SEVENTH EDITION
AN EVOLUTIONARY APPROACH
A ARIZONA STATE UNIVERSITY
SINAUER ASSOCIATES, INC. SUNDERLAND, MASSACHUSETTS
TM C_ A ~ itIk ('OIlwy1' ~ informatioo. about .... fiP1~ uponry 10 ri,'~ INln. ~aph by Ilruc'l' lyan.
1M FrontiJPi«~ 1lw lhrNt d;,.pa.y of tIw l-WnadJyas Nboon noion many qun"'- for n 'olutionary ~ ~aph by C K. 1.oftnz-
Animal ~hovior. An Evolutionary Approach, ~nfh Edifion C Copyright 2001 by SiN..... AS6Oriare.. lee. All rillh tll ........ ".l"Tlb 170 TIlt Effrr:ts of u,n.l.litwI iii Iitt' C...... Anok 171 H~tklp~i:.tSocMlBoIMI'" 17J T~
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Adaptation and Antipredator Behavior 182
T1w MNln ing of Adapl.llioo 184 T1w Comp.uati\·" Method for T..,;tin g Adapl.lliooist Hypotlll"Sol."S 187 ~ Impvrlana of Dit\'rgffll ft\liw'iQII 189 TIlt Imp"',an.:t uf CoIl""":f a Sign0' History of .. Sign.al-Rf'mving M..dwusm 2'l7 n", History of 1n"d Wing. 289 s"n.r I/ptJ 5"...... Coo'Ipt1" .... JJ7 Malt CWlrdin)( JJ8 s", u..l s"lt'ction ..nd Mat.. Choice 341 f~ .MIlt Chc>ict' ,,"1110104 R~""""Y ~~J5J
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12 j The Evolution of Mating Systems 360 Is Monogamy Ad..pti,·..? 362 M.mllllamy III .MI......../. J64 M"nllllamy i" Bird. J66 ulrl/-Pai, C"P"iIIfio>r.: n",.MIk Prrsp«fi.". 369 £xItI-Pllir CDJ'IUIIfiorr£ TJw FtrItIIh P....ptdit'" 370 Poly.andry without Pol)·gyny m Pol)·gyny J77 f"""/t [)o/nst Polygyny: Tht f"""lt Prnp«tiror 379
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The Evolution of Parental Care 394
Why Is Parenl,ll Care More Often Maternal than Paternal? 396 EXCl7'tion~ to tlw Ruit 397 Wh.~ Do Mille Wattr Bugs Do All tlw Work? 400 Discriminating Paren tal Cart' 402 Offip"ng Rt>:ognition; C"",,,,,rati,,,, St udin'd. Purin!\ thi, time, much thai L, d"Preso;ing hils occurn.';, but i""tt'ad ronsider the pooitive side of the It'dl;t"f,which includes the many exce]\tonI P"J""T" on animal ochdvior tha t have been w rittJ1 over Ill, a fi g"... thaI unde""brnalt"!' the actual inc",. ... bi>cau,rn,~ whal, J how" bc\>n abl.. to Inrorrx-"'dl~ ....,1'" illustration. ltiroul':h text, Ihanks 10 Ih~ w illin gn ..," of mv publi.her, Sinau~r A''''lC;at...., to m~ k .. th.. mow f,om hlM k and ",hitt, to full rolor. This change not only add, 10 Ih
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An Evolutionary Approach to Animal Behavior or hundreds of thousa nds of years, humans observed animals because their lives depended on a kno wledge of animal behavior. Even today, the subject still has great practica l significance. Information on the reprod uctive behavior of insect pests, for example, may ultimately lead 10 their control, while knowled ge of the migratory routes of an endangered whale or shorebird may enable conservanonlsts to design adequa te reserves to save the animal from extinction. Moreover, an unders tanding of the evolutionary basis of our own behavior might help us identify why we so often damage our environmen ts, perhaps enabling us to reduce ou r destructive tendencies (1251). But even if the on ly beneficia ries of studies of a nima l behavior were the persons who conducted the research, 1 suspect tha t work in this field would continue. Learning how and why animals beha ve is an in trinsically fascina ting business. Perhaps you ca n imagine what it would be like to be the first person to discover that male ... (""Tk.
