r o l l e d a t a different l o c u s , t h e a l t e r n a t i v e s b e i n g p i n k a n d b l u e . A c a t e r p i l l a r t h a t i s a l l b l u e o r a l l p i n k i s m o r e successful t h a n o n e that is a m i x t u r e of colours because, o n c e a g a i n , predators h a v e learned that m i x e d colour lupins do not occur. T h e r e is no theoretical reason w h y twot o n e c a t e r p i l l a r s s h o u l d n o t o c c u r , b u t s u p p o s e t h a t , a s a result o f s e l e c t i o n , they do n o t : in a n y o n e a r e a the local caterpillars are either all pink or all blue. We have 'harmonious cooperation' again. How
might
the
harmonious
cooperation
come
about?
By
definition,
M o d e l 1 w o u l d b e a p p l i c a b l e o n l y i f t h e g e n e s r e s p o n s i b l e for t h e c o l o r a t i o n of the different s e g m e n t s w e r e linked tightly in a supergene. M u l t i - c o l o u r e d supergenes w o u l d be p e n a l i z e d at the expense of p u r e pink and pure blue supergenes.
I n this h y p o t h e t i c a l s p e c i e s , h o w e v e r , t h e r e l e v a n t g e n e s a r e
w i d e l y spread on different c h r o m o s o m e s , and we h a v e to a p p l y M o d e l 2. In a n y g i v e n l o c a l a r e a , o n c e o n e c o l o u r starts t o p r e d o m i n a t e a t a m a j o r i t y o f loci, selection w o r k s to increase the f r e q u e n c y of that c o l o u r at all loci. In a p a r t i c u l a r area, if all the loci save one are d o m i n a t e d by pink genes, the odd l o c u s w h i c h i s d o m i n a t e d b y b l u e g e n e s w i l l s o o n b e b r o u g h t i n t o line b y selection. As in the case of the hypothetical cicadas, historical accidents in different l o c a l a r e a s a u t o m a t i c a l l y set u p s e l e c t i o n p r e s s u r e s i n f a v o u r o f o n e o r a n o t h e r o f t w o e v o l u t i o n a r i l y s t a b l e states. T h e p o i n t o f this t h o u g h t e x p e r i m e n t i s t h a t M o d e l 2 i s e q u a l l y a p p l i c a b l e both b e t w e e n a n d w i t h i n i n d i v i d u a l s . In both the caterpillar a n d the c i c a d a case,
pink genes are favoured in gene-pools already d o m i n a t e d by pink
genes, and blue genes are favoured in gene-pools already dominated by blue g e n e s . I n t h e c a t e r p i l l a r s t h e r e a s o n i s t h a t e a c h g e n e benefits i f i t shares a body w i t h o t h e r g e n e s p r o d u c i n g t h e s a m e c o l o u r a s itself. I n t h e c i c a d a s t h e r e a s o n i s t h a t e a c h g e n e b e n e f i t s i f t h e b o d y i t i s i n m e e t s another b o d y b e a r i n g a g e n e p r o d u c i n g t h e s a m e c o l o u r a s itself. I n t h e c a t e r p i l l a r e x a m p l e , t h e c o o p e r a t i n g g e n e s o c c u p y different l o c i i n t h e s a m e i n d i v i d u a l . I n t h e c i c a d a example
the
cooperating
genes
occupy
the
same
locus
in
different
i n d i v i d u a l s . M y p u r p o s e i s t o c l o s e t h e c o n c e p t u a l g a p b e t w e e n these t w o kinds of g e n e interaction, by s h o w i n g that genetic interaction at a distance is n o t , i n p r i n c i p l e , different f r o m g e n e t i c i n t e r a c t i o n w i t h i n o n e b o d y . T o r e s u m e m y series o f q u o t a t i o n s f r o m M a y r : T h e result of the c o a d a p t i n g selection is a h a r m o n i o u s l y integrated g e n e c o m p l e x . T h e c o a c t i o n o f the genes m a y o c c u r a t m a n y levels,
A c t i o n at a D i s t a n c e
that
of the
chromosome,
nucleus,
cell,
tissue,
organ,
and
245
whole
organism. T h e r e a d e r w i l l b y n o w h a v e n o d i f f i c u l t y i n g u e s s i n g h o w M a y r ' s list i s t o b e e x t e n d e d . C o a c t i o n a m o n g g e n e s i n different o r g a n i s m s i s n o t f u n d a m e n t a l l y different f r o m c o a c t i o n a m o n g g e n e s i n t h e s a m e o r g a n i s m . E a c h g e n e w o r k s in a world of p h e n o t y p i c consequences of other genes. S o m e of those other genes will be m e m b e r s of the same g e n o m e . O t h e r s will be m e m b e r s of the same gene-pool operating through other bodies. Y e t others m a y be m e m b e r s o f different g e n e - p o o l s , different s p e c i e s , different p h y l a . T h e n a t u r e o f the f u n c t i o n a l m e c h a n i s m s o f p h y s i o l o g i c a l i n t e r a c t i o n are
[sic]
only
of minor
interest
to
the
evolutionist,
whose
main
c o n c e r n is the viability of the u l t i m a t e p r o d u c t , the p h e n o t y p e . M a y r hits t h e n a i l o n t h e h e a d a g a i n , b u t his ' p h e n o t y p e ' i s n o t t h e u l t i m a t e : it can be e x t e n d e d outside the i n d i v i d u a l b o d y . Many
devices
tend
to
maintain
the
status
quo
of
gene
pools,
quantitatively and qualitatively. T h e lower limit of genetic diversity is determined
b y the frequent a d v a n t a g e o f h e t e r o z y g o s i t y . . . T h e
u p p e r limit is d e t e r m i n e d by the fact that o n l y those g e n e s c a n be incorporated that are able to ' c o a d a p t ' h a r m o n i o u s l y . No g e n e has a f i x e d selective v a l u e ; the same g e n e m a y confer h i g h f i t n e s s o n o n e genetic b a c k g r o u n d and be virtually lethal on another. Excellent, but r e m e m b e r that 'genetic b a c k g r o u n d ' c a n i n c l u d e genes in other organisms as well as genes w i t h i n the s a m e o r g a n i s m . T h e result o f t h e c l o s e i n t e r d e p e n d e n c e o f a l l g e n e s i n a g e n e p o o l i s tight cohesion. N o g e n e frequency c a n b e c h a n g e d , nor a n y g e n e b e a d d e d t o t h e g e n e p o o l , w i t h o u t a n effect o n t h e g e n o t y p e a s a w h o l e , and thus indirectly on the selective v a l u e of o t h e r genes. M a y r h i m s e l f has n o w s u b t l y shifted t o t a l k i n g a b o u t a c o a d a p t e d g e n e pool, rather than a c o a d a p t e d individual g e n o m e . T h i s is a g r e a t step in the right d i r e c t i o n , b u t w e m u s t still t a k e o n e f u r t h e r s t e p . M a y r i s h e r e t a l k i n g a b o u t interactions b e t w e e n all the genes in o n e g e n e - p o o l , regardless of the bodies they
happen
to
be sitting
in.
T h e doctrine
of the
extended
phenotype
ultimately requires us to a c k n o w l e d g e the same kind of interactions a m o n g g e n e s o f different g e n e - p o o l s , different p h y l a , d i f f e r e n t k i n g d o m s . Consider a g a i n the w a y s in w h i c h a pair of genes in the same gene-pool can interact, m o r e specifically the w a y s in w h i c h the f r e q u e n c y of e a c h in the
246
A c t i o n at a D i s t a n c e
g e n e - p o o l c a n affect t h e s u r v i v a l p r o s p e c t s o f t h e o t h e r . T h e first w a y , a n d t h e o n e w h i c h I s u s p e c t M a y r h a d m a i n l y i n m i n d , i s t h r o u g h s h a r i n g the s a m e b o d y . T h e s u r v i v a l prospects of g e n e A are influenced by the frequency i n t h e p o p u l a t i o n o f g e n e B , b e c a u s e B's f r e q u e n c y i n f l u e n c e s t h e p r o b a b i l i t y t h a t A w i l l find i t s e l f s h a r i n g a b o d y w i t h B . T h e i n t e r a c t i o n b e t w e e n the l o c i d e t e r m i n i n g m o t h stripe direction and sitting direction w a s an e x a m p l e of this. S o w a s t h e h y p o t h e t i c a l l u p i n - m i m i c k i n g c a t e r p i l l a r . S o i s a p a i r o f genes
c o d i n g for
enzymes
that
are
necessary
for s u c c e s s i v e
stages
in
a
p a r t i c u l a r p a t h w a y s y n t h e s i z i n g a useful s u b s t a n c e . C a l l this t y p e o f g e n e interaction 'within-body' interaction. T h e second w a y in w h i c h the frequency of a gene B in a population can affect t h e s u r v i v a l p r o s p e c t s o f a g e n e A i s ' b e t w e e n - b o d y ' i n t e r a c t i o n . T h e v i t a l i n f l u e n c e h e r e i s o n t h e p r o b a b i l i t y t h a t a n y b o d y i n w h i c h A sits w i l l m e e t a n o t h e r b o d y i n w h i c h B sits. M y h y p o t h e t i c a l c i c a d a s p r o v i d e d a n e x a m p l e of this. So does Fisher's sex ratio theory. As I h a v e e m p h a s i z e d , it h a s b e e n o n e o f m y p u r p o s e s i n this c h a p t e r t o m i n i m i z e t h e d i s t i n c t i o n b e t w e e n the t w o kinds of g e n e interaction, w i t h i n - b o d y and b e t w e e n - b o d y interaction. But
now
consider
interactions
between
genes
in
different
gene-pools,
d i f f e r e n t s p e c i e s . I t w i l l b e s e e n t h a t t h e r e i s r a t h e r little d i s t i n c t i o n b e t w e e n a cross-species g e n e interaction a n d a within-species b e t w e e n - i n d i v i d u a l gene interaction. In neither case do the i n t e r a c t i n g genes share a b o d y . In both c a s e s t h e s u r v i v a l p r o s p e c t s o f e a c h m a y d e p e n d o n t h e f r e q u e n c y , i n its o w n g e n e - p o o l , of the o t h e r g e n e .
L e t me illustrate the point using the lupin
t h o u g h t e x p e r i m e n t a g a i n . S u p p o s e there is a species of beetle w h i c h is p o l y m o r p h i c like the c i c a d a s . In s o m e areas it turns out that the pink morphs of b o t h species, c i c a d a s a n d beetles, p r e d o m i n a t e , w h i l e in other areas the b l u e m o r p h s o f b o t h s p e c i e s p r e d o m i n a t e . T h e t w o s p e c i e s differ i n b o d y s i z e . T h e y ' c o o p e r a t e ' in faking inflorescences, the smaller-bodied cicadas tending t o sit n e a r t h e tips o f s t e m s , w h e r e s m a l l f l o w e r s m i g h t b e e x p e c t e d , t h e l a r g e r b e e t l e s t e n d i n g t o sit n e a r e r t h e b a s e o f e a c h f a k e i n f l o r e s c e n c e . A j o i n t b e e t l e / c i c a d a ' i n f l o r e s c e n c e ' fools b i r d s m o r e e f f e c t i v e l y t h a n e i t h e r a pure beetle or a pure c i c a d a one. M o d e l 2's f r e q u e n c y - d e p e n d e n t s e l e c t i o n w i l l t e n d t o l e a d t o t h e e v o l u t i o n o f o n e o f t w o e v o l u t i o n a r i l y s t a b l e states, j u s t a s b e f o r e , e x c e p t t h a t t w o species are n o w i n v o l v e d . If historical accident leads to one local area being dominated
by
pink morphs
(regardless of species),
selection
species will f a v o u r pink m o r p h s o v e r b l u e ; and vice versa.
within
both
If the beetle
s p e c i e s w a s r e l a t i v e l y r e c e n t l y i n t r o d u c e d i n t o a r e a s a l r e a d y c o l o n i z e d b y the c i c a d a species, the d i r e c t i o n of selection w i t h i n the beetle species will d e p e n d o n the c o l o u r o f the l o c a l l y p r e d o m i n a n t m o r p h o f c i c a d a s . T h u s there will be frequency-dependent interaction between genes in pools,
the
gene-pools
of two
non-interbreeding
t w o different g e n e -
species.
In
faking
the
A c t i o n at a D i s t a n c e
247
inflorescence of a lupin, c i c a d a s m i g h t c o o p e r a t e w i t h spiders or snails just as effectively as w i t h beetles or w i t h c i c a d a s of a n o t h e r species. M o d e l 2 w o r k s across s p e c i e s a n d a c r o s s p h y l a , a s w e l l a s a c r o s s i n d i v i d u a l s a n d w i t h i n individuals. Across usitissimum)
kingdoms, and
the
too.
Consider
rust
fungus
the
interaction
Melampsora
lini,
antagonistic rather than a cooperative interaction.
between although
flax
(Linum
this
is
an
' T h e r e is e s s e n t i a l l y a
one-to-one m a t c h i n g in w h i c h a specific allele in the flax confers resistance to a specific a l l e l e i n t h e rust. T h i s " g e n e - f o r - g e n e " s y s t e m h a s s i n c e b e e n f o u n d in numerous other plant species . . . M o d e l s of gene-for-gene interactions are not formulated in
terms of e c o l o g i c a l p a r a m e t e r s b e c a u s e of the specific
n a t u r e o f the g e n e t i c s y s t e m s . I t i s o n e c a s e i n w h i c h t h e g e n e t i c i n t e r a c t i o n s b e t w e e n species c a n be understood w i t h o u t reference to the p h e n o t y p e s . A model of a gene-for-gene system w o u l d necessarily h a v e between-species frequency dependence . . . (Slatkin & M a y n a r d Smith 1979, pp. 2 5 5 - 2 5 6 ) . I n this c h a p t e r , a s i n o t h e r s , I h a v e u s e d h y p o t h e t i c a l t h o u g h t e x p e r i m e n t s to aid clear e x p l a n a t i o n . In case they are found too far-fetched, let me turn t o W i c k l e r a g a i n for a n e x a m p l e o f a r e a l c i c a d a w h i c h d o e s s o m e t h i n g a t least as f a r - f e t c h e d as a n y t h i n g I h a v e i n v e n t e d . Ityraea nigrocincta, l i k e I. gregorii,
practises c o o p e r a t i v e
m i m i c r y of lupin-like
inflorescences,
but
it
'possesses a f u r t h e r p e c u l i a r i t y i n t h a t b o t h s e x e s h a v e t w o m o r p h s , a g r e e n form a n d a y e l l o w f o r m . T h e s e t w o m o r p h s m a y s q u a t t o g e t h e r , a n d t h e g r e e n forms t e n d t o sit a t t h e t o p o f t h e s t e m , e s p e c i a l l y o n v e r t i c a l s t e m s , with
the
yellow
"inflorescence",
forms
below.
because
the
The
true
result
flowers
is
an
extremely
convincing
of inflorescences
often
open
p r o g r e s s i v e l y f r o m b a s e t o a p e x , s o t h a t g r e e n b u d s a r e still p r e s e n t a t t h e tip w h e n the base is c o v e r e d w i t h o p e n flowers' ( W i c k l e r 1968). T h e s e three chapters h a v e e x t e n d e d the c o n c e p t o f p h e n o t y p i c expression of genes by easy stages. We b e g a n with the recognition that e v e n within a b o d y there are m a n y degrees o f distance o f g e n e control o v e r p h e n o t y p e s . F o r a n u c l e a r g e n e t o c o n t r o l t h e s h a p e o f t h e c e l l i n w h i c h i t sits i s p r e s u m a b l y simpler than to control the shape of s o m e o t h e r cell, or of the w h o l e b o d y i n w h i c h t h e c e l l sits. Y e t w e c o n v e n t i o n a l l y l u m p t h e t h r e e t o g e t h e r a n d c a l l t h e m a l l g e n e t i c c o n t r o l o f p h e n o t y p e . M y thesis h a s b e e n t h a t the s l i g h t
further c o n c e p t u a l step outside
the
immediate
b o d y is
a
c o m p a r a t i v e l y m i n o r o n e . N e v e r t h e l e s s i t i s a n u n f a m i l i a r o n e , a n d I tried t o d e v e l o p the i d e a i n s t a g e s , w o r k i n g t h r o u g h i n a n i m a t e a r t e f a c t s t o i n t e r n a l parasites
controlling
their
hosts'
behaviour.