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first showed that female Seychelles warblers could control
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Questions about Behavior lli>"\'d for one """'mo:"I" in Monl\"\"(>flje. a tiny communiI)' in 1:1\0' I'f\IIfIIain: of C"" U RK 1.;,,;1. ....,. f"""""-'d by pac;fi>t Qua~ f the L"nilo!'t:l sea... around I n of ttw Korean War. Whilr I ...as t a frwnd Ioarwd . black liK!'1. which 1h\U\K up by a wrule """'" on I back pordo of our . The ultra>'ioIo:t ,a~ of the lamp altractN hund~ of rnoth!oe«h nighl.and many olayed .... the .t-i until I could insp«I them. 50.,...,.. fI\Of1\ing> I found a h"l/;'" btijlht Y'-~k"" rnolh b .1..", l;>.K'k al n,.. (Figlll\' Any"".. ....-injl Au/omeris abnJplly "~I""" i~ hindwin" ....y to Animal
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ft"m Ih. as i5 any'......• who wanl>o the .""w..... 10 'll>e authurthenadJed,"Of course_ the monky. may .imply ""i''Y.the ......"'"i,..," as if this ""planalion n",.nt that w,' could ill""'" the ll'It.'didnal bt.,..,fil hypoIIK'Sis. Th.I ....o uld bt- a mista ke. At 0 p"",imalv l,'\'v[. monk~ys may indwd d,'rive pl~.~u"" Imm a pplying cvrtain suI>sl_lnn'S 10 Ihe;, bodi,.,;, bul this explanation d'.... nul "'placand hicycling up 10 70 mil,,,, a day in om..r 10Ia'" m",,, ah""t tlv:rn [1137]. The sf""'i... of digger "'asp thai cought Tinbergm', eye was Phiumlhu' lriangulunl, the h,.., ,""01l. so ""med ITIIs off the ""'in tunnt.-l. 1be l>ey the nt'Sling r..m..le. Som~ s.:mddunt'S in Hl1lshorsl w~", doUN wilh hundn-ds olhurrows...ach m.rk"" with a low m,,1IDd of Y"llow "'nd thai the hom.1e b...,wolf had Iran.. portn. How co"ld thl'y IoW' horne so easHy? The wa,p" p",videcal Llndrnarks in lhe nesting an", f,tr u.", wht-rt n'tumin,; 10 lhe nesl ''11lrar..,... To lgic of science. Tinbe""",,'. """arch is typical of mosl sci""lific inn,'Stig"lions. Indeed. lhe scientific m!hod is familiar
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by 8tuU.~ systt-m. 'The new gene, with its dL,tindh'" d"velopmental eftect, could not MV" l"'rslst.>d unless the individuallhal first c.rJit>d it "'l'n>ducro mo", successfully th.n other birds, with their dift.,..."t g'gOOd this prt'dicti"n with a simple expcrirneewllil wa,p, He beg.n wilh (1) a qoeshon; \'iny hdd black-head,,,j gulls l.'\IoIwd a . pecial respon.., to the egg>hells in their nests? He then general. de!; sw.rying ,"plal"kllion of how l.'\Iolutinndry change might ,-.;nIl' within sJ-"-'ci.... o..",;n'. gn.-.>t idea re;1S on ttwe commonly ,lbs..,''-.,.] fealul'l'S of llvtng things: 1. Variation: Ml'mbu't~t"blf when tht'!IC tho... cond i!it"" """'" in a ~ (Fillure 'I). [f blad.-headro gulls, lor insla""'-', pnldOCO' """'-'&.pring th.,n ,>tht-rs, and if their .>dulloffspring haw inherilro the trdil (such as ..j;j\s.... U ",moval ) that ad vdncM thei r sucres~fu l reproduction. tllt>Jl th
8 A va,iabt~ ,~io>, . Thr ladybird ,*,_oqr;diI .. hibrt, hoted iUlry va""'",,, io in color pan~rn, Photog'"i>/'>' by Mike MajHo.
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9 Natural select io n. If the differences in the color patterns of ladybird beetles are hereditary, and if one type of beetle leaves more surviving offspring on average than the other, then the population will evolve, becoming more and more dominated by the
reproductively successful type.
spring that do surv ive may inherit their disad vantage and thus may also leav e relati vely few surviving progeny. As a resu lt, traits that compromise lifetime reproductive success will beco me progressively rarer over evolu tionary time. Dar win called this pro cess natural selection beca use he saw the elimina tion of traits unfa vorable to reproduction and the spread of ben eficial ones as the natural consequence of hereditary va riation. Thus, Darwinian logic lead s us to expect that evoluti onary change will always be in the direction that promotes successful reproduction by indi vidu als. Darwin develop ed the theory of natural selection before critical discoveries abo u t the nature of heredity had bee n mad e. Genes are now kn own to be nucleic acids that faith fully encode the information need ed for the synthesis of proteins, which are critically impo rtant for all living thin gs. Genes can be cop ied and tran smitted to offspring. When this happens, the genes themselves are essentially reproducing, with the organism merely acting as a mortal vehicle for the process. The modern evolutionary approac h to animal behavior applies Darwinian logic at the gene tic level in much the same way that Darw in applied it to individuals: 1. Genetic variation: Gene s can occur in more than one form . When alterna -
tive form s, or alleles, of a gene exist, the different alleles ma y lead to the production of slightly d ifferent forms of the same protein. 2. Heredity: Alleles can be tran smitted from parent to offspring. 3. Differential reproduction: Some alleles are better than others at producing effects that cause their bea rers to tran smit copies of their alleles to subsequent generation s.
If these three conditions apply, then alleles that help make indi viduals more reproductively successful will become more common in the population over evo lutionary time. Oth er alleles that confer less reproductive success on indi-
An Evolut iona ry Approac h to Animal Behavior v id ua ls w ill eventua lly disappear. (We ass ume that populations cann ot gro w
exponentia lly forever, so that only a limited number of copies of a gene can exist at anyone time .) The logical conclusio n is that selection on individuals will favor alleles that help bu ild bodies that are unusually good at promoting the propagation of those alleles-or, as E. O . Wilson puts it, a chicken is really the way that chicken genes ma ke more copies of themselves [1247].
Darwinian Logic and the Study of Behavior No ma tter how the logic of natural selection is pre sented , it is a blockbuster of an ide a. It means that human s and all other living things have been shaped by pas t selection favor ing cha racteristics that enhanced their ability to reprodu ce and pass on their genes. An understanding of this point helps us identify questions worth as king while at the same time shap ing the kinds of hypotheses that we will test. Let's illustrate the utility of Darwinian theory with the case of infanticide in hanum an langurs . These graceful primates live in band s, which often consist
of one large, reprod uctively active male and a group of smaller adult females and their offspring (Figure 10). From time to time, the resident male is pushed ou t of the grou p by a new comer, usually after a series of violent clashes. After such a takeover, infants tend to die. Although the cause of death is often unclear, the new male is the prime suspect in man y instances, and males have been seen doing the deed several times (Figure 11) [132, 553]. The ph enomenon of infanti cide is pre cisely the sort of thing likely to attract the attention of a Darwinian biologist. Why should a male langur that has just spe nt days in a dan gerous mooing battle with the previous resid ent male tum on the offspring of the very fema les he has finally succeeded in joining? Having avoided incapacitating injur y during his battles with the rival male, why sho uld he now take the chance of being bitten by one of his female companions as she attempts to protect an infant (Figure 11 )? In other words, how can infanticide possibly adva nce a male's reproduc tive success? This question jumps out at an evolutionary biologist precisely becau se infanticide by male langurs seems so unlikely to have evolved by natural selection. Indeed , the behavior might not be an evolved trai t that contributes to the male's reproductive success, but could instead be a social pathology brought on by overcrowd ing. Under high-density conditions, males may encoun ter each
lOA band of hanuman langur females and their offspring . Males fight to monopolize sexual access to the females in groups like this. Photograph
byS.Nagendra.
13
11 Male Infanticide In hanum an langun. Ileft) Aninfant·killing male langu' fI.., Imm a f=\ale belonging ,o,~ bond ~ i, a"emp'ing pn. lR;ghtl Anurlli ....'oI"'al StIKtw., [123'1]. YI'illiam.showed th.,t tho> .urvival of all''TThlli'·.... U... I"" was much mo", lik...ly to be dir population for tho> long -te-rm henefit of th..i.ll F"thnlogy and F''l'ul~li,m n,gulation hypothcst.. lor lan>;u, Inf.nticide.