From
internal
parasites
we
m o v e d via c u c k o o s to action at a distance. In theory, g e n e t i c action at a distance c o u l d i n c l u d e almost all interactions b e t w e e n i n d i v i d u a l s of the s a m e o r different s p e c i e s . T h e l i v i n g w o r l d c a n b e s e e n a s a n e t w o r k o f interlocking fields of replicator power. It
is
hard
for
me
to
imagine
the
kind
of
mathematics
that
the
A c t i o n at a D i s t a n c e
248
u n d e r s t a n d i n g of the details w i l l e v e n t u a l l y d e m a n d . I h a v e a d i m vision of p h e n o t y p i c c h a r a c t e r s i n a n e v o l u t i o n a r y s p a c e b e i n g t u g g e d i n different directions by replicators u n d e r selection. It is of the essence of my a p p r o a c h that the replicators t u g g i n g on a n y given p h e n o t y p i c feature will include s o m e f r o m o u t s i d e t h e b o d y a s w e l l a s t h o s e i n s i d e it. S o m e w i l l o b v i o u s l y b e tugging
harder
than
others,
so
the
arrows
of force
will
have
varying
m a g n i t u d e as w e l l as d i r e c t i o n . P r e s u m a b l y the theory of arms races—the r a r e - e n e m y effect, t h e l i f e / d i n n e r p r i n c i p l e , e t c . — w i l l h a v e a p r o m i n e n t role to p l a y in the assignment of these m a g n i t u d e s . S h e e r physical p r o x i m i t y will p r o b a b l y p l a y a role: genes seem likely, other things b e i n g equal, to exert more p o w e r over n e a r b y phenotypic characters than over distant ones. As an i m p o r t a n t s p e c i a l c a s e o f this, c e l l s a r e l i k e l y t o b e q u a n t i t a t i v e l y m o r e h e a v i l y influenced by genes inside t h e m than by genes inside other cells. T h e s a m e w i l l g o for b o d i e s . B u t t h e s e w i l l b e q u a n t i t a t i v e effects, t o b e w e i g h e d in the b a l a n c e w i t h other considerations from arms r a c e theory. S o m e t i m e s , s a y b e c a u s e o f t h e r a r e - e n e m y effect, g e n e s i n o t h e r b o d i e s m a y e x e r t m o r e p o w e r t h a n t h e b o d y ' s ' o w n ' g e n e s , o v e r p a r t i c u l a r a s p e c t s o f its p h e n o t y p e . M y h u n c h i s t h a t a l m o s t a l l p h e n o t y p i c c h a r a c t e r s w i l l t u r n o u t t o b e a r the m a r k s o f c o m p r o m i s e b e t w e e n internal a n d external replicator forces. T h e i d e a o f c o n f l i c t a n d c o m p r o m i s e b e t w e e n m a n y s e l e c t i o n pressures b e a r i n g o n a g i v e n p h e n o t y p i c c h a r a c t e r is, o f c o u r s e , f a m i l i a r f r o m o r d i n a r y b i o l o g y . W e o f t e n s p e a k of, s a y , t h e s i z e o f a b i r d ' s tail a s a c o m p r o m i s e b e t w e e n the needs of a e r o d y n a m i c s a n d the needs of sexual attractiveness. I d o n o t k n o w w h a t k i n d o f m a t h e m a t i c s a r e c o n s i d e r e d s u i t a b l e for d e s c r i b i n g this k i n d o f w i t h i n - b o d y c o n f l i c t a n d c o m p r o m i s e , b u t w h a t e v e r t h e y a r e , they should be g e n e r a l i z e d to c o p e with the analogous problems of genetic action at a distance and extended phenotypes. But I h a v e not the w i n g s to fly in m a t h e m a t i c a l spaces. T h e r e must be a v e r b a l m e s s a g e for t h o s e t h a t s t u d y a n i m a l s i n t h e field. W h a t d i f f e r e n c e w i l l the
doctrine
of the
extended
phenotype
make
to
how we
a c t u a l l y see
a n i m a l s ? M o s t s e r i o u s field b i o l o g i s t s n o w s u b s c r i b e t o t h e t h e o r e m , l a r g e l y d u e to H a m i l t o n , that a n i m a l s are e x p e c t e d to b e h a v e as if m a x i m i z i n g the s u r v i v a l c h a n c e s o f a l l t h e g e n e s i n s i d e t h e m . I h a v e a m e n d e d this t o a n e w c e n t r a l t h e o r e m o f the e x t e n d e d p h e n o t y p e : A n a n i m a l ' s b e h a v i o u r tends t o m a x i m i z e t h e s u r v i v a l o f t h e g e n e s ' f o r ' t h a t b e h a v i o u r , w h e t h e r o r n o t those g e n e s h a p p e n t o b e i n t h e b o d y o f t h e p a r t i c u l a r a n i m a l p e r f o r m i n g the b e h a v i o u r . T h e t w o theorems w o u l d a m o u n t to the same thing if animal phenotypes
were
always
under
the
unadulterated
control
of their o w n
g e n o t y p e s , a n d u n i n f l u e n c e d b y the genes o f other organisms. I n a d v a n c e o f a
mathematical
theory
to
handle
the
quantitative
interactions
between
c o n f l i c t i n g p r e s s u r e s , p e r h a p s t h e s i m p l e s t q u a l i t a t i v e c o n c l u s i o n i s t h a t the b e h a v i o u r w e a r e l o o k i n g a t m a y b e , a t l e a s t p a r t l y , a n a d a p t a t i o n for the
A c t i o n at a D i s t a n c e
249
preservation of some other animal's or plant's genes. It m a y therefore be p o s i t i v e l y m a l a d a p t i v e for t h e o r g a n i s m p e r f o r m i n g t h e b e h a v i o u r . O n c e w h e n I tried to p e r s u a d e a c o l l e a g u e of this—he is a s t a u n c h b e l i e v e r in the p o w e r of D a r w i n i a n selection, a n d a g o o d field i n v e s t i g a t o r of i t — h e thought that I was m a k i n g an anti-adaptation point. He w a r n e d me that t i m e a n d a g a i n p e o p l e h a d w r i t t e n off s o m e q u i r k o f a n i m a l b e h a v i o u r o r m o r p h o l o g y as functionless or m a l a d a p t i v e , only to d i s c o v e r that they h a d n o t fully u n d e r s t o o d it. H e w a s r i g h t . B u t t h e p o i n t I a m m a k i n g i s d i f f e r e n t . W h e n I s a y h e r e t h a t a b e h a v i o u r p a t t e r n is m a l a d a p t i v e , I o n l y m e a n it is m a l a d a p t i v e for t h e individual animal p e r f o r m i n g it. I am s u g g e s t i n g t h a t t h e i n d i v i d u a l p e r f o r m i n g t h e b e h a v i o u r i s n o t t h e e n t i t y for w h o s e b e n e f i t t h e behaviour responsible
is
an
for
adaptation. them,
and
Adaptations only
benefit
incidentally
the
the
genetic
replicators
individual
organisms
involved. This
could
have
been
the
end
of the
book.
We
have
extended
the
p h e n o t y p e o u t a s far a s i t c a n g o . T h e p a s t t h r e e c h a p t e r s b u i l d t o a c l i m a x o f a sort, a n d w e m i g h t h a v e b e e n c o n t e n t w i t h this a s c o n s u m m a t i o n . B u t I prefer
to end
on
an
upbeat,
to begin
the arousing of a
tentative
new
c u r i o s i t y . I c o n f e s s e d a t t h e o u t s e t t o b e i n g a n a d v o c a t e , a n d a n e a s y w a y for a n y a d v o c a t e t o p r e p a r e t h e g r o u n d for his c a s e i s t o a t t a c k t h e a l t e r n a t i v e . Before a d v o c a t i n g the d o c t r i n e o f the e x t e n d e d p h e n o t y p e o f a n a c t i v e g e r m line r e p l i c a t o r , t h e r e f o r e , I t r i e d t o u n d e r m i n e t h e r e a d e r ' s c o n f i d e n c e i n t h e individual o r g a n i s m as the unit of a d a p t i v e benefit. B u t , n o w that we h a v e discussed the e x t e n d e d p h e n o t y p e itself, i t i s t i m e t o r e o p e n t h e q u e s t i o n o f t h e o r g a n i s m ' s e x i s t e n c e a n d o b v i o u s i m p o r t a n c e i n t h e h i e r a r c h y o f life, a n d see w h e t h e r w e see i t a n y c l e a r e r i n t h e l i g h t o f t h e e x t e n d e d p h e n o t y p e . G i v e n t h a t life d i d n o t have t o b e p a c k a g e d i n t o d i s c r e t e o r g a n i s m s , a n d a l l o w i n g that organisms are not a l w a y s totally discrete, w h y , nevertheless, d i d a c t i v e g e r m - l i n e r e p l i c a t o r s s o c o n s p i c u o u s l y o p t for t h e o r g a n i s m a l w a y of doing things?
14 Rediscovering the O r g a n i s m
H a v i n g d e v o t e d m o s t o f this b o o k t o p l a y i n g d o w n t h e i m p o r t a n c e o f the
individual
organism,
and
to
building up an
alternative image of a
t u r m o i l o f selfish r e p l i c a t o r s , b a t t l i n g for t h e i r o w n s u r v i v a l a t t h e e x p e n s e o f their alleles, r e a c h i n g u n i m p e d e d through individual b o d y walls as though those walls w e r e transparent, interacting w i t h the w o r l d a n d w i t h e a c h other w i t h o u t regard to organismal boundaries, we n o w hesitate. T h e r e really is something pretty impressive about individual organisms. If we actually could w e a r s p e c t a c l e s t h a t m a d e b o d i e s t r a n s p a r e n t a n d d i s p l a y e d o n l y D N A , the d i s t r i b u t i o n o f D N A t h a t w e w o u l d see i n t h e w o r l d w o u l d b e o v e r w h e l m i n g l y n o n - r a n d o m . I f c e l l n u c l e i g l o w e d l i k e stars a n d a l l else w a s i n v i s i b l e , multicellular bodies would show up as close-packed galaxies with cavernous space b e t w e e n them. A million billion g l o w i n g pinpricks m o v e in unison with e a c h o t h e r a n d o u t o f step w i t h all the m e m b e r s o f other such g a l a x i e s . T h e o r g a n i s m i s a p h y s i c a l l y d i s c r e t e m a c h i n e , u s u a l l y w a l l e d off from other such machines.
It has an internal organization,
often o f s t a g g e r i n g
c o m p l e x i t y , a n d it displays to a h i g h d e g r e e the q u a l i t y that J u l i a n H u x l e y (1912) labelled 'individuality'—literally indivisibility—the quality of being sufficiently h e t e r o g e n e o u s in form to be rendered non-functional if cut in half. G e n e t i c a l l y s p e a k i n g , t o o , t h e i n d i v i d u a l o r g a n i s m i s u s u a l l y a c l e a r l y d e f i n a b l e u n i t , w h o s e c e l l s h a v e t h e s a m e g e n e s a s e a c h o t h e r b u t different genes from the cells o f o t h e r organisms. T o a n i m m u n o l o g i s t the i n d i v i d u a l o r g a n i s m has a special kind of 'uniqueness' ( M e d a w a r 1 9 5 7 ) , in that it will r e a d i l y a c c e p t g r a f t s f r o m o t h e r p a r t s o f its o w n b o d y , b u t n o t f r o m o t h e r bodies.
To
the
ethologist—and
indivisibility—the
organism
s t r o n g e r sense t h a n , s a y ,
is
a
this
is
really
an
aspect
unit of b e h a v i o u r a l
action
of in
Huxley's a
much
two organisms, or a limb of an organism. T h e
organism has one coordinated central nervous system.
It takes 'decisions'
( D a w k i n s & D a w k i n s 1 9 7 3 ) a s a u n i t . A l l its l i m b s c o n s p i r e h a r m o n i o u s l y t o g e t h e r to a c h i e v e o n e end at a time. On those occasions w h e n t w o or more organisms
try
to
coordinate
their
efforts, 250
say
when
a
pride
o f lions
R e d i s c o v e r i n g the O r g a n i s m
251
c o o p e r a t i v e l y s t a l k s p r e y , t h e feats o f c o o r d i n a t i o n a m o n g i n d i v i d u a l s a r e feeble
compared
with
the
intricate orchestration,
with
high
spatial
and
temporal precision, of the hundreds of muscles within e a c h i n d i v i d u a l . E v e n a starfish, w h o s e t u b e - f e e t e n j o y a m e a s u r e o f a u t o n o m y a n d m a y t e a r t h e a n i m a l in t w o if the c i r c u m - o r a l nerve ring has b e e n s u r g i c a l l y cut, looks like a single entity, a n d in n a t u r e b e h a v e s as if it h a d a single p u r p o s e . I
am grateful
to Dr J.
P.
H a i l m a n for n o t w i t h h o l d i n g f r o m m e t h e
s a r c a s t i c r e a c t i o n o f a c o l l e a g u e t o t h e p a p e r t h a t w a s a b r i e f t r i a l - r u n for this book ( D a w k i n s 1 9 7 8 a ) : ' R i c h a r d D a w k i n s has rediscovered the o r g a n i s m . ' T h e i r o n y w a s n o t lost o n m e , b u t t h e r e a r e w h e e l s w i t h i n w h e e l s . W e a g r e e that there is s o m e t h i n g special a b o u t the i n d i v i d u a l o r g a n i s m as a l e v e l in the h i e r a r c h y o f life, b u t i t i s n o t s o m e t h i n g o b v i o u s , t o b e a c c e p t e d w i t h o u t q u e s t i o n . M y h o p e i s t h a t this b o o k h a s r e v e a l e d t h a t t h e r e i s a s e c o n d side t o the N e c k e r C u b e . B u t N e c k e r C u b e s h a v e a h a b i t o f f l i p p i n g b a c k a g a i n t o their original orientation, a n d then c o n t i n u i n g to a l t e r n a t e . W h a t e v e r it is t h a t i s s p e c i a l a b o u t t h e i n d i v i d u a l o r g a n i s m a s a u n i t o f life, w e s h o u l d a t least see i t m o r e c l e a r l y for h a v i n g v i e w e d t h e o t h e r s i d e o f t h e N e c k e r C u b e , for h a v i n g t r a i n e d o u r e y e s t o see t h r o u g h b o d y w a l l s i n t o t h e w o r l d o f replicators, and out and b e y o n d to their e x t e n d e d p h e n o t y p e s . S o , w h a t i s i t t h a t i s s p e c i a l a b o u t t h e i n d i v i d u a l o r g a n i s m ? G i v e n t h a t life can be v i e w e d as consisting of replicators w i t h their e x t e n d e d p h e n o t y p i c tools o f s u r v i v a l , w h y i n p r a c t i c e h a v e r e p l i c a t o r s c h o s e n t o g r o u p t h e m s e l v e s together b y the h u n d r e d s o f thousands i n cells, a n d w h y h a v e they influenced those cells t o c l o n e t h e m s e l v e s b y t h e m i l l i o n s o f b i l l i o n s i n o r g a n i s m s ? O n e kind o f a n s w e r i s suggested b y the logic o f c o m p l e x systems. S i m o n (1962) has written a s t i m u l a t i n g essay on ' T h e a r c h i t e c t u r e of c o m p l e x i t y ' , w h i c h suggests
(using a p a r a b l e of t w o w a t c h m a k e r s called T e m p u s a n d
H o r a , w h i c h has b e c o m e well k n o w n ) , a g e n e r a l functional reason w h y complex
organization
of any
kind,
biological
or
artificial,
tends
to
be
o r g a n i z e d i n t o n e s t e d h i e r a r c h i e s o f r e p e a t e d s u b u n i t s . I h a v e d e v e l o p e d his argument
in
the
ethological
context,
concluding
that
the
evolution
of
statistically ' i m p r o b a b l e assemblies p r o c e e d s m o r e r a p i d l y if there is a succession o f i n t e r m e d i a t e s t a b l e s u b - a s s e m b l i e s . S i n c e t h e a r g u m e n t c a n b e applied to e a c h sub-assembly, it follows that h i g h l y c o m p l e x systems w h i c h exist i n t h e w o r l d a r e l i k e l y t o h a v e a h i e r a r c h i c a l a r c h i t e c t u r e ' ( D a w k i n s 1976b).
In
the
present
context
the
hierarchy
consists
of genes
within
cells a n d cells w i t h i n o r g a n i s m s . M a r g u l i s ( 1 9 8 1 ) m a k e s a p e r s u a s i v e a n d f a s c i n a t i n g c a s e for a n o l d i d e a t h a t the h i e r a r c h y c o n t a i n s y e t a n o t h e r intermediate level:
eukaryotic
'cells'
are themselves,
in a sense,
multi-
cellular clusters, s y m b i o t i c unions of entities such as m i t o c h o n d r i a , plastids and cilia, w h i c h are h o m o l o g o u s to, a n d d e s c e n d e d from, p r o k a r y o t i c cells. I will not pursue the m a t t e r further here. S i m o n ' s point is a v e r y g e n e r a l one, a n d we need a m o r e specific a n s w e r to the question of w h y replicators
252
R e d i s c o v e r i n g the O r g a n i s m
chose to o r g a n i z e their p h e n o t y p e s into functional units, especially at the t w o levels of the cell a n d the m u l t i c e l l u l a r o r g a n i s m . I n o r d e r t o a s k q u e s t i o n s a b o u t w h y t h e w o r l d i s t h e w a y i t is, w e h a v e t o i m a g i n e h o w i t m i g h t h a v e b e e n . W e i n v e n t p o s s i b l e w o r l d s i n w h i c h life m i g h t h a v e b e e n o r g a n i z e d d i f f e r e n t l y , a n d ask w h a t w o u l d h a v e h a p p e n e d i f i t h a d b e e n . W h a t i n s t r u c t i v e a l t e r n a t i v e s t o t h e w a y life is, t h e n , c a n w e i m a g i n e ? F i r s t , i n o r d e r t o see w h y r e p l i c a t i n g m o l e c u l e s g a n g e d u p i n cells, w e i m a g i n e a w o r l d i n w h i c h t h e r e a r e r e p l i c a t i n g m o l e c u l e s f l o a t i n g freely in the sea. T h e r e are different varieties of replicator, and they are c o m p e t i n g w i t h e a c h o t h e r for s p a c e a n d for t h e c h e m i c a l r e s o u r c e s n e e d e d t o b u i l d copies of themselves, b u t they are not g r o u p e d together in chromosomes of nuclei. E a c h solitary replicator exerts p h e n o t y p i c p o w e r to m a k e copies of itself, a n d s e l e c t i o n f a v o u r s t h o s e w i t h t h e m o s t e f f e c t i v e p h e n o t y p i c p o w e r . I t i s e a s y t o b e l i e v e t h a t this f o r m o f life w o u l d n o t b e e v o l u t i o n a r i l y s t a b l e . I t w o u l d be i n v a d e d by m u t a n t replicators that ' g a n g up'. C e r t a i n replicators w o u l d h a v e c h e m i c a l effects t h a t c o m p l e m e n t t h o s e o f o t h e r r e p l i c a t o r s , c o m p l e m e n t t h e m i n t h e s e n s e t h a t w h e n t h e t w o c h e m i c a l effects a r e p u t together replication of b o t h is facilitated ( M o d e l 2 in the previous c h a p t e r ) . I h a v e a l r e a d y u s e d t h e e x a m p l e o f g e n e s c o d i n g for e n z y m e s t h a t c a t a l y s e successive stages of a b i o c h e m i c a l chain reaction. T h e same principle m a y be applied to larger groups of mutually complementary replicating molecules I n d e e d , e a r t h l y b i o c h e m i s t r y suggests that the m i n i m a l unit of replication, e x c e p t p o s s i b l y i n t h e f o o d - r i c h e n v i r o n m e n t o f a t o t a l p a r a s i t e , i s a b o u t fifty cistrons ( M a r g u l i s 1 9 8 1 ) . It m a k e s no difference to the a r g u m e n t w h e t h e r n e w g e n e s arise by d u p l i c a t i o n of old ones and r e m a i n close together, or w h e t h e r p r e v i o u s l y i n d e p e n d e n t g e n e s p o s i t i v e l y c o m e t o g e t h e r . W e c a n still discuss the e v o l u t i o n a r y stability of the state of b e i n g ' g a n g e d u p ' . G a n g i n g up of genes together into cells, then, is easily understood, but w h y d i d c e l l s g a n g t o g e t h e r i n t o m u l t i c e l l u l a r c l o n e s ? I n this c a s e i t m i g h t b e thought
that
we
do
not
have
to
invent
thought
experiments,
because
unicellular, or acellular, organisms abound on our world. These, however, a r e a l l s m a l l , a n d i t m a y b e useful t o i m a g i n e a p o s s i b l e w o r l d i n w h i c h t h e r e exist l a r g e a n d c o m p l e x u n i c e l l u l a r o r m o n o n u c l e a t e organisms. C o u l d there b e a f o r m o f life i n w h i c h o n e s i n g l e set o f g e n e s , e n t h r o n e d i n a s i n g l e c e n t r a l nucleus, directed the biochemistry of a macroscopic b o d y with c o m p l e x o r g a n s , either a single g i g a n t i c ' c e l l ' , or a m u l t i c e l l u l a r b o d y in w h i c h all but o n e of the cells l a c k e d their o w n p r i v a t e copies of the g e n o m e ? I think such a f o r m o f life c o u l d o n l y e x i s t i f its e m b r y o l o g y f o l l o w e d
principles very
different from those w i t h w h i c h we are familiar. In the e m b r y o l o g i e s that we know,
only
a
minority
of genes
are
'turned
on'
in
any
one
type
of
d i f f e r e n t i a t i n g tissue a t a n y o n e t i m e ( G u r d o n 1 9 7 4 ) . I t i s a d m i t t e d l y a w e a k a r g u m e n t a t this s t a g e , b u t i f t h e r e w e r e o n l y o n e set o f g e n e s i n t h e e n t i r e b o d y , i t i s n o t e a s y t o see h o w the a p p r o p r i a t e g e n e p r o d u c t s c o u l d b e
R e d i s c o v e r i n g the O r g a n i s m
conveyed
to
the v a r i o u s parts of the differentiating
body
at
the
253
appro-
priate times. B u t w h y d o e s t h e r e h a v e t o b e a complete set o f g e n e s i n e v e r y c e l l o f a d e v e l o p i n g b o d y ? I t i s s u r e l y e a s y t o i m a g i n e a f o r m o f life i n w h i c h p a r t s o f t h e g e n o m e a r e h i v e d off d u r i n g d i f f e r e n t i a t i o n , s o t h a t a g i v e n t y p e o f tissue, l i v e r tissue o r k i d n e y tissue s a y , h a s o n l y t h e g e n e s t h a t i t n e e d s . O n l y t h e germ-line cells, it w o u l d seem, really need to preserve the entire g e n o m e . It m a y be that the reason is simply that there is no easy w a y , p h y s i c a l l y , to h i v e off p a r t s o f t h e g e n o m e . I t i s n o t , after a l l , a s t h o u g h t h e g e n e s n e e d e d i n any particular differentiated region of the d e v e l o p i n g b o d y are all segregated o n o n e c h r o m o s o m e . W e c o u l d , I s u p p o s e , n o w a s k o u r s e l v e s w h y this h a d t o b e the c a s e . G i v e n t h a t i t i s t h e c a s e , full d i v i s i o n o f t h e e n t i r e g e n o m e a t e v e r y c e l l d i v i s i o n m a y s i m p l y b e t h e easiest a n d m o s t e c o n o m i c a l w a y o f doing things. H o w e v e r , in the light of my p a r a b l e ( C h a p t e r 9) of the rosys p e c t a c l e d M a r t i a n a n d t h e n e e d for c y n i c i s m , t h e r e a d e r m a y b e t e m p t e d t o s p e c u l a t e further. C o u l d i t b e t h a t t h e t o t a l , r a t h e r t h a n p a r t i a l , d u p l i c a t i o n of the g e n o m e in mitosis is an a d a p t a t i o n by s o m e genes to k e e p t h e m s e l v e s in
a
position
to
oversee
and
thwart
would-be
outlaws
among
their
c o l l e a g u e s ? P e r s o n a l l y I d o u b t it, n o t b e c a u s e t h e i d e a i s i n h e r e n t l y farf e t c h e d b u t b e c a u s e i t i s h a r d t o see h o w a g e n e i n t h e l i v e r , s a y , c o u l d s t a n d to gain from b e i n g an o u t l a w a n d m a n i p u l a t i n g the liver in a w a y that w o u l d be to the d e t r i m e n t of genes in the k i d n e y or the spleen. F o l l o w i n g the logic o f t h e c h a p t e r o n p a r a s i t e s , t h e interests o f ' l i v e r g e n e s ' a n d ' k i d n e y g e n e s ' w o u l d overlap because they share the same germ-line a n d the same g a m e t i c route out of the present b o d y . I h a v e n o t p r o v i d e d a r i g o r o u s d e f i n i t i o n o f t h e o r g a n i s m . I t is, i n d e e d , a r g u a b l e that the o r g a n i s m is a c o n c e p t of d u b i o u s utility, precisely b e c a u s e i t i s s o difficult t o d e f i n e s a t i s f a c t o r i l y . F r o m t h e i m m u n o l o g i c a l o r g e n e t i c points of v i e w , a pair of m o n o z y g o t i c twins w o u l d h a v e to c o u n t as a single organism, yet clearly they w o u l d not so qualify from the point of v i e w of the physiologist, the ethologist, or H u x l e y ' s indivisibility criterion. W h a t is 'the individual' in a colonial siphonophore or b r y o z o a n ? Botanists h a v e good r e a s o n t o b e less f o n d o f t h e p h r a s e ' i n d i v i d u a l o r g a n i s m ' t h a n z o o l o g i s t s a r e : ' T h e i n d i v i d u a l fruit f l y , f l o u r b e e t l e , r a b b i t ,
flatworm
or e l e p h a n t is a
population at the cellular but not at a n y h i g h e r level. S t a r v a t i o n does not c h a n g e the n u m b e r o f l e g s , h e a r t s o r l i v e r s o f a n a n i m a l b u t t h e effect o f stress on a plant is to alter both the rate of formation of n e w leaves a n d the rate of d e a t h o f o l d o n e s : a p l a n t m a y r e a c t t o stress b y v a r y i n g t h e n u m b e r o f its parts' (Harper 1 9 7 7 , p p . 2 0 - 2 1 ) . To H a r p e r , as a plant p o p u l a t i o n biologist, the l e a f m a y b e a m o r e s a l i e n t ' i n d i v i d u a l ' t h a n ' t h e p l a n t ' , s i n c e t h e p l a n t i s a s t r a g g l i n g , v a g u e e n t i t y for w h o m r e p r o d u c t i o n m a y b e h a r d t o d i s t i n g u i s h from w h a t a z o o l o g i s t w o u l d h a p p i l y c a l l ' g r o w t h ' . H a r p e r feels o b l i g e d t o coin
two
new
t e r m s for different
kinds of 'individual'
in
botany.
'The
254
R e d i s c o v e r i n g the O r g a n i s m
" r a m e t " i s t h e u n i t o f c l o n a l g r o w t h , t h e m o d u l e t h a t m a y often f o l l o w a n i n d e p e n d e n t e x i s t e n c e i f s e v e r e d f r o m the p a r e n t p l a n t . ' S o m e t i m e s , a s i n strawberries, the r a m e t is the unit that we ordinarily call a 'plant'. In other c a s e s s u c h a s w h i t e c l o v e r t h e r a m e t m a y b e t h e s i n g l e leaf. T h e ' g e n e t ' , o n t h e o t h e r h a n d , i s t h e u n i t w h i c h s p r i n g s f r o m o n e s i n g l e - c e l l e d z y g o t e , the ' i n d i v i d u a l ' in the sense of a zoologist w h o s e a n i m a l s r e p r o d u c e sexually. J a n z e n ( 1 9 7 7 ) faces up to the s a m e difficulty, suggesting that a clone of dandelions should be regarded as one 'evolutionary individual'
(Harper's
g e n e t ) , e q u i v a l e n t t o a s i n g l e tree a l t h o u g h s p r e a d o u t a l o n g t h e g r o u n d rather than raised up in the air on a trunk, and a l t h o u g h d i v i d e d up into s e p a r a t e p h y s i c a l ' p l a n t s ' ( H a r p e r ' s r a m e t s ) . A c c o r d i n g t o this v i e w , t h e r e m a y b e a s f e w a s f o u r i n d i v i d u a l d a n d e l i o n s c o m p e t i n g w i t h e a c h o t h e r for t h e t e r r i t o r y o f t h e w h o l e o f N o r t h A m e r i c a . J a n z e n sees a c l o n e o f a p h i d s i n the s a m e w a y . H i s p a p e r has no literature citations at all, but the v i e w is not a n e w o n e . I t g o e s b a c k a t least a s far a s 1 8 5 4 , w h e n T . H . H u x l e y ' t r e a t e d e a c h life c y c l e a s a n i n d i v i d u a l , w i t h a l l t h e p r o d u c t s f r o m s e x u a l e v e n t t o sexual event b e i n g a single unit. He even treated an asexual lineage of aphids a s a n i n d i v i d u a l ' ( G h i s e l i n i n p r e s s ) . T h e r e i s m e r i t i n this w a y o f t h i n k i n g , but I shall show that it leaves out something important. O n e w a y to re-express the H u x l e y / J a n z e n a r g u m e n t is as follows. T h e g e r m - l i n e of a t y p i c a l o r g a n i s m , say a h u m a n , goes t h r o u g h a sequence of perhaps a few d o z e n mitotic divisions b e t w e e n each meiosis. E m p l o y i n g C h a p t e r 5's ' b a c k w a r d s ' w a y o f l o o k i n g a t t h e ' p a s t e x p e r i e n c e o f a g e n e ' , a n y g i v e n g e n e in a living h u m a n has a history of cell divisions as follows: meiosis
mitosis
mitosis . . . mitosis
meiosis.