'lCy ...plroi.hing lhei, .kpleted eneq:y """'t\',,". If '0, kill", m.l... could d."i h.mdits from their actions th.t could.....,p them .live to due" mo than mal,.. Ih.t did not kill and eOflSUm" youn)\st.,r.; whII\O-'-;i.. tt.."ting, nute tMI mo", than 0"" ..,planallon can I".ld to the So,m.' pR-'didion••s w" just saw wI>i, own olkpring are born to tllt' ,..."id..o! It'malt",_ In th., ",,,,,,,od c~",.. we e~pt'Ct males 10 Slop killiog inlAnts .Ilt>r they m·.......t fmm thei, ..,...·'W'ti(.lIy ,"'p.,n..";"" t"kv~,."ly n;'u tl>dletlons """,ived ronfirm"tl"fl from v.rious "'U"'eS [553, 10ll5[. ftl' ,,~ampl.., a ,...,..,.",her obse,,,;ng. lan>;ut group of S('\'",.l adult mal.'S Ii"inl'; togdhe, with ...a riou. I"mal•., 1\'Ct>rd,'f
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An Evo lutionary Ap proac h to Animal Beha vior
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infanticide for which DNA samples had been collected from the presumptive killer male and his victim. In every ins tance the killer was not the father of the deceased infant. Moreover, females who had lost their young prom ptly regained their sexual receptivity, and the new infants that resulted were fathered by the infanticidal males, as wa s again demo ns tra ted conclus ively through DNA tes ting [132]. These findings provide strong suppo rt for the increased rep roductive opportunities hypothesis for infanticide. But the more tests, the better. If natural selection has prod uced ma le Hanuman langu rs that kill infants to gain more rap id sexua l access to females, then we would expect to observe infa nticide in many other species whose social systems resem ble tha t of the lan gur. This pred iction has now been confirmed through studies of various other anima ls in which newcomer males replace p revious residen t ma les, kill infants fathered by those ma les, and then mate wi th the fema les that have lost their youngsters [344]. In lions, for example, infanticide often occurs when a new gro up of males ousts the males from a pride containing a number of females w ith yo ung cubs [943]. The incoming males hunt down cu bs less than 9 months old and try to kill them (Figure 12), although, like female langu rs, lionesses try (some times successfully) to p rotect their cubs. Lionesses that keep their cubs alive give birth at 2-year intervals, b ut fema les whose babies are killed resu me sexua l cycling at once and mate w ith the killers of thei r offspring . Since a ma le can expec t to remain in a pride and have access to its fema les for just 2 yea rs on average, the reprod uctive benefits of infanticide from the male's perspective are eviden t. Ind eed, male lions probably kill a quarter of all the cubs th at die in their first year in some pop ulations [943]. The observation tha t lions and other anima ls commit infan ticide under certain predictable cond itions supports the increased reproductive opportunities hypothesis. If these conditions favor the evolu tion of male infa n ticide, then we can predic t that infanticide sho uld be practiced by females of those unusual species in whic h sexual access to males limits female reproductive success . This pre d iction has been confirmed for a gia n t waterbug whose ma les take care of egg masses (Figure 13), which are sometimes att acked by egg-stabbing females.
12 Infanticide by a male lion. The male carriesa cub he has killed after displaci ng the adult males that once lived with the pride. Photograph by George Schaller.
17
18
Chap ter 1 After the destruction of a clutch of eggs, the male associates with the infanticidal female , mates with her, and cares for a new brood of her eggs [5631. Likewise, in a water bird called the jacana, males provide exclusive care of the eggs and young. Territory-defending females sometimes attack the chicks of neighboring females, forcing the brooding male to abandon these offspring. He may then mate with and accept a new clutch of eggs from the infanticidal female. When researchers experimentally removed some territorial females, neighb orin g females quickly invaded the vacated territories and, in three of four cases, either killed the baby jacanas there or forced them to flee. Within 48 hours the males that had lost their offspring were involved in sexual liaisons with the infanti cidal females. By com mitting infanti cide, these fem ales had gained caretakers for their eggs soo ne r than if th ey had waited for th e ma les to finish rear ing their curren t brood s [361].
Certainty and Science
13
Protect ion against infanticide.
This male waterbug guards a clutch of eggsagainst infanticidal females that may destroy hiscurrent clutch in order to replace these eggs with their own.
Photograph by Bob Smith.