In
every
successive
body,
in
parallel w i t h the mitotic division of the g e r m - l i n e , other mitotic divisions h a v e furnished the g e r m - l i n e with a large clone of 'helper' cells, grouped together into a b o d y in w h i c h the germ-line is housed. In every generation the g e r m - l i n e is funnelled d o w n into a one-celled ' b o t t l e n e c k '
(a g a m e t e
f o l l o w e d b y a z y g o t e ) , t h e n i t fans o u t i n t o a m a n y - c e l l e d b o d y , t h e n i t i s funnelled d o w n into a n e w bottleneck, etc. (Bonner 1 9 7 4 ) . T h e m a n y - c e l l e d b o d y i s a m a c h i n e for t h e p r o d u c t i o n o f s i n g l e - c e l l e d p r o p a g u l e s . L a r g e b o d i e s , l i k e e l e p h a n t s , a r e best s e e n a s h e a v y p l a n t a n d m a c h i n e r y , a t e m p o r a r y resource drain, invested in so as to i m p r o v e later propagule production (Southwood
1 9 7 6 ) . I n a sense t h e g e r m - l i n e w o u l d
'like' to r e d u c e c a p i t a l i n v e s t m e n t in h e a v y m a c h i n e r y , r e d u c e the n u m b e r of cell divisions in the g r o w t h part of the c y c l e , so as to r e d u c e the interval b e t w e e n r e c u r r e n c e o f t h e r e p r o d u c t i o n p a r t o f t h e c y c l e . B u t this r e c u r r e n c e i n t e r v a l h a s a n o p t i m a l l e n g t h w h i c h i s d i f f e r e n t for d i f f e r e n t w a y s o f life. G e n e s that caused elephants to reproduce w h e n too y o u n g and small w o u l d propagate
themselves
less
efficiently than alleles
tending to produce an
o p t i m a l r e c u r r e n c e i n t e r v a l . T h e o p t i m a l r e c u r r e n c e i n t e r v a l for g e n e s t h a t h a p p e n t o f i n d t h e m s e l v e s i n e l e p h a n t g e n e - p o o l s i s m u c h l o n g e r t h a n the
R e d i s c o v e r i n g the O r g a n i s m
255
o p t i m a l r e c u r r e n c e i n t e r v a l for g e n e s i n m o u s e g e n e - p o o l s . I n t h e e l e p h a n t case, m o r e c a p i t a l i n v e s t m e n t is required to be laid d o w n before returns on investment are sought. A p r o t o z o a n largely dispenses w i t h the g r o w t h phase o f t h e c y c l e a l t o g e t h e r , a n d its c e l l d i v i s i o n s a r e a l l ' r e p r o d u c t i v e ' c e l l divisions. I t f o l l o w s f r o m this w a y o f l o o k i n g a t o r g a n i s m s t h a t t h e e n d p r o d u c t , t h e ' g o a l ' o f the g r o w t h phase o f the c y c l e , i s r e p r o d u c t i o n . T h e m i t o t i c cell divisions w h i c h p u t together an e l e p h a n t are all d i r e c t e d to the end of finally propagating viable gametes w h i c h succeed in p e r p e t u a t i n g the germ-line. N o w , h o l d i n g this i n m i n d , l o o k a t a p h i d s . D u r i n g t h e s u m m e r , a s e x u a l females g o t h r o u g h r e p e a t e d g e n e r a t i o n s o f a s e x u a l r e p r o d u c t i o n c u l m i n a t i n g i n a s i n g l e s e x u a l g e n e r a t i o n w h i c h restarts t h e c y c l e . C l e a r l y , b y a n a l o g y with the e l e p h a n t , it is easy to follow J a n z e n in seeing the s u m m e r a s e x u a l g e n e r a t i o n s a s a l l d i r e c t e d t o w a r d s t h e final e n d o f s e x u a l r e p r o d u c t i o n i n a u t u m n . A s e x u a l r e p r o d u c t i o n , a c c o r d i n g t o this v i e w , i s n o t r e a l l y r e p r o duction at all. It is g r o w t h , just like the g r o w t h of a single e l e p h a n t ' s b o d y . For J a n z e n the w h o l e clone of female a p h i d s is a single e v o l u t i o n a r y indiv i d u a l because it is the p r o d u c t of a single sexual fusion. It is an u n u s u a l individual in that it h a p p e n s to be split up into a n u m b e r of p h y s i c a l l y s e p a r a t e u n i t s , b u t s o w h a t ? E a c h o f t h o s e p h y s i c a l u n i t s c o n t a i n s its o w n f r a g m e n t o f g e r m - l i n e , b u t t h e n s o d o e s t h e left o v a r y a n d t h e r i g h t o v a r y o f a female elephant. T h e fragments of g e r m - l i n e in the a p h i d case are s e p a r a t e d b y thin air, w h i l e t h e t w o o v a r i e s o f a n e l e p h a n t a r e s e p a r a t e d b y g u t s b u t , again, so w h a t ? P e r s u a s i v e a s this l i n e o f a r g u m e n t is, I h a v e a l r e a d y m e n t i o n e d t h a t I t h i n k i t misses a n i m p o r t a n t p o i n t . I t i s r i g h t t o r e g a r d m o s t m i t o t i c c e l l divisions as ' g r o w t h ' , ' a i m e d ' at the final g o a l of r e p r o d u c t i o n , a n d it is right t o r e g a r d the i n d i v i d u a l o r g a n i s m a s t h e p r o d u c t o f o n e r e p r o d u c t i v e e v e n t , but J a n z e n is w r o n g to e q u a t e the r e p r o d u c t i o n / g r o w t h distinction w i t h the s e x u a l / a s e x u a l d i s t i n c t i o n . T h e r e is, t o b e s u r e , a n i m p o r t a n t d i s t i n c t i o n lurking here, but it is not the distinction b e t w e e n sex a n d non-sex, nor is it the distinction b e t w e e n meiosis a n d mitosis. T h e distinction that I wish to emphasize is that b e t w e e n germ-line cell division (reproduction), and somatic or ' d e a d - e n d ' cell division ( g r o w t h ) . A germ-line cell division is one w h e r e the genes b e i n g d u p l i c a t e d h a v e a c h a n c e o f b e i n g the a n c e s t o r s o f a n i n d e f i n i t e l y l o n g l i n e o f d e s c e n d a n t s , w h e r e t h e genes are, in fact, true g e r m - l i n e replicators in the sense of C h a p t e r 5. A germ-line cell division m a y be a mitosis or a meiosis. If we s i m p l y look at a cell division u n d e r a m i c r o s c o p e , there m a y be no w a y of telling w h e t h e r it is a germ-line division or not. Both germ-line and somatic cell divisions m a y be mitoses o f i d e n t i c a l a p p e a r a n c e . I f w e l o o k a t a g e n e i n a n y c e l l i n a l i v i n g o r g a n i s m a n d t r a c e its h i s t o r y b a c k w a r d s i n e v o l u t i o n a r y t i m e , t h e m o s t r e c e n t f e w c e l l d i v i s i o n s o f its
256
R e d i s c o v e r i n g the O r g a n i s m
' e x p e r i e n c e ' m a y be somatic, but once we reach a g e r m - l i n e cell division in o u r b a c k w a r d s m a r c h , a l l p r e v i o u s o n e s i n the g e n e ' s h i s t o r y m u s t b e g e r m line divisions. G e r m - l i n e cell divisions m a y be thought of as proceeding forwards in evolutionary time, while somatic cell divisions are proceeding s i d e w a y s . S o m a t i c c e l l d i v i s i o n s a r e u s e d t o m a k e m o r t a l tissues, o r g a n s a n d instruments w h o s e ' p u r p o s e ' is the p r o m o t i n g of g e r m - l i n e cell divisions. T h e world
is
populated
by
genes
which
have survived
in
germ-lines
as
a
c o n s e q u e n c e of aid that they r e c e i v e d from their e x a c t d u p l i c a t e s in somatic cells. G r o w t h c o m e s a b o u t t h r o u g h the p r o p a g a t i o n o f d e a d - e n d somatic cells, w h i l e r e p r o d u c t i o n is the m e a n s of the p r o p a g a t i o n of g e r m - l i n e cells. H a r p e r (1977) makes a distinction between reproduction and growth in plants, w h i c h w i l l n o r m a l l y a m o u n t to the s a m e as my distinction b e t w e e n germ-line and somatic cell division:
' T h e distinction m a d e here between
" r e p r o d u c t i o n " a n d " g r o w t h " is that r e p r o d u c t i o n involves the formation of a n e w i n d i v i d u a l f r o m a s i n g l e c e l l : this i s u s u a l l y ( t h o u g h n o t a l w a y s e . g . a p o m i c t s ) a z y g o t e . I n this p r o c e s s a n e w i n d i v i d u a l i s " r e p r o d u c e d " b y the i n f o r m a t i o n t h a t i s c o d e d i n t h e c e l l . G r o w t h , i n c o n t r a s t , results from the development
of organized
meristems'
(Harper
1977,
p.
27
fn.).
What
matters here is w h e t h e r there really is an important biological distinction b e t w e e n g r o w t h a n d r e p r o d u c t i o n w h i c h is not the same as the distinction between
mitosis
and
meiosis + sex.
Is
there
really
a
crucial
difference
b e t w e e n ' r e p r o d u c i n g ' t o m a k e t w o aphids o n the o n e h a n d , and ' g r o w i n g ' t o m a k e o n e a p h i d t w i c e a s l a r g e o n t h e o t h e r ? J a n z e n w o u l d p r e s u m a b l y say no. H a r p e r w o u l d p r e s u m a b l y say yes. I a g r e e w i t h H a r p e r , but I w o u l d not h a v e b e e n a b l e to justify my position until I had read J. T. Bonner's (1974) i n s p i r i n g b o o k O n Development. T h e j u s t i f i c a t i o n i s best m a d e w i t h t h e aid o f thought experiments. I m a g i n e a p r i m i t i v e p l a n t c o n s i s t i n g o f a flat, p a d - l i k e t h a l l u s , f l o a t i n g o n t h e s u r f a c e o f t h e s e a , a b s o r b i n g n u t r i e n t s t h r o u g h its l o w e r s u r f a c e a n d s u n l i g h t t h r o u g h its u p p e r s u r f a c e . I n s t e a d o f ' r e p r o d u c i n g ' (i.e. s e n d i n g off s i n g l e - c e l l e d p r o p a g u l e s t o g r o w e l s e w h e r e ) , i t s i m p l y g r o w s a t its m a r g i n s , s p r e a d i n g i n t o a n e v e r l a r g e r c i r c u l a r g r e e n c a r p e t , l i k e a m o n s t r o u s lily p a d s e v e r a l m i l e s a c r o s s a n d still g r o w i n g .
M a y b e older parts of the thallus
e v e n t u a l l y die, so that it consists of an e x p a n d i n g r i n g rather than a filled c i r c l e l i k e a t r u e l i l y p a d . P e r h a p s a l s o , f r o m t i m e t o t i m e , c h u n k s o f the t h a l l u s s p l i t off, l i k e i c e f l o e s s h e a r i n g a w a y f r o m t h e p a c k i c e , a n d s e p a r a t e c h u n k s drift t o d i f f e r e n t p a r t s o f t h e o c e a n . E v e n i f w e a s s u m e this k i n d o f fission, I s h a l l s h o w t h a t it is n o t r e p r o d u c t i o n in an i n t e r e s t i n g sense. N o w c o n s i d e r a s i m i l a r k i n d o f p l a n t w h i c h differs i n o n e c r u c i a l r e s p e c t . I t s t o p s g r o w i n g w h e n i t a t t a i n s a d i a m e t e r o f 1 foot, a n d r e p r o d u c e s i n s t e a d . It manufactures single-celled propagules, either sexually or asexually, and sheds t h e m into the air w h e r e they m a y be carried a l o n g w a y on the w i n d . W h e n o n e o f t h e s e p r o p a g u l e s l a n d s o n the w a t e r s u r f a c e i t b e c o m e s a n e w
R e d i s c o v e r i n g the O r g a n i s m
257
t h a l l u s , w h i c h g r o w s u n t i l i t i s 1 foot w i d e , t h e n r e p r o d u c e s a g a i n . I s h a l l c a l l the t w o s p e c i e s G (for g r o w t h ) a n d R (for r e p r o d u c t i o n ) r e s p e c t i v e l y . F o l l o w i n g t h e l o g i c o f J a n z e n ' s p a p e r , w e s h o u l d see a c r u c i a l d i f f e r e n c e b e t w e e n the t w o s p e c i e s o n l y i f t h e ' r e p r o d u c t i o n ' o f t h e s e c o n d s p e c i e s , R , i s sexual.
If it is asexual,
the propagules shed into the air b e i n g mitotic
p r o d u c t s g e n e t i c a l l y i d e n t i c a l t o t h e c e l l s o f t h e p a r e n t t h a l l u s , t h e r e is, for Janzen,
no i m p o r t a n t difference
between
the
two
species.
The
separate
'individuals' in R are no m o r e g e n e t i c a l l y distinct than different regions of the t h a l l u s i n G m i g h t b e . I n e i t h e r s p e c i e s , m u t a t i o n c a n i n i t i a t e n e w c l o n e s of cells. T h e r e is no p a r t i c u l a r reason w h y , in R, m u t a t i o n s s h o u l d o c c u r during propagule formation any more than during thallus g r o w t h .
R is
simply a m o r e fragmented version of G, just as a c l o n e of d a n d e l i o n s is like a fragmented tree. M y purpose i n m a k i n g the t h o u g h t e x p e r i m e n t , h o w e v e r , was to disclose an i m p o r t a n t difference b e t w e e n the t w o h y p o t h e t i c a l species, representing the difference b e t w e e n g r o w t h a n d r e p r o d u c t i o n , e v e n w h e n r e p r o d u c t i o n is a s e x u a l . G just grows, while R g r o w s and reproduces in alternation. W h y is the distinction i m p o r t a n t ? T h e answer cannot be a genetic one in a n y simple sense b e c a u s e , a s w e h a v e s e e n , m u t a t i o n s a r e j u s t a s l i k e l y t o i n i t i a t e g e n e t i c change during growth-mitosis as d u r i n g reproduction-mitosis. I suggest that the i m p o r t a n t d i s t i n c t i o n b e t w e e n t h e t w o s p e c i e s i s t h a t a l i n e a g e o f R i s capable of evolving c o m p l e x adaptations in a w a y
that G is not. T h e
reasoning goes as follows. C o n s i d e r a g a i n t h e p a s t h i s t o r y of a g e n e , in this c a s e a g e n e s i t t i n g in a cell o f R . I t h a s h a d a h i s t o r y o f p a s s i n g r e p e a t e d l y f r o m o n e ' v e h i c l e ' t o a n o t h e r s i m i l a r v e h i c l e . E a c h o f its s u c c e s s i v e b o d i e s b e g a n a s a s i n g l e - c e l l e d propagule, then g r e w through a fixed c y c l e , then passed the g e n e on into a n e w s i n g l e - c e l l e d p r o p a g u l e a n d h e n c e a n e w m u l t i c e l l u l a r b o d y . Its h i s t o r y h a s b e e n a c y c l i c a l o n e , a n d n o w h e r e i s t h e p o i n t . S i n c e e a c h o f this l o n g series o f s u c c e s s i v e b o d i e s d e v e l o p e d a n e w f r o m s i n g l e - c e l l e d b e g i n n i n g s , i t i s possible
for
predecessors.
successive Evolution
bodies
to
develop
of complex
body
slightly structure
differently with
from
organs,
their say
a
c o m p l e x a p p a r a t u s for c a t c h i n g i n s e c t s like a V e n u s fly t r a p , i s o n l y p o s s i b l e if t h e r e is a c y c l i c a l l y r e p e a t i n g d e v e l o p m e n t a l p r o c e s s to e v o l v e . I s h a l l r e t u r n to this p o i n t in a m o m e n t . M e a n w h i l e , c o m p a r e G. A g e n e sitting in a y o u n g cell at the g r o w i n g m a r g i n of the h u g e thallus has a history w h i c h is not c y c l i c a l , or is c y c l i c a l only at the cellular level. T h e ancestor of the present cell w a s a n o t h e r cell, a n d the c a r e e r o f t h e t w o c e l l s w a s v e r y s i m i l a r . E a c h c e l l o f a n R p l a n t , b y contrast, has a definite place in the g r o w t h sequence. It is either n e a r the c e n t r e o f t h e 1-foot t h a l l u s , o r n e a r t h e r i m , o r a t s o m e p a r t i c u l a r p l a c e i n b e t w e e n . I t c a n t h e r e f o r e d i f f e r e n t i a t e t o f i l l its s p e c i a l r o l e i n its a p p o i n t e d p l a c e i n a n o r g a n o f the p l a n t . A c e l l o f G h a s n o s u c h s p e c i f i c d e v e l o p m e n t a l
258
R e d i s c o v e r i n g the O r g a n i s m
identity.
All
cells
first
appear
at
the
growing
margin,
and
later find
t h e m s e l v e s e n c l o s e d b y o t h e r , y o u n g e r c e l l s . T h e r e i s c y c l i c i t y o n l y a t the cellular level, w h i c h m e a n s that in G evolutionary c h a n g e can take place o n l y a t t h e c e l l u l a r l e v e l . C e l l s m i g h t i m p r o v e o n t h e i r p r e d e c e s s o r s i n the cell lineage, d e v e l o p i n g more c o m p l e x internal organelle structure, say. But t h e e v o l u t i o n o f o r g a n s a n d a d a p t a t i o n s a t t h e m u l t i c e l l u l a r l e v e l c o u l d not t a k e p l a c e , b e c a u s e r e c u r r e n t , c y c l i c a l d e v e l o p m e n t o f w h o l e g r o u p s o f cells d o e s n o t o c c u r . I t is, o f c o u r s e , t r u e t h a t i n G t h e c e l l s a n d t h e i r a n c e s t o r s a r e i n p h y s i c a l c o n t a c t w i t h o t h e r c e l l s , a n d i n this sense f o r m a m u l t i c e l l u l a r ' s t r u c t u r e ' . B u t a s far a s p u t t i n g t o g e t h e r c o m p l e x m u l t i c e l l u l a r o r g a n s i s concerned, they might just as well have been free-swimming protozoa. In order
to
put
together
a
complex
multicellular organ
you
need
a
c o m p l e x d e v e l o p m e n t a l s e q u e n c e . A c o m p l e x d e v e l o p m e n t a l s e q u e n c e has t o h a v e e v o l v e d f r o m a n e a r l i e r d e v e l o p m e n t a l s e q u e n c e w h i c h w a s s l i g h t l y less c o m p l e x . T h e r e has to be an evolutionary progression of developmental sequences,
each
one
in
the
series
being
a
slight
improvement
on
its
predecessor. G does not h a v e a recurring d e v e l o p m e n t a l sequence other than t h e h i g h - f r e q u e n c y c y c l e o f d e v e l o p m e n t a t the s i n g l e - c e l l l e v e l . T h e r e f o r e i t c a n n o t e v o l v e multicellular differentiation and organ-level complexity. T o t h e e x t e n t t h a t i t c a n b e s a i d t o h a v e a m u l t i c e l l u l a r d e v e l o p m e n t a l process at all, that d e v e l o p m e n t continues non-cyclically through geological time: the species m a k e s no s e p a r a t i o n b e t w e e n would-be cycle
evolution
available
to
time-scale. it
is
the
The
cell
only
cycle.
the g r o w t h
time-scale and
high-frequency R,
on
the
the
developmental
other
hand,
has
a
m u l t i c e l l u l a r d e v e l o p m e n t a l c y c l e w h i c h i s fast c o m p a r e d w i t h e v o l u t i o n a r y time. T h e r e f o r e , as the ages succeed, later d e v e l o p m e n t a l cycles can be different from earlier d e v e l o p m e n t a l cycles, a n d m u l t i c e l l u l a r c o m p l e x i t y c a n e v o l v e . W e a r e m o v i n g t o w a r d s a d e f i n i t i o n o f t h e o r g a n i s m a s the u n i t which
is
initiated
developmental
by
a
new
act
of
reproduction
via
a
single-celled
'bottleneck'.
T h e i m p o r t a n c e of the difference b e t w e e n g r o w t h and reproduction is that each act of reproduction involves a new developmental cycle. G r o w t h simply i n v o l v e s s w e l l i n g o f t h e e x i s t i n g b o d y . W h e n a n a p h i d g i v e s rise t o a n e w aphid by parthenogenetic reproduction the n e w aphid, if it is a mutant, m a y b e r a d i c a l l y d i f f e r e n t f r o m its p r e d e c e s s o r . W h e n a n a p h i d g r o w s t o t w i c e its o r i g i n a l s i z e , o n t h e o t h e r h a n d , a l l its o r g a n s a n d c o m p l e x s t r u c t u r e s s i m p l y swell.
It might
be said
that somatic mutations could
o c c u r within cell
lineages of the g r o w i n g giant aphid. T r u e , but a mutation within a somatic c e l l l i n e i n a h e a r t , s a y , c a n n o t r a d i c a l l y r e - o r g a n i z e t h e s t r u c t u r e o f the h e a r t . T o s w i t c h t h e e x a m p l e t o v e r t e b r a t e s , i f the p r e s e n t h e a r t i s t w o c h a m b e r e d , w i t h o n e a u r i c l e f e e d i n g o n e v e n t r i c l e , n e w m u t a t i o n s i n the m i t o t i c cells at the g r o w i n g m a r g i n of the heart are v e r y unlikely to a c h i e v e r a d i c a l r e s t r u c t u r i n g o f t h e h e a r t s o t h a t i t c o m e s t o h a v e four c h a m b e r s w i t h
R e d i s c o v e r i n g the O r g a n i s m
259
a p u l m o n a r y c i r c u l a t i o n k e p t s e p a r a t e f r o m t h e rest. I n o r d e r t o p u t t o g e t h e r new complexity, n e w d e v e l o p m e n t a l beginnings are required. A n e w e m b r y o m u s t start f r o m s c r a t c h , w i t h o u t a n y h e a r t a t a l l . T h e n a m u t a t i o n c a n a c t o n sensitive key points in e a r l y d e v e l o p m e n t to b r i n g a b o u t a n e w f u n d a m e n t a l architecture of the heart. D e v e l o p m e n t a l r e c y c l i n g a l l o w s a return ' b a c k to t h e d r a w i n g b o a r d ' (see b e l o w ) i n e v e r y g e n e r a t i o n . W e b e g a n this c h a p t e r b y w o n d e r i n g w h y r e p l i c a t o r s h a v e g a n g e d u p i n t o large, multicellular clones called organisms, and we initially g a v e a rather unsatisfactory answer. A m o r e satisfying a n s w e r is n o w starting to e m e r g e . A n o r g a n i s m i s t h e p h y s i c a l u n i t a s s o c i a t e d w i t h o n e s i n g l e life c y c l e . Replicators that g a n g up in multicellular organisms a c h i e v e a regularly r e c y c l i n g life h i s t o r y , a n d c o m p l e x a d a p t a t i o n s t o a i d t h e i r p r e s e r v a t i o n , a s they progress through e v o l u t i o n a r y time. S o m e a n i m a l s h a v e a life c y c l e i n v o l v i n g m o r e t h a n o n e d i s t i n c t b o d y . A b u t t e r f l y i s u t t e r l y d i f f e r e n t f r o m t h e c a t e r p i l l a r w h i c h p r e c e d e d it. I t i s h a r d to i m a g i n e a butterfly g r o w i n g from a caterpillar by slow, w i t h i n - o r g a n change:
caterpillar
organ
growing
into
corresponding
butterfly
organ.
Instead, w h a t h a p p e n s is that the c o m p l e x o r g a n structure of the c a t e r p i l l a r i s l a r g e l y b r o k e n d o w n a n d t h e tissues o f t h e c a t e r p i l l a r a r e u s e d a s fuel for the d e v e l o p m e n t o f a w h o l e n e w b o d y . T h e n e w b u t t e r f l y b o d y d o e s n o t q u i t e restart f r o m a s i n g l e c e l l , b u t t h e p r i n c i p l e i s t h e s a m e . I t d e v e l o p s a radically
new
bodily
structure
from
simple,
relatively
undifferentiated
i m a g i n a l discs. T h e r e is a partial return to the d r a w i n g b o a r d . R e t u r n i n g t o t h e g r o w t h / r e p r o d u c t i o n d i s t i n c t i o n itself, J a n z e n w a s n o t a c t u a l l y w r o n g . D i s t i n c t i o n s c a n b e u n i m p o r t a n t for s o m e p u r p o s e s , w h i l e t h e y r e m a i n i m p o r t a n t for o t h e r p u r p o s e s . F o r d i s c u s s i n g c e r t a i n k i n d s o f ecological or economic questions, there m a y be no i m p o r t a n t distinction between
growth
and
asexual
reproduction.
A
sisterhood
of aphids
may
i n d e e d b e a n a l o g o u s t o a s i n g l e b e a r . B u t for o t h e r p u r p o s e s , for d i s c u s s i n g the e v o l u t i o n a r y p u t t i n g t o g e t h e r o f c o m p l e x o r g a n i z a t i o n , t h e d i s t i n c t i o n i s crucial. A certain type of ecologist m a y gain illumination from c o m p a r i n g a field full o f d a n d e l i o n s w i t h a s i n g l e t r e e . important to u n d e r s t a n d the differences,
B u t for o t h e r p u r p o s e s i t i s
a n d t o see t h e s i n g l e d a n d e l i o n
r a m e t as a n a l o g o u s to the tree. B u t J a n z e n ' s p o s i t i o n is, i n a n y c a s e , a m i n o r i t y o n e . A m o r e t y p i c a l biologist m i g h t think it perverse of J a n z e n to r e g a r d a s e x u a l r e p r o d u c t i o n in aphids
as
vegetative
growth,
and
propagation
equally by
perverse
multicellular
of Harper runners,
and as
me
growth
to
regard
and
not
reproduction. O u r decision is based on the assumption that the r u n n e r is a multicellular meristem rather than a single-celled propagule, but w h y should w e r e g a r d this a s a n i m p o r t a n t p o i n t ? A g a i n , t h e a n s w e r m a y b e s e e n i n a t h o u g h t e x p e r i m e n t i n v o l v i n g t w o h y p o t h e t i c a l s p e c i e s o f p l a n t s , i n this c a s e s t r a w b e r r y - l i k e p l a n t s c a l l e d M a n d S ( D a w k i n s in p r e s s ) .
260
R e d i s c o v e r i n g the O r g a n i s m
B o t h the h y p o t h e t i c a l s t r a w b e r r y - l i k e species p r o p a g a t e v e g e t a t i v e l y , by runner.
In both
there is a p o p u l a t i o n of w h a t a p p e a r to be distinct and
r e c o g n i z a b l e ' p l a n t s ' c o n n e c t e d by a n e t w o r k of runners. In both species, e a c h ' p l a n t ' ( i . e . r a m e t ) c a n g i v e rise t o m o r e t h a n o n e d a u g h t e r p l a n t , s o that w e h a v e the possibility o f e x p o n e n t i a l g r o w t h o f the ' p o p u l a t i o n '
(or
g r o w t h o f the ' b o d y ' d e p e n d i n g o n y o u r point o f v i e w ) . E v e n t h o u g h there i s n o s e x , t h e r e c a n b e e v o l u t i o n s i n c e m u t a t i o n s w i l l s o m e t i m e s o c c u r i n the m i t o t i c c e l l d i v i s i o n s ( W h i t h a m & S l o b o d c h i k o f f i n p r e s s ) . N o w c o m e s the crucial difference b e t w e e n the t w o species. multicellular,
or
meristem),
the
runner
is
In species M a
(for m a n y , o r
broad-fronted
multicellular
m e r i s t e m . T h i s m e a n s t h a t t w o c e l l s i n a n y o n e ' p l a n t ' m a y b e the m i t o t i c descendants of t w o different cells in the p a r e n t plant.
In terms of mitotic
descent, a cell m a y therefore be a closer cousin of a cell in a n o t h e r 'plant' t h a n i t i s o f a n o t h e r c e l l i n its o w n p l a n t . I f m u t a t i o n h a s i n t r o d u c e d g e n e t i c h e t e r o g e n e i t y i n t o t h e c e l l p o p u l a t i o n , this m e a n s t h a t i n d i v i d u a l p l a n t s m a y be g e n e t i c m o s a i c s , w i t h s o m e cells h a v i n g closer genetic relatives in other p l a n t s t h a n i n t h e i r o w n . W e w i l l see t h e c o n s e q u e n c e s o f this for e v o l u t i o n i n a m o m e n t . M e a n w h i l e we turn to the other h y p o t h e t i c a l species. S p e c i e s S (for s i n g l e ) i s e x a c t l y l i k e M , e x c e p t t h a t e a c h r u n n e r c u l m i n a t e s i n a s i n g l e a p i c a l c e l l . T h i s c e l l a c t s a s t h e b a s a l m i t o t i c a n c e s t o r o f a l l the c e l l s o f t h e n e w d a u g h t e r p l a n t . T h i s m e a n s t h a t a l l cells i n a g i v e n p l a n t a r e closer cousins to e a c h other t h a n t h e y are to a n y cells in other plants. If m u t a t i o n i n t r o d u c e s g e n e t i c h e t e r o g e n e i t y into the p o p u l a t i o n of cells, there will be relatively few mosaic plants. R a t h e r , each plant will tend to be a g e n e t i c a l l y u n i f o r m c l o n e , b u t i t m a y differ g e n e t i c a l l y f r o m s o m e o t h e r plants, w h i l e b e i n g genetically identical to yet other plants. T h e r e will be a t r u e p o p u l a t i o n o f plants, e a c h o n e o f w h i c h has a g e n o t y p e c h a r a c t e r i s t i c o f a l l its c e l l s . I t i s t h e r e f o r e p o s s i b l e t o c o n c e i v e o f s e l e c t i o n , i n t h e sense w h i c h I h a v e c a l l e d ' v e h i c l e selection', a c t i n g at the level of the w h o l e plant. S o m e w h o l e plants m a y be better than others, because of their superior genotypes. In species M, especially if the runners are very broad-fronted meristems, a geneticist will not discern a p o p u l a t i o n of plants at all.
H e w i l l see a
p o p u l a t i o n o f c e l l s , e a c h w i t h its o w n g e n o t y p e . S o m e c e l l s w i l l b e g e n e t i c a l l y i d e n t i c a l , o t h e r s w i l l h a v e different g e n o t y p e s . A f o r m o f n a t u r a l s e l e c t i o n m i g h t go on a m o n g cells, but it is hard to i m a g i n e selection a m o n g 'plants', b e c a u s e ' t h e p l a n t ' i s n o t a u n i t t h a t c a n b e i d e n t i f i e d a s h a v i n g its o w n characteristic g e n o t y p e . R a t h e r , the w h o l e mass o f s t r a g g l i n g v e g e t a t i o n will h a v e to be r e g a r d e d as a p o p u l a t i o n of cells, w i t h cells of a n y one g e n o t y p e b e i n g u n t i d i l y p e p p e r e d a c r o s s t h e different ' p l a n t s ' . T h e u n i t w h i c h I h a v e called the ' g e n e v e h i c l e ' , a n d w h i c h J a n z e n has called the ' e v o l u t i o n a r y i n d i v i d u a l ' , w i l l , i n s u c h a c a s e , b e n o l a r g e r t h a n t h e c e l l . I t i s cells t h a t w i l l be the g e n e t i c c o m p e t i t o r s . E v o l u t i o n m a y take the form of i m p r o v e m e n t s in c e l l s t r u c t u r e a n d p h y s i o l o g y , b u t i t i s h a r d t o see h o w i t c o u l d t a k e t h e form of i m p r o v e m e n t s in i n d i v i d u a l plants or their organs.
R e d i s c o v e r i n g the O r g a n i s m
261
It might be thought that i m p r o v e m e n t s in o r g a n structure c o u l d e v o l v e , if it regularly happened
that particular subpopulations of cells,
in discrete
a r e a s o f the p l a n t , w e r e a c l o n e , d e s c e n d e d f r o m a s i n g l e m i t o t i c a n c e s t o r . F o r i n s t a n c e , t h e r u n n e r g i v i n g rise t o a n e w ' p l a n t ' m i g h t b e a b r o a d - f r o n t e d m e r i s t e m , b u t i t m i g h t still b e t h e c a s e t h a t e a c h l e a f s p r a n g f r o m a s i n g l e c e l l a t its o w n b a s e . A l e a f c o u l d t h e r e f o r e b e a c l o n e o f c e l l s m o r e c l o s e l y r e l a t e d t o e a c h o t h e r t h a n t o c e l l s a n y w h e r e else i n t h e p l a n t . G i v e n t h e c o m m o n n e s s of somatic mutation in plants ( W h i t h a m & S l o b o d c h i k o f f in press), m i g h t one not therefore i m a g i n e the e v o l u t i o n of i m p r o v e d c o m p l e x a d a p t a t i o n at the l e v e l o f t h e leaf, i f n o t a t t h e l e v e l o f t h e w h o l e p l a n t ? A g e n e t i c i s t c o u l d now discern a genetically heterogeneous p o p u l a t i o n of leaves, e a c h one m a d e up of genetically h o m o g e n o u s cells, so m i g h t not natural selection go on b e t w e e n successful l e a v e s a n d u n s u c c e s s f u l l e a v e s ? I t w o u l d b e t i d y i f t h e a n s w e r t o this q u e s t i o n c o u l d b e y e s ; t h a t is, i f w e c o u l d assert t h a t v e h i c l e selection will go on at a n y level in the h i e r a r c h y of m u l t i c e l l u l a r units, provided
that
compared
the
with
cells
cells
within
in
other
a
unit
units
at
tend
to
the
be
same
genetically level.
uniform
Unfortunately,
h o w e v e r , s o m e t h i n g h a s b e e n left o u t o f t h e r e a s o n i n g . It
will
be
replicators
remembered
and
dead-end
that
I
classified
replicators.
Natural
replicators
into
selection
results
germ-line in
some
replicators b e c o m i n g m o r e n u m e r o u s at the e x p e n s e of rival replicators, b u t this l e a d s t o e v o l u t i o n a r y c h a n g e o n l y i f t h e r e p l i c a t o r s a r e i n g e r m - l i n e s . A m u l t i c e l l u l a r u n i t q u a l i f i e s a s a v e h i c l e , i n a n e v o l u t i o n a r i l y i n t e r e s t i n g sense, only
if at
normally
least do
replicators.
some
o f its
so
qualify,
not
L e a f cells
cells for
synthesize
contain their
germ-line nuclei
chemical
replicators.
contain
substances
only
which
Leaves
dead-end ultimately
benefit o t h e r c e l l s t h a t d o c o n t a i n g e r m - l i n e c o p i e s o f t h e l e a f g e n e s , t h e genes w h i c h g a v e the leaves their characteristically leafy p h e n o t y p e s . B u t we cannot
accept
the
conclusion of the
previous
paragraph,
that
inter-leaf
vehicle selection, a n d inter-organ selection g e n e r a l l y , c o u l d go on if o n l y the cells w i t h i n a n o r g a n w e r e c l o s e r m i t o t i c c o u s i n s t h a n c e l l s i n d i f f e r e n t organs.