You must have deduced from my summary of research on infanticide that I think the increased reproductive opportunities hypothesis applies to langurs and lions, wa terbugs and jacanas. I do-but I could be wrong, and indeed, some other researchers believe that langurs and some other animals do not commit infanticide in ways that increase their reproductive success [75, 118, 276]. These disagreements remind us that all scientific conclusions must be considered ten tative to some degree. In the past, majority opinion has changed drama tically when a previously unconsidered hypothesis came along or new data surfaced that destroyed an es tablished hypothesis. When I was student at Amherst Co llege, my pa leontology professor convinced me that the earth's con tinents have always bee n w he re they are now located . However, as new evi dence came in, everyone, including me, abandoned the old view; now the genera lly accepted hyp oth esis is th at the contine nts "float" aro und the planet on moveable plates. The rejection of es tablished wisdom happens all the time in science. Scientists tend to be a skeptical lot, perhaps because special rewards go to those who can show tha t previously published conclusions are incorrect. Researchers constantly criticize their colleagues' ideas, in good humor or otherwise, sometimes causing their fellow scientists to change their minds. The uncertainty about Truth tha t scientists accept, at least when talking about other people's ideas, often makes nonscientists nervous, in part because scientific results are usually presented to the p ublic as if they were written in stone. But anyone who has taken a look at the his tory of any scientific endeavor will learn that new ideas con tin ua lly surface and old ones are reg ularly replaced or modified. I repeat, complete certainty is never achieved in science. The strength of science stems from the willingn ess of at least some scien tists to consider new ideas and to test hyp oth eses repeatedl y. I hop e that yo u will keep this point in mind as we review the find ings of scien tis ts and their in terp re tatio ns of evi dence in th e cha pters ahead. We will first examine the proximate and ultimate aspects of bird singing behavior (Chapter 2) before lookin g more closely at the different components of a proximate ana lysis of behavior (in Chapters 3 through 6). Then we tum to ultimate questions about evolutionary history and adaptive value (in Chapters 7 through 14). The book concludes with a chapter on the evolution of human behavior. Thanks to the small array of behavioral researchers that have attacked these questions, there is m uch to say on these topics, so let's get started.
An Evolutionary Appfoach 10 Animal Behavior
Summary 1. Ilos;c qu""tin" ."'lUl animal beh.l.vior faU inlo two cal"l'ori"". "How qll p""""l, and why has evolution followed one palh insl.ad of anot~r ?
2. /loth pro'imdle and ulhmate qU""hons can be in"""hgated scienhficaJJy lul low;ng tI",,,,, sl't'" I , We beg;n wilh a cau",,1qu""ti"" aboul whal cau",," """e1rung to
happm. 2 We d,,,,i,,, a working hypothesi,. or pth....... . on how traits mil(hl prt>lI\Ote \he "m'i..,l 01 the g""'-"" of indi,-idoal. with tht,.., tr.its; U'lngs
6. Toda}' olmost an bi'havirn-al biolog;sls U'lO .....'Y. many dil,. "'''''' hy dmwning •• !hey ' l!ioIod,ff lly, n...... for .. umfW. in • gmot m.on~' ~rd ~ malo>srommUNbor.1r 0. "h...tJtod " l'uliution thai tht-r gi... mou...nd. of h ....... each ,;piing.. ... ~, I..."., prod ...... , im p lee. 1I noore. but ,. I~, if full-fIe,;l~ "'~ " . _ alth.>ugh all rnaIe " 'Iu............-no.ing h.ot "miLany. >hac. ing a b.>sJt: I'-'IMn th.ot ma..... them.U id""hfi.ablt" WIuIE-de, t\Wwna,.
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Proximate and Ultimate Causes of Behavior
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allowed 10- to SG-day-old youngsters to listen to tapes of white-crowned sparrow song. The isolated birds eventually reproduced the exact song they had heard on tape . If a young male had listened to a tape of a Berkeley dialect, he would mimic that song; if he had instead been treated to a steady diet of Marin song , he wo uld sing that dialect by the time he was 200 days old. These resu lts offer powerful support for the environmental differences hypothesis. Young birds that grow up near Marin hear only the Marin dialect as sung by olde r males in their neighborhood. They store the acoustical information they acquire from their "tu tors" and later match their own song output against their memories of the song, eventually coming to duplicate a particular diale ct. Additional laboratory experiments with isolated birds and taped song s led Marler to the following conclusions about song learning in the white-crowned sparrow [757]: 1. Song recognition: A male white-crowned sparrow is predisposed to learn his own species' song, not that of ano ther species , especially during a critical period when he is between 10 and 50 days old. Isolated white-crowns of this age that listen to tapes of song sparrows instead of white-crowns develop aberrant songs that generally resemble those of birds that have heard no so ngs at all. However, if the young bird hears a tape w ith both
1
25
Song dialects in white-crowned
sparrows from Marin, Berkeley, and Sunset Beach, California. Males in each location have their own distinctive song dialect. as revealed in these sonograms of the songs of six birds fromeach location. Sonograms shown in the same color are the same dialect.Sonograms courtesy of Peter Marler.
26
Chapt er 2 song spa rrow an d white-erowned sparrow songs on it, he will develop normal white-crown ed sparrow song, learning the white-crown dialect from the tape while ign oring the song sparrow song [650). The inna te preference of young white-erown males for white-crowned spa rrow song is so great that fled glings can acquire songs from tu tor tap es that play whitecrowned spa rrow song in reverse [121 9]. 2. Song practice: If a yo ung bird hears white-erown song d uri ng the critical period atlO to 50 days of age, no additional acoustical experience is required until he is abo ut 150 d ays of age, when he begins to prod uce a va riab le, exploratory "subsong ." At this time, he must be able to hear himself sing if he is ever to develop a normal full song [649). If he is deafened before subsong begins, he cannot match his own vocal output with the memory of his species' song acq uired when he was 10 to 50 da ys old. As a result, development of the song halts, and the end product is highly abnormal. 3. Song crystallizatio n: Once an un deafened young male has generated a large and va riable repertoire of songs d uring the practice ph ase, he can select one of hi s own that matches a memorized lutor song. By repea ted ly singing that song, the bird forms a crystallized full song, w hich wi ll become his ma in vocalization as an ad ult male. In nature, therefore, most ad ults sing a copy of the song they heard sung by a natur al tut or early in their lives.
Social Experience and Song Development Marl er interpreted the results of these taped -tutor expe riments to mean that as the mal e white-crowned spa rro w' s brain develop s, he acq uires a neu ral mechanism that is highly spec ialized for learning his species' song . The juvenile male 's brain is abl e to store acou sti cal informat ion from sing ing whitecrowned sparrows during an early period in his life (Figure 2) [7571. If Marler 's in terpretation is correct, then we can pred ict that male white-crowned spa rrows will never be able to sing an oth er species' song . Occasionally, however, ornithologists have heard wild white-crowned spa rrows singing like song sparrows. Ob servati ons of this so rt caused Luis Baptista to wonde r whether some othe r factor in addition to acoustical expe rience might influence the song learning process. Marler 's fam ous taped-tutor experi ments were all done with birds deprived of social interactions wi th ad ults. Perh ap s social stimuli can also affect what a young white-crow n learns abo ut song. Baptista and his colleague Lewis Petrinovich tested this social learning hypothesis by placing fledgling hand-reared white-erowns in cages where they could see and hear living adult song sparrows or strawberry finches [72). These young white-crowns learned their social tutor 's song even though they could hear, but not see, other white-crowns (Figure 3). Moreover, white-crowns that were older
2
Song learning hypothesis based on
laboratory experiments with whitecrowned sparrows. According to this hypothesis, young white-crownshave a critical period 10 to SO daysafter hatching when their neural systemscanacquire information by listening to white-crown song. but not from any other species ' song . Later in life, the bird matches hisown subsong w ith his memoryof the tutor's song, and eventually imitates it perfectly-
unless he is deafened. Based on a diagram
by Peter Marler.
Son gs present c d
Song sparrow song
. .., --
, I
• I · ..
Songs developed White-crowned spa rrow song
- - \~\ ~ \I\\\\\\ l..
I
o 10
-r: v
:
Neural tem plate open
50
Fullsong
Subsong
100 Age (days)
150
\1 \" \ \ _• • _
Matching phase
zoo
I\\\I\\\\\\...
Proxi m ate and Ultimate Causes o f Behavior
3
(A) Strawberry finch
27
Social experience influences song develop-
ment. A white-crowned sparrow that hasbeen caged next to a strawberry finch will learn the song of its
6
","'--"!!"'g
2 N
J:OL-- - - - L -- - - - - ' - -
-'-
17 -;---1 ~ r:
.; \ 1 ~
1: \ 1
~~"'\ "h ~ r'" ~
social tutor. (A)The songof a tutor strawberry finch; (B) the song of a sparrow caged nearby.The letters beneath the sonograms label the syllables of the finch song and their counterparts in the song learned by the sparrow. Sonogramscourtesy of Luis Baptista.
-'-_
~
C ~
"
u,
. ..
(B) white-crowned sparrow
'7
6
2
.....