Inter-leaf selection could h a v e evolutionary consequences only if
leaves directly s p a w n e d d a u g h t e r leaves. L e a v e s are organs, not organisms. For inter-organ selection to occur, it is necessary that the organs c o n c e r n e d s h o u l d h a v e t h e i r o w n g e r m l i n e s a n d d o t h e i r o w n r e p r o d u c i n g , a n d this they normally do not. O r g a n s are parts of organisms, and r e p r o d u c t i o n is the prerogative of organisms. For clarity
I
have
been
a bit
extreme.
There
could
be
a r a n g e of
intermediates between my two strawberry-like plants. Species M ' s runner w a s said to be a broad-fronted m e r i s t e m , w h i l e species S's r u n n e r n a r r o w e d d o w n to a one-celled bottleneck at the base of e a c h n e w plant. B u t w h a t if there w a s an i n t e r m e d i a t e species w i t h a t w o - c e l l e d b o t t l e n e c k at the base of e a c h n e w p l a n t ? T h e r e are t w o m a i n possibilities here.
If the pattern of
d e v e l o p m e n t is such that it is u n p r e d i c t a b l e w h i c h cells in the d a u g h t e r p l a n t
262
R e d i s c o v e r i n g the O r g a n i s m
will be d e s c e n d e d from w h i c h of the t w o stem cells, the point I h a v e m a d e about developmental bottlenecks will simply be weakened quantitatively: g e n e t i c m o s a i c s m a y o c c u r i n t h e p o p u l a t i o n o f p l a n t s , b u t t h e r e w i l l still b e a s t a t i s t i c a l t e n d e n c y for c e l l s t o b e g e n e t i c a l l y c l o s e r t o f e l l o w m e m b e r s o f t h e s a m e p l a n t t h a n t o c e l l s i n o t h e r p l a n t s . T h e r e f o r e w e m a y still t a l k meaningfully plants,
but
about vehicle selection the
inter-plant selection
between
plants in
pressure m a y
have
a population of to
be strong
to
o u t w e i g h s e l e c t i o n a m o n g c e l l s w i t h i n p l a n t s . T h i s is, i n c i d e n t a l l y , a n a l o g o u s t o o n e o f t h e c o n d i t i o n s for ' k i n - g r o u p s e l e c t i o n ' ( H a m i l t o n 1 9 7 5 a ) t o w o r k . T o m a k e t h e a n a l o g y , w e h a v e o n l y t o see t h e p l a n t a s a ' g r o u p ' o f c e l l s . The
second
possibility arising out
of the
assumption
of a
two-celled
b o t t l e n e c k a t t h e b a s e o f e a c h p l a n t i s t h a t t h e p a t t e r n o f d e v e l o p m e n t o f the species m i g h t be such that certain organs of the plant are a l w a y s the mitotic d e s c e n d a n t s o f a d e s i g n a t e d o n e o f t h e t w o c e l l s . F o r i n s t a n c e , c e l l s o f the root system m i g h t d e v e l o p from a cell in the l o w e r part of the runner, w h i l e t h e rest o f t h e p l a n t d e v e l o p e d f r o m t h e o t h e r c e l l , i n t h e u p p e r p a r t o f the r u n n e r . If, f u r t h e r , t h e l o w e r c e l l i s a l w a y s d e s c e n d e d f r o m a r o o t c e l l i n the p a r e n t plant, w h i l e the u p p e r cell is recruited from an a b o v e - g r o u n d cell in the p a r e n t p l a n t , w e w o u l d h a v e a n interesting situation. R o o t cells w o u l d b e closer cousins of o t h e r root cells in the p o p u l a t i o n at large than they w o u l d b e o f s t a l k a n d l e a f c e l l s i n t h e i r ' o w n ' p l a n t . M u t a t i o n w o u l d o p e n u p the possibility of e v o l u t i o n a r y c h a n g e , but it w o u l d be split-level evolution. G e n o t y p e s b e l o w g r o u n d c o u l d e v o l v e a w a y from g e n o t y p e s a b o v e g r o u n d , irrespective of a p p a r e n t joint m e m b e r s h i p in discrete 'plants'. Theoretically we could even have a kind of within-organism 'speciation'. To recapitulate, reproduction
is
the significance o f the difference b e t w e e n g r o w t h and that
reproduction
permits
a
new
beginning,
a
new
developmental cycle and a new organism which m a y be an improvement, in terms
of the
fundamental
organization
of complex
structure,
over
its
p r e d e c e s s o r . O f c o u r s e i t m a y not b e a n i m p r o v e m e n t , i n w h i c h c a s e its g e n e t i c basis w i l l b e e l i m i n a t e d b y n a t u r a l selection. B u t g r o w t h w i t h o u t r e p r o d u c t i o n d o e s n o t e v e n a l l o w the possibility o f r a d i c a l c h a n g e a t t h e o r g a n level, either in the direction of i m p r o v e m e n t or the reverse. It allows only s u p e r f i c i a l t i n k e r i n g . Y o u m a y d i v e r t a d e v e l o p i n g B e n t l e y i n t o a fully g r o w n R o l l s R o y c e , s i m p l y b y t i n k e r i n g w i t h t h e a s s e m b l y p r o c e s s a t the l a t e p o i n t w h e r e the r a d i a t o r is a d d e d . B u t if y o u w a n t to c h a n g e a F o r d into a R o l l s R o y c e y o u m u s t s t a r t a t t h e d r a w i n g b o a r d , b e f o r e t h e c a r starts ' g r o w i n g ' o n t h e a s s e m b l y l i n e a t a l l . T h e p o i n t a b o u t r e c u r r e n t r e p r o d u c t i o n life c y c l e s , a n d h e n c e , by i m p l i c a t i o n , the point a b o u t organisms, is that they a l l o w repeated returns to the d r a w i n g board during evolutionary time. W e must b e w a r e here o f the heresy o f 'biotic' a d a p t a t i o n i s m
(Williams
1 9 6 6 ) . W e h a v e s e e n t h a t r e c u r r e n t r e p r o d u c t i o n life c y c l e s , i.e. ' o r g a n i s m s ' , m a k e t h e e v o l u t i o n o f c o m p l e x o r g a n s p o s s i b l e . I t i s a l l t o o e a s y t o t r e a t this
R e d i s c o v e r i n g the O r g a n i s m
263
as a sufficient a d a p t i v e e x p l a n a t i o n for t h e existence of o r g a n i s m a l life c y c l e s , o n the g r o u n d s t h a t c o m p l e x o r g a n s a r e , i n s o m e v a g u e s e n s e , a g o o d i d e a . A related point is that repeated r e p r o d u c t i o n is possible o n l y if i n d i v i d u a l s die (Maynard
Smith
1969),
but we should
not
therefore wish
to say that
individuals die as an adaptation to keep evolution g o i n g ! T h e same could be said of m u t a t i o n : its e x i s t e n c e is a n e c e s s a r y p r e c o n d i t i o n for e v o l u t i o n to occur, but it is nevertheless quite likely that natural selection has favoured evolution
in
attained
the
direction
(Williams
1966).
of a The
zero
mutation
rate—fortunately
growth/reproduction/death
type
never o f life
c y c l e — t h e m u l t i c e l l u l a r c l o n a l ' o r g a n i s m ' t y p e o f life c y c l e — h a s h a d farreaching consequences
and
was probably
essential
for
the
evolution
of
a d a p t i v e c o m p l e x i t y , b u t this i s n o t t a n t a m o u n t t o a n a d a p t i v e e x p l a n a t i o n for the e x i s t e n c e o f this t y p e o f life c y c l e . T h e D a r w i n i a n m u s t b e g i n b y s e e k i n g i m m e d i a t e b e n e f i t s t o g e n e s p r o m o t i n g this k i n d o f life c y c l e , a t t h e expense o f their alleles. H e m a y g o o n t o a c k n o w l e d g e the possibility o f other levels of selection, differential l i n e a g e e x t i n c t i o n , say. B u t he m u s t s h o w the s a m e c i r c u m s p e c t i o n i n this difficult t h e o r e t i c a l f i e l d a s F i s h e r Williams (1975)
and M a y n a r d Smith (1978a)
suggestions a b o u t sexual
reproduction
(1930a),
b r o u g h t to the a n a l o g o u s
being there
because it speeds up
evolution. T h e organism has the f o l l o w i n g attributes. It is either a single cell, or if it is multicellular
its c e l l s a r e c l o s e g e n e t i c
kin
of e a c h other:
they are
descended from a single stem cell, w h i c h m e a n s that they h a v e a m o r e recent c o m m o n ancestor w i t h e a c h other than w i t h the cells o f a n y o t h e r o r g a n i s m . T h e o r g a n i s m i s a u n i t w i t h a life c y c l e w h i c h , h o w e v e r c o m p l i c a t e d i t m a y b e , r e p e a t s t h e e s s e n t i a l c h a r a c t e r i s t i c s o f p r e v i o u s life c y c l e s , a n d m a y b e a n i m p r o v e m e n t o n p r e v i o u s life c y c l e s . T h e o r g a n i s m e i t h e r c o n s i s t s o f g e r m line c e l l s , o r i t c o n t a i n s g e r m - l i n e c e l l s a s a s u b s e t o f its o w n c e l l s , o r , a s i n t h e c a s e of a sterile s o c i a l i n s e c t w o r k e r , it is in a p o s i t i o n to w o r k for t h e w e l f a r e o f g e r m - l i n e cells i n c l o s e l y r e l a t e d o r g a n i s m s . I h a v e n o t a s p i r e d in this final c h a p t e r to g i v e a c o m p l e t e l y s a t i s f y i n g a n s w e r t o the q u e s t i o n o f w h y t h e r e a r e l a r g e m u l t i c e l l u l a r o r g a n i s m s . I w i l l be content if I accepting
that
c a n arouse n e w curiosity a b o u t the question. organisms
exist
and
asking
how
adaptations
Instead of benefit
the
o r g a n i s m s d i s p l a y i n g t h e m , I h a v e tried t o s h o w t h a t t h e v e r y e x i s t e n c e o f o r g a n i s m s s h o u l d b e t r e a t e d a s a p h e n o m e n o n d e s e r v i n g o f e x p l a n a t i o n i n its o w n right. R e p l i c a t o r s exist. T h a t is f u n d a m e n t a l . P h e n o t y p i c manifestations of them, including extended phenotypic manifestations, m a y be expected to function complex
a s tools
to keep replicators existing.
assemblages
of such
tools,
Organisms are
assemblages
shared
by
huge and gangs
of
replicators w h o in principle need not h a v e g o n e a r o u n d t o g e t h e r but in fact do go a r o u n d together a n d share a c o m m o n interest in the survival a n d reproduction
of
the
organism.
As
well
as
drawing
attention
to
the
264
R e d i s c o v e r i n g the O r g a n i s m
p h e n o m e n o n o f t h e o r g a n i s m a s o n e t h a t n e e d s e x p l a n a t i o n , I h a v e tried i n this last c h a p t e r t o s k e t c h t h e g e n e r a l d i r e c t i o n i n w h i c h w e m i g h t p r o c e e d i n s e e k i n g a n e x p l a n a t i o n . I t i s o n l y a p r e l i m i n a r y s k e t c h , b u t , for w h a t i t i s w o r t h , I s u m m a r i z e it here. The
replicators
that
exist
tend
to
be
the
ones
that
are
good
at
m a n i p u l a t i n g t h e w o r l d t o t h e i r o w n a d v a n t a g e . I n d o i n g this t h e y e x p l o i t t h e o p p o r t u n i t i e s offered b y t h e i r e n v i r o n m e n t s , a n d a n i m p o r t a n t a s p e c t o f the e n v i r o n m e n t of a replicator is other replicators a n d their p h e n o t y p i c manifestations. T h o s e r e p l i c a t o r s are successful w h o s e beneficial p h e n o t y p i c effects a r e c o n d i t i o n a l u p o n t h e p r e s e n c e o f o t h e r r e p l i c a t o r s w h i c h h a p p e n t o b e c o m m o n . T h e s e o t h e r replicators are also successful, o t h e r w i s e they w o u l d not b e c o m m o n . T h e w o r l d therefore tends t o b e c o m e populated b y m u t u a l l y c o m p a t i b l e sets o f s u c c e s s f u l r e p l i c a t o r s , r e p l i c a t o r s t h a t g e t o n w e l l together.
I n p r i n c i p l e this a p p l i e s t o r e p l i c a t o r s i n different g e n e p o o l s ,
different species, classes, p h y l a a n d k i n g d o m s . B u t a relationship of specially i n t i m a t e m u t u a l c o m p a t i b i l i t y has g r o w n u p b e t w e e n subsets o f replicators that share cell nuclei a n d , w h e r e the existence of s e x u a l r e p r o d u c t i o n makes the expression m e a n i n g f u l , share gene-pools. T h e cell n u c l e u s as a p o p u l a t i o n of uneasily c o h a b i t i n g replicators is a r e m a r k a b l e p h e n o m e n o n i n itself. J u s t a s r e m a r k a b l e , a n d q u i t e d i s t i n c t , i s the p h e n o m e n o n o f m u l t i c e l l u l a r c l o n i n g , the p h e n o m e n o n o f the multicellular
organism.
replicators
to
Replicators produce
whose
effects
multicellular
interact
organisms
with
achieve
those for
of other
themselves
vehicles w i t h c o m p l e x organs and behaviour patterns. C o m p l e x organs and b e h a v i o u r patterns are favoured in arms races. T h e evolution of complex organs a n d b e h a v i o u r patterns is possible b e c a u s e the o r g a n i s m is an entity w i t h a r e c u r r e n t life c y c l e , e a c h c y c l e b e g i n n i n g w i t h a s i n g l e c e l l . T h e f a c t that each cycle
restarts
in
every generation
from a single cell permits
m u t a t i o n s to a c h i e v e r a d i c a l e v o l u t i o n a r y c h a n g e s by g o i n g ' b a c k to the d r a w i n g b o a r d ' o f e m b r y o l o g i c a l e n g i n e e r i n g . I t a l s o , b y c o n c e n t r a t i n g the efforts o f a l l c e l l s i n t h e o r g a n i s m o n t h e w e l f a r e o f a n a r r o w , s h a r e d g e r m l i n e , p a r t l y r e m o v e s t h e ' t e m p t a t i o n ' for o u t l a w s t o w o r k for t h e i r o w n p r i v a t e g o o d at the e x p e n s e of the other replicators w i t h a stake in the same germ-line. T h e integrated multicellular organism is a phenomenon which has e m e r g e d as a result of n a t u r a l selection on primitively i n d e p e n d e n t selfish
replicators.
phenotypic
power
It has by
paid
which
replicators
they
ensure
to
behave gregariously.
their survival is in
The
principle
e x t e n d e d a n d u n b o u n d e d . In p r a c t i c e the o r g a n i s m has arisen as a partially bounded local concentration, a shared knot of replicator power.
Glossary
T h i s b o o k i s p r i m a r i l y i n t e n d e d for b i o l o g i s t s w h o w i l l h a v e n o n e e d of a glossary,
but it has been suggested
to me that it w o u l d
be w o r t h
e x p l a i n i n g a few t e c h n i c a l terms to m a k e the b o o k m o r e w i d e l y accessible. M a n y of the terms are w e l l defined in other places
(e.g. W i l s o n
1975;
B o d m e r & C a v a l l i - S f o r z a 1976). My definitions are certainly no i m p r o v e ment on
those
already
available,
but
I
have
added
personal
asides on
c o n t r o v e r s i a l w o r d s , o r o n m a t t e r s o f p a r t i c u l a r r e l e v a n c e t o t h e t h e s i s o f this b o o k . I h a v e tried t o a v o i d c l u t t e r i n g u p t h e g l o s s a r y w i t h e x c e s s i v e n u m b e r s of explicit cross-references, but m a n y of the w o r d s used in the definitions w i l l be found to h a v e their o w n definitions elsewhere in the glossary.
adaptation A technical term which has evolved somewhat a w a y from its c o m m o n usage as a near synonym of 'modification'. From sentences like 'cricket wings are adapted (modified from their primary function of flying) for singing' (and by implication are well designed for singing), 'an adaptation' has c o m e to m e a n approximately an attribute of an organism that is ' g o o d ' for something. G o o d in what sense?, and good for what or for w h o m ? , are difficult questions w h i c h are discussed at length in this book. alleles (short for allelomorphs) E a c h gene is able to o c c u p y only a particular region of chromosome, its locus. At any given locus there m a y exist, in the population, alternative forms of the gene. T h e s e alternatives are called alleles of one another. T h i s book emphasizes that there is a sense in w h i c h alleles are competitors of each other, because over evolutionary time successful alleles achieve numerical superiority over others at the same locus, in all the chromosomes of the population. allometry A disproportionate relationship between size of a body part and size of the whole body, the comparisons being made either across individuals or across different life stages in the same individual. For e x a m p l e , large ants (but small humans) tend to have relatively very large heads; the head grows at a different rate from the body as a whole. M a t h e m a t i c a l l y , the size of the part is usually taken as being related to the size of the whole raised to a power, w h i c h m a y be fractional. 283
284
Glossary
allopatric theory of speciation T h e widely supported view that the evolutionary divergence of populations into separate species (which no longer interbreed) takes place in g e o g r a p h i c a l l y separate places. T h e alternative, sympatric theory gives rise to difficulties in understanding how the incipient species can separate if they are continuously in a position to interbreed with each other, and therefore to mix their gene-pools (q.v.). altruism Biologists use the word in a restricted (some would say misleadingly so) sense, only superficially related to c o m m o n usage. An entity, such as a baboon or a gene, is said to be altruistic if it has the effect (not purpose) of promoting the welfare of another entity, at the expense of its o w n welfare. V a r i o u s shades of m e a n i n g of 'altruism' result from various interpretations of 'welfare' (see page 57). Selfish is used in exactly the opposite sense. anaphase T h a t phase of the cycle of cell division during w h i c h the paired chromosomes m o v e apart. In meiosis (q.v.) there are two successive divisions and correspondingly t w o anaphases. anisogamy A sexual system in w h i c h fusion takes place at fertilization between a large (female) and a small (male) gamete. Contrast with isogamy in which there is sexual fusion but no male/female separation: all gametes are of roughly the same size. antibodies Protein molecules, produced in the i m m u n e response of animals, which neutralize i n v a d i n g foreign bodies (antigens). antigens Foreign bodies, usually protein molecules, which provoke the formation of antibodies. aposematism T h e p h e n o m e n o n w h e r e b y distasteful or dangerous organisms like wasps ' w a r n ' enemies by bright colours or equivalent strong stimuli. These are presumed to work by m a k i n g it easy for the enemies to learn to avoid them, but there are (not insuperable) theoretical difficulties over how the phenomenon might evolve in the first place. assortative m a t i n g T h e tendency of individuals to choose mates that resemble (positive assortative m a t i n g or h o m o g a m y ) or specifically do not resemble (negative assortative mating) themselves. S o m e people use the word only in the positive sense. autosome
A chromosome that is not one of the sex chromosomes.
Baldwin/Waddington Effect First proposed by S p a l d i n g in 1873. A largely hypothetical evolutionary process (also called genetic assimilation) whereby natural selection c a n create an illusion of the inheritance of acquired characteristics. Selection in favour of a genetic tendency to acquire a characteristic in response to environmental stimuli leads to the evolution of increased sensitivity to the same environmental stimuli, and eventual emancipation from the need for them. On page 44 I suggest that we might breed a race of spontaneously milk-producing male m a m m a l s by treating successive generations of males with female hormones and selecting for increased sensitivity to female hormones. T h e role of the hormones, or other environmental treatment, is to bring out into the open genetic variation w h i c h w o u l d otherwise lie dormant.
Glossary
285
central d o g m a In molecular biology the d o g m a that nucleic acids act as templates for the synthesis of proteins, but never the reverse. M o r e generally, the d o g m a that genes exert an influence over the form of a body, but the form of a b o d y is never translated back into genetic c o d e : acquired characteristics are not inherited. chromosome O n e of the chains of genes found in cells. In addition to D N A itself, there is usually a complicated supporting structure of protein. Chromosomes become visible under the light microscope only at certain times in the cell c y c l e , but their number and linearity m a y be inferred by statistical reasoning from the facts of inheritance alone (see linkage). T h e chromosomes are usually present in all cells in the body, even though only a minority of them will be active in any one cell. T h e r e are usually two sex chromosomes in every diploid cell as well as a number of autosomes (44 in humans). cistron O n e w a y of defining a gene. In molecular genetics the cistron has a precise definition in terms of a specific experimental test. M o r e loosely it is used to refer to a length of chromosome responsible for the encoding of one chain of a m i n o acids in a protein. codon A triplet of units (nucleotides) in the genetic code, specifying the synthesis of a single unit (amino acid) in a protein chain. clone In cell biology, a set of genetically identical cells, all derived from the same ancestral cell. A h u m a n body is a gigantic clone of some 10 cells. T h e w o r d is also used of a set of organisms all of whose cells are members of the same clone. T h u s a pair of identical twins may be said to be members of the same clone. 15
Cope's Rule An empirical generalization that evolutionary trends towards larger body size are c o m m o n . crossing-over A complicated process w h e r e b y chromosomes, while engaged in meiosis, e x c h a n g e portions of genetic material. T h e result is the permutation of an almost infinite variety of gametes. D ' A r c y Thompson's transformations A g r a p h i c a l technique demonstrating that an animal shape can be transformed into the shape of a related animal by a mathematically specifiable distortion. D ' A r c y T h o m p s o n w o u l d d r a w one of the two shapes on ordinary graph paper, then show that it was transformed approximately into the other shape if the coordinate system were distorted in some particular w a y . diploid A cell is said to be diploid if it has chromosomes in pairs, in sexual cases one from each parent. An organism is said to be diploid if its body cells are diploid. Most sexually reproducing organisms are diploid. dominance A gene is said to be dominant to one of its alleles if it suppresses the phenotypic effect of that (recessive) allele when the two are together. For example, if brown eyes are dominant to blue, only individuals with two blue-eyed genes (homozygous recessive) would actually have blue eyes; those with one blue and one brown gene (heterozygotes) would be indistinguishable from those with two brown genes (homozygous dominant). D o m i n a n c e may be incomplete, in w h i c h case heterozygotes have an intermediate phenotype. T h e opposite of dominant is recessive. Dominance/recessiveness is a property of a phenotypic effect, not of a
286
Glossary
gene as s u c h : thus a gene m a y be dominant in one of its phenotypic effects and recessive in another (see pleiotropy). epigenesis A w o r d with a long history of controversy in embryology. As opposed to preformationism (q.v.) it is the doctrine that bodily complexity emerges by a developmental process of gene/environment interaction from a relatively simple zygote, rather than being totally mapped out in the egg. In this book it is used for the idea, w h i c h I favour, that the genetic code is more like a recipe than a blueprint. It is sometimes said that the epigenesis/preformationism distinction has been m a d e irrelevant by modern molecular biology. I disagree, and have made m u c h of the distinction in C h a p t e r 9, where I claim that epigenesis, but not preformationism, implies that embryonic development is fundamentally, and in principle, irreversible (see central d o g m a ) . epistasis A class of interactions between pairs of genes in their phenotypic effects. T e c h n i c a l l y the interactions are non-additive w h i c h means, roughly, that the combined effect of the two genes is not the same as the sum of their separate effects. For instance, one gene might mask the effects of the other. T h e word is mostly used of genes at different loci, but some authors use it to include interactions between genes at the same locus, in which case dominance/recessiveness is a special case. See also d o m i n a n c e . eukaryotes O n e of the two major groups of organisms on Earth, including all animals, plants, protozoa and fungi. C h a r a c t e r i z e d by the possession of a cell nucleus, and other m e m b r a n e - b o u n d e d cell organelles (analogue of 'organ' within the cell) such as mitochondria. Contrast with prokaryotes (q.v.). T h e prokaryote/eukaryote distinction is m u c h more fundamental than the animal/plant distinction (not to mention the relatively negligible h u m a n / ' a n i m a l ' distinction!). eusociality T h e most a d v a n c e d of the grades of sociality recognized by entomologists. C h a r a c t e r i z e d by a complex of features, the most important of w h i c h is the presence of a caste of sterile 'workers' w h o assist the reproduction of their long-lived mother, the queen. It is usually considered to be confined to wasps, bees, ants and termites, but various other kind of animals approach eusociality in interesting w a y s . evolutionarily stable strategy (ESS) [Note 'evolutionarily' not 'evolutionary'. T h e latter is a c o m m o n g r a m m a t i c a l error in this context.] A strategy that does well in a population dominated by the same strategy. T h i s definition captures the intuitive essence of the idea (see C h a p t e r 7), but is somewhat imprecise; for a m a t h e m a t i c a l definition, see M a y n a r d Smith, 1974. extended phenotype A l l effects of a gene upon the world. As always, 'effect' of a gene is understood as m e a n i n g in comparison with its alleles. T h e conventional phenotype is the special case in w h i c h the effects are regarded as being confined to the individual b o d y in which the gene sits. In practice it is convenient to limit 'extended p h e n o t y p e ' to cases where the effects influence the survival chances of the gene, positively or negatively. fitness A technical term with so m a n y confusing meanings that I have devoted a whole chapter to discussing them (Chapter 10).
Glossary
game theory A mathematical theory originally developed for generalized to human economics and military strategy, and theory of evolutionarily stable strategy (q.v.). G a m e theory wherever the optimum policy is not fixed, but depends upon statistically most likely to be adopted by opponents.
287
h u m a n games, and to evolution in the comes into its o w n the policy w h i c h is
gamete O n e of the sex cells w h i c h fuse in sexual reproduction. Sperms and eggs are both gametes. gemmule A discredited concept espoused by D a r w i n in his 'pangenesis' theory of the inheritance of acquired characteristics—probably the only serious scientific error he ever made, and an example of the 'pluralism' for w h i c h he has recently been praised. G e m m u l e s were supposed to be small hereditary particles w h i c h carried information from all parts of the body into the germ cells. gene A unit of heredity. M a y be defined in different w a y s for different purposes (see page 85). M o l e c u l a r biologists usually employ it in the sense of cistron (q.v.). Population biologists sometimes use it in a more abstract sense. F o l l o w i n g W i l l i a m s (1966, p. 24), I sometimes use the term gene to m e a n 'that w h i c h segregates and recombines with appreciable frequency', and (p. 25) as 'any hereditary information for which there is a favorable or unfavorable selection bias equal to several or many times its rate of endogenous c h a n g e ' . gene-pool T h e whole set of genes in which the term is based is a h a p p y undeniable fact that genes actually go idea of genes flowing about the world
a breeding population. T h e metaphor on one for this book, for it de-emphasizes the about in discrete bodies, and emphasizes the like a liquid.
genetic drift C h a n g e s in gene frequencies over generations, resulting from c h a n c e rather than selection. genome
T h e entire collection of genes possessed by one organism.
genotype T h e genetic constitution of an organism at a particular locus or set of loci. Sometimes used more loosely as the whole genetic counterpart to phenotype (q.v.). gens (pl. gentes) ' R a c e ' of female cuckoos all parasitizing one host species. T h e r e must be genetic differences between gentes, and these are presumed to be on the Y chromosome. M a l e s have no Y chromosomes, and do not belong to gentes. T h e word is poorly chosen, since in the Latin it refers to a clan tracing descent through the male line. germ-line T h a t part of bodies w h i c h is potentially immortal in the form of reproductive copies: the genetic contents of gametes and of cells that give rise to gametes. Contrast with soma, the parts w h i c h are mortal and w h i c h work for the preservation of genes in the germ-line. gradualism T h e doctrine that evolutionary change is g r a d u a l and does not go in jumps. In modern palaeontology it is the subject of an interesting controversy over whether the gaps in the fossil record are artefactual or real (see C h a p t e r 6). Journalists have blown this up into a pseudo-controversy over the validity of Darwinism, w h i c h they say is a gradualist theory. It is true that all sane Darwinians are gradualists in the extreme sense that they do not believe in the de
288
Glossary
novo creation of very complex and therefore statistically improbable new adaptations like eyes. T h i s is surely what D a r w i n understood by the aphorism ' N a t u r e does not make leaps'. But within the spectrum of gradualism in this sense, there is room for disagreement about whether evolutionary change occurs smoothly or in small jerks punctuating long periods of stasis. It is this that is the subject of the modern controversy, and it does not remotely bear, one w a y or the other, on the validity of D a r w i n i s m . group selection A hypothetical process of natural selection a m o n g groups of organisms. Often invoked to explain the evolution of altruism (q.v.). Sometimes confused with kin selection (q.v.). In C h a p t e r 6 I use the replicator/vehicle distinction to distinguish g r o u p selection of altruistic traits from species selection (q.v.) resulting in macroevolutionary trends. haplodiploid A genetic system in which males grow from unfertilized eggs and are haploid, while females grow from fertilized eggs and are diploid. Therefore males have no father and no sons. M a l e s pass all their genes on to their daughters, while females receive only half their genes from their fathers. Haplodiploidy occurs in nearly all social and non-social H y m e n o p t e r a (ants, bees, wasps, etc.), and also a few bugs, beetles, mites, ticks and rotifers. T h e complications which haplodiploidy introduces into closeness of genetic kinship have been ingeniously invoked in theories of the evolution of eusociality (q.v.) in H y m e n o p t e r a . haploid A cell is said to be haploid if it has a single set of chromosomes. Gametes are haploid, and w h e n they fuse in fertilization a diploid cell (q.v.) is produced. S o m e organisms (e.g. fungi and male bees) are haploid in all their cells, and are referred to as haploid organisms. heterozygous T h e condition of h a v i n g nonidentical alleles at a chromosomal locus. Is usually applied to an individual organism, in which case it refers to two alleles at a given locus. M o r e loosely it may refer to the overall statistical withinlocus heterogeneity of alleles averaged over all loci in an individual or in a population. homeotic mutation A mutation causing one part of a body to develop in a manner appropriate to another part. For example, the homeotic mutation 'antennopedia' in Drosophila causes a leg to grow where an antenna normally does. T h i s is interesting, as it shows the power of a single mutation to have elaborate and c o m p l e x effects, but only w h e n there is elaborate complexity already there to be altered. homozygous T h e condition of h a v i n g identical alleles at a chromosomal locus. Is usually applied to an individual organism, in which case it indicates that the individual has two identical alleles at the locus. M o r e loosely it may refer to the overall statistical within-locus homogeneity of alleles averaged over all loci in an individual or in a population. K-selection Selection for the qualities needed to succeed in stable, predictable environments where there is likely to be heavy competition for limited resources between individuals well-equipped to compete, at population sizes close to the
Glossary
289
m a x i m u m that the habitat can bear. A variety of qualities are thought to be favoured by K-selection, including large size, long life, and small numbers of intensively cared-for offspring. Contrast with r-selection ( q . v . ) . T h e 'K' and V are symbols in the conventional algebra of population biologists. kin selection Selection of genes causing individuals to favour close kin, o w i n g to the high probability that kin share those genes. Strictly speaking 'kin' includes immediate offspring, but it is unfortunately undeniable that m a n y biologists use the phrase 'kin selection' specifically when talking about kin other than offspring. K i n selection is also sometimes confused with g r o u p selection (q.v.), from w h i c h it is logically distinct, although where species happen to go around in discrete kin groups the two may incidentally amount to the same thing—'kin g r o u p selection'. Lamarckism Regardless of what L a m a r c k actually said, L a m a r c k i s m is n o w a d a y s the name given to the theory of evolution that relies on the assumption that acquired characteristics can be inherited. F r o m the point of view of this book, the significant feature of the L a m a r c k i a n theory is the idea that new genetic variation tends to be adaptively directed, rather than ' r a n d o m ' (i.e. non-directed) as in the Darwinian theory. T h e orthodox view today is that the L a m a r c k i a n theory is completely wrong. linkage T h e presence on the same chromosome of a pair (or a set) of loci. L i n k a g e is normally recognized by the statistical tendency for alleles at linked loci to be inherited together. For example, if hair colour and eye colour are linked, a child that inherits your eye colour is likely to inherit your hair colour too, while a child that fails to inherit your eye colour is also likely to fail to inherit your hair colour. Children are relatively unlikely to inherit one but not the other, though this can come about due to crossing-over (q.v.), the probability being related to the distance apart of the loci on the chromosome. T h i s is the basis for the technique of chromosome m a p p i n g . linkage disequilibrium T h e statistical tendency for alleles to occur together, in the bodies or gametes of a population, with particular alleles at other loci. For example, if we observed a tendency for fair-haired individuals to be blue-eyed, this might indicate linkage disequilibrium. R e c o g n i z e d as any tendency for the frequency of combinations of alleles at different loci to depart from the frequencies that would be expected from the overall frequencies of the alleles themselves in the population. locus T h e position on a chromosome occupied by a gene (or a set of alternative alleles). For instance, there might be an eye-colour locus, at w h i c h the alternative alleles code for green, b r o w n and red. Usually applied at the level of the cistron (q.v.), the concept of the locus can be generalized to smaller or larger lengths of chromosome. macroevolution T h e study of evolutionary changes that take place over a very large time-scale. Contrast with microevolution, the study of evolutionary changes within populations. Microevolutionary change is c h a n g e in gene frequencies in populations. M a c r o e v o l u t i o n a r y change is usually recognized as c h a n g e in gross morphology in a series of fossils. T h e r e is some controversy over whether
290
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macroevolutionary change is fundamentally just cumulated microevolutionary c h a n g e , or whether the two are 'decoupled' and driven by fundamentally different kinds of process. T h e name macroevolutionist is sometimes misleadingly restricted to partisans on one side of this controversy. It should be a neutral label for anybody studying evolution on the grand time-scale. meiosis T h e kind of cell division in which a cell (usually diploid) gives rise to daughter cells (usually haploid) with half as m a n y chromosomes. Meiosis is an essential part of normal sexual reproduction. It gives rise to the gametes which subsequently fuse to restore the original chromosome number. meiotic drive T h e p h e n o m e n o n whereby alleles affect meiosis so that they secure for themselves a greater than 50 per cent chance of finding themselves in a successful g a m e t e . S u c h genes are said to be 'driving' because they tend to spread through the population in spite of any deleterious effects they may have on organisms. See also segregation distorter. meme A unit of cultural inheritance, hypothesized as analogous to the particulate gene, and as naturally selected by virtue of its 'phenotypic' consequences on its o w n survival and replication in the cultural environment. Mendelian inheritance N o n - b l e n d i n g inheritance by means of pairs of discrete hereditary factors (now identified with genes), one member of each pair coming from each parent. T h e main theoretical alternative is 'blending inheritance'. In M e n d e l i a n inheritance genes m a y blend in their effects on a body, but they themselves do not blend, and they are passed on intact to future generations. microevolution
See m a c r o e v o l u t i o n .
mitochondria S m a l l c o m p l e x organelles within eukaryotic cells, made of membranes, the site of most of the energy-releasing biochemistry of the cells. M i t o c h o n d r i a h a v e their o w n D N A and reproduce autonomously within cells, and, a c c o r d i n g to one theory, they originated in evolution as symbiotic prokaryotes (q.v.). mitosis T h e kind of cell division in which a cell gives rise to daughter cells having a complete set of all its chromosomes. Mitosis is the ordinary cell division of bodily g r o w t h . Contrast with meiosis. modifier gene A gene whose phenotypic effect is to modify the effect of another gene. Geneticists no longer m a k e a distinction between two types of genes, 'major genes' and 'modifiers', but recognize that many (and perhaps most) genes modify the effects of m a n y (and perhaps most) other genes. monophyletic A g r o u p of organisms is said to be monophyletic if all are descended from a c o m m o n ancestor w h i c h w o u l d also have been classified as a member of the group. For instance, the birds are probably a monophyletic group since the most recent c o m m o n ancestor of all birds would probably have been classified as a bird. T h e reptiles, h o w e v e r , are probably polypkyletic, in that the most recent common ancestor of all reptiles w o u l d probably not have been classified as a reptile. Some would argue that polyphyletic groups do not deserve names, and that the Class Reptilia should not be a c k n o w l e d g e d . mutation
An inherited c h a n g e in the genetic material.
In D a r w i n i a n theory
mutations are said to be r a n d o m . T h i s does not mean that they are not lawfully
Glossary
291
caused, but only that there is no specific tendency for them to be directed towards improved adaptation. Improved adaptation comes about only through selection, but it needs mutation as the ultimate source of the variants a m o n g w h i c h it selects. muton T h e m i n i m u m unit of mutational c h a n g e . definitions of gene (with cistron and recon).
O n e of several
alternative
neo-Darwinism A term coined (actually re-coined, for the w o r d was used in the 1880s for a very different g r o u p of evolutionists) in the middle part of this century. Its purpose was to emphasize (and in my opinion exaggerate) the distinctness of the modern synthesis of Darwinism and M e n d e l i a n genetics, a c h i e v e d in the 1920s and 1930s, from D a r w i n ' s o w n view of evolution. I think the need for the ' n e o ' is fading, and D a r w i n ' s o w n a p p r o a c h to 'the e c o n o m y of nature' now looks very modern. neoteny An evolutionary slowing d o w n of bodily d e v e l o p m e n t relative to the development of sexual maturity, with the result that reproduction comes to be practised by organisms w h i c h resemble the j u v e n i l e stages of ancestral forms. It is hypothesized that some major steps in evolution, for e x a m p l e the origin of the vertebrates, c a m e about through neoteny. neutral mutation A mutation that has no selective a d v a n t a g e or d i s a d v a n t a g e in comparison with its allele. T h e o r e t i c a l l y , a neutral mutation m a y b e c o m e 'fixed' (i.e. numerically predominant in the population at its locus) after a n u m b e r of generations, and this would be a form of evolutionary c h a n g e . T h e r e is legitimate controversy over the importance of such random fixations in evolution, but there should be no controversy over their importance in the direct production of adaptation: it is zero. nucleotide A kind of biochemical molecule, notable as the basic building block of D N A and R N A . D N A and R N A are polynucleotides, consisting o f long chains o f nucleotides. T h e nucleotides are 'read' in triplets, each triplet being k n o w n as a codon. ontogeny T h e process of individual development. In practice d e v e l o p m e n t is often taken to culminate in the production of the adult, but strictly it includes later stages such as senescence. T h e doctrine of the extended p h e n o t y p e w o u l d lead us to generalize 'ontogeny' to include the ' d e v e l o p m e n t ' of extracorporeal adaptations, for example artefacts like beaver dams. optimon T h e unit of natural selection, in the sense of the unit for whose benefit adaptations m a y be said to exist. T h e thesis of this book is that the optimon is neither the individual nor the group of individuals but the g e n e or genetic replicator. But the dispute is in part a semantic one, whose resolution occupies portions of Chapters 5 and 6. orthoselection Sustained selection on the members of a lineage over a long period, causing continued evolution in a given direction. C a n create an a p p e a r a n c e of ' m o m e n t u m ' or 'inertia' in evolutionary trends. outlaw gene A gene w h i c h is favoured by selection at its o w n locus, in spite of its deleterious effects on the other genes in the organisms in w h i c h it finds itself. Meiotic drive (q.v.) provides a good e x a m p l e .
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Paley's watch A reference to the best known of William Paley's (1743-1805) arguments for the existence of G o d . A watch is too complicated, and too functional, to have c o m e about by accident: it carries its own evidence of having been purposefully designed. T h e argument seems to apply a fortiori to a living body, w h i c h is even more complicated than a watch. D a r w i n , as a y o u n g man, was deeply impressed by this. A l t h o u g h he later destroyed the G o d part of the argument, by showing that natural selection can play the role of watchmaker to living bodies, he did not destroy the fundamental point — still under-appreciated— that complicated design demands a very special kind of explanation. G o d apart, the natural selection of small inherited variations is probably the only agency c a p a b l e of doing the j o b . phenotype T h e manifested attributes of an organism, the joint product of its genes and their environment during ontogeny. A gene m a y be said to have phenotypic expression in, say, eye colour. In this book the concept of phenotype is extended to include functionally important consequences of gene differences, outside the bodies in w h i c h the genes sit. pheromone A chemical substance secreted by an individual, and adapted to influence the nervous systems of other individuals. Pheromones are often thought of as chemical 'signals' or 'messages', and as the inter-body analogue of hormones. In this book they are more often treated as analogous to manipulative drugs. phylogeny
Ancestral history on the evolutionary time-scale.
plasmid O n e of a set of more or less synonymous words used for small, selfreplicating fragments of genetic material, found in cells but outside chromosomes. pleiotropy T h e phenomenon whereby a change at one genetic locus can bring about a variety of apparently unconnected phenotypic changes. For instance a particular mutation might at one and the same time affect eye colour, toe length, and milk yield. Pleiotropy is probably the rule rather than the exception, and is entirely to be expected from all that we understand about the complex way in which development happens. pluralism In modern D a r w i n i a n j a r g o n , the belief that evolution is driven by m a n y agencies, not just natural selection. Enthusiasts sometimes overlook the distinction between evolution (any kind of change in gene frequencies, which may well be pluralistically caused) and adaptation (which only natural selection, as far as we know, c a n bring a b o u t ) . polygene O n e of a set of genes each exerting a small, cumulative effect on a quantitative trait. polymorphism T h e occurrence together in the same locality of two or more discontinuous forms of a species in such proportions that the rarest of them cannot be maintained merely by recurrent mutation. Polymorphism necessarily occurs during the transient course of an evolutionary change. Polymorphisms may also be maintained in stable balance by various special kinds of natural selection. polyphyletic
See monophyletic.
preformationism As opposed to epigenesis (q.v.) it is the doctrine that the form of the adult body is in some sense mapped in the zygote. O n e early partisan thought
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he could discern, with his microscope, a little man curled up in the head of a sperm. In C h a p t e r 9 it is used for the idea that the genetic code is more like a blueprint than a recipe, implying that the processes of embryonic d e v e l o p m e n t are in principle reversible, in the same sense as, say, you m a y reconstruct its blueprint from a house. prokaryotes O n e of the two major groups of organisms on Earth (contrast eukaryotes) including bacteria and blue-green a l g a e . They have no nucleus and no membrane-bounded organelles such as m i t o c h o n d r i a : indeed one theory has it that mitochondria and other such organelles in eukaryotic cells are, in origin, symbiotic prokaryotic cells. propagule A n y kind of reproductive particle. T h e w o r d is used specifically when we wish not to commit ourselves over whether we are speaking about sexual or asexual reproduction, about gametes or spores, etc.
r-selection Selection for the qualities needed to succeed in unstable, unpredictable environments, where ability to reproduce rapidly and opportunistically is at a premium, and where there is little value in adaptations to succeed in competition. A variety of qualities are thought to be favoured by r-selection, including high fecundity, small size, and adaptations for long-distance dispersal. W e e d s , and their animal equivalents, are examples. Contrast with K-selection ( q . v . ) . It is customary to emphasize that r-selection and K-selection are the extremes of a continuum, most real cases lying somewhere between. Ecologists enjoy a curious love/hate relationship with the r/K concept, often pretending to disapprove of it while finding it indispensable. recessiveness
Opposite of dominance (q.v.).
recon T h e minimum unit of recombination. O n e of several different definitions of gene, but, like muton, it has not yet received sufficient currency to be usable without simultaneous definition. replicator A n y entity in the universe of which copies are m a d e . C h a p t e r 5 contains an extended discussion of replicators, and a classification of active/passive, and germ-line/dead-end replicators. reproductive value A d e m o g r a p h i c technical term, a measure of an individual's expected number of future (female) children. segregation distorter A gene whose phenotypic effect is to influence meiosis so that the gene has a greater than 50 per cent chance of ending up in a successful gamete. See also meiotic drive. selfish
See altruism.
sex chromosome A special chromosome concerned with the determination of sex. In mammals there are two sex chromosomes called X and Y. M a l e s have the genotype X Y , females X X . A l l eggs therefore bear one X chromosome, but sperms may bear either one X (in which case the sperm will give rise to a daughter) or one Y (in which case the sperm will give rise to a son). T h e male sex is therefore referred to as heterogametic, the female as homogametic. Birds have a very similar
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system, except that males are homogametic (the equivalent of X X ) and females heterogametic (the equivalent of X Y ) . Genes carried on sex chromosomes are called 'sex-linked'. T h i s is sometimes confused (e.g. page 10) with 'sex-limited', w h i c h means h a v i n g expression in one sex or the other (not necessarily carried on sex chromosomes). somatic Literally pertaining to the body. In biology it is used for the mortal part of the body, as opposed to the germ-line. speciation T h e process of evolutionary produced from one ancestral species.
divergence
whereby
two
species
are
species selection T h e theory that some evolutionary change takes place by a form of natural selection at the level of species or lineages. If species with certain qualities are more likely to go extinct than species with other qualities, large-scale evolutionary trends in the direction of the favoured qualities may result. These favoured qualities at the species level m a y in theory have nothing to do with the qualities that are favoured by selection within species. C h a p t e r 6 argues that although species selection m a y account for some simple major trends, it cannot account for the evolution of complex adaptation (see Paley's w a t c h , and m a c r o e v o l u t i o n ) . T h e theory of species selection in this sense comes from a different historical tradition from the theory of group selection (q.v.) of altruistic traits, and the two are distinguished in C h a p t e r 6. stasis In evolutionary theory, a period during w h i c h no evolutionary change takes place. See also gradualism. strategy L i k e 'altruism', used by ethologists in a special sense, almost misleadingly distantly related to its c o m m o n usage. It was imported from g a m e theory into biology in the theory of evolutionarily stable strategies (q.v.), where it is essentially synonymous with ' p r o g r a m ' in the computer sense, and means a preprogrammed rule that an animal obeys. T h i s meaning is precise, but unfortunately strategy has become a m u c h abused b u z z - w o r d , and is now bandied about as a trendy synonym for ' b e h a v i o u r pattern'. A l l individuals of a population might follow the strategy ' I f small flee, if large a t t a c k ' ; an observer would then observe two behaviour patterns, fleeing and attacking, but he would be w r o n g to call them two strategies: both behaviour patterns are manifestations of the same conditional strategy. survival value selection.
T h e quality for which a characteristic was favoured by natural
symbiosis T h e intimate living together (with mutual dependence) of members of different species. S o m e modern textbooks omit the mutual dependence proviso, and understand symbiosis to include parasitism (in parasitism, only one side, the parasite, is dependent on the other, the host, w h i c h would be better off alone). Such textbooks use mutualism in place of symbiosis as defined above. symphylic substance C h e m i c a l substance used by social insect colony parasites (e.g. beetles) to influence the behaviour of their hosts.
teleonomy T h e science of adaptation. In effect, teleonomy is teleology made respectable by D a r w i n , but generations of biologists have been schooled to avoid
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'teleology' as though it were an incorrect construction in L a t i n g r a m m a r , and many feel more comfortable with a euphemism. Not m u c h thought has been given to what the science of teleonomy will consist of, but some of its major preoccupations will presumably be the questions of units of selection, and of costs and other constraints on perfection. T h i s book is an essay in teleonomy. tetraploid H a v i n g four of each chromosome type rather than the more usual two (diploid) or one (haploid). N e w species of plants are sometimes formed by a doubling of chromosomes to tetraploidy, but subsequently the species behaves like an ordinary diploid w h i c h happens to have twice as m a n y chromosomes as a closely related species, and it is convenient to consider it diploid for most purposes. Chapter 11 suggests that although individual termites are diploid, the whole termite nest may be regarded as the extended phenotypic product of a tetraploid genotype. vehicle Used in this book for any relatively discrete entity, such as an individual organism, which houses replicators (q.v.), and w h i c h can be regarded as a machine programmed to preserve and propagate the replicators that ride inside it. Weismannism T h e doctrine of a rigid separation between an immortal germ-line and the succession of mortal bodies w h i c h house it. In particular the doctrine that the germ-line m a y influence the form of the body, but not the other w a y around. See also central d o g m a . zygote T h e cell that is the immediate product of sexual fusion between t w o gametes.