~,~ a
~. ~
b
d
~')r i' f
b
f " -,,, g
O'---------'----- - ' - - - - - - - ' - - - - - L 0.5
1.0
1.5
2.0
Time (seconds)
than 50 days when they first encountered a social tutor could stilileam the alien song, showing that song learning can occur past the 5O-daymark under some circumstances [71]. Indeed, some wild male white-crowns modify their songs throughout their lives. By recording the songs of known individuals (using distinctive combinations of colored leg bands to identify them) and comparing their songs wi th those of males in neighbo ring territories, researchers have shown that older male white-crowns in some populations regularly inco rporate song elements of their current neighbors into their vocalizations [70]. Social experience shapes singing behavior in many birds in addition to whitecrowned sparrows. Captive starlings , for example, are adept at mimicking human speech, producing such phrases as "see you soon baboon" or "basic research" as well as the sounds of laughter or kissing or coughing. But they will do so ollly ifthey are hand -reared in a human household where they participate in the social life of their caregivers (Figure 4) [12091. In nature, yo ung male starlings and
4 Social effects on song learning. Kuro the starling learnedto include words in his vocalizations because he had a close relationshipwith the family of Keigo lizuka. Photograph by Birgine Nielsen, courtesy of K.l izuka.
28
Chapte, 2 whit..-crownd sparrow. """,in" both "",oustical and s"cial.timulation lrom adull malt-s of their own sp""ies, and both lactors Mve somthing to do ...; th the development of their song•. So, in proximate term •. why do male whitcts, ",,",' from Iht> sparrow.' ""tal populalion and the other fr"m a rry;ion aboul 20J hn away, aboul two-third. of lhe young.n·... ,·"""tuaUy imitated the natal dialed, c"mpar«! wi th only "ne-third tMI mimick..-d Ihe foreign d ialec l. The...' .....ulls demon.slrailt.-tmino, cha' • "..ri~"'" ul living thin!\" . ... dc>lh), l11.a1 is, a dift~n'11C. de....Io.>pmiork on t t .....""'" .. still in its inf.ncy, bul' ....... Idwn two,... ~ thai ....,ng ..... ming OCCUR in 'f'II'Cin bekJnging 10 just ) of tho: 21 owdn-o of birds (FiKu'" 10): hpur0i5.lhr h~andtho: ~~ [14l'11_ H.1osHCh group ~1Iy ~ Itk rwu,.l
u
I
If the independent origins scenario were true, we would expect to find major differences among the song control systems of the three groups. Careful anatomical studies have revealed that the key control centers are positioned quite differently in the brains of songbirds and of parrots [150]. On the other hand, the budgerigar, a parrot, possesses the same Z ENK gene that songbirds have. Moreover, this regulatory gene is activated in various parts of the song control system when the budgerigar hears budgie warbles or when it is vocalizing. At the gene tic level, therefore, real similarities exist between songbirds and parrots, with both sharing at least one major gene invo lved in the development of struc tures that contribute to song recogn ition and song production [577]. As a result, we cannot S.lY for certain whether parrots, hummingbirds, and songbirds secured their remarkable song-learning skills by inheriting the genes for their kind of song system development from a distant common ancestor, or whether they independently evolved similar abilities, making use of some of the same long-persisting genes and ancient vocal systems present in the species preceeding them.
The Adaptationist Approach The song control systems that make learning a distinctive song possible have an evolutionary history with a beginning almost certainly followed by a long series of modifications, some of which were retained and others that were lost over evolutionary time. The current song system of any species is the prod-
35
10 The phylogeny of song learning in birds. Ifwe assume that the lonq extinct bird that gave rise to all modern species did not learn elementsof itssong s, but instead produced innate vocalizations, asdo many modern bird groups, then song learning has evolved independently in three different lineages of modern birds. On the other hand, song learning may have originated in a common ancestorof parrots (pslttactform es), hummingbirds (Trochiliformes), and passerines, and been retained in thesethree lineages while having been lost in other descendantsof an ancestral so nq-learninq species. After Brenowitz [1461.
36
Chapt er 2
11 Female red-winged blackbirds adopt the precopulatory display position (tail elevated)more often when hearing their own species' song than when listening to (A) a tape of a swamp sparrow's
songor (B) a tape of a mockingbirdsinging
(R)
(A)
10
15
8
12
their own specie s' so ng (mockingbirds mimicthe songs of other species). After Orians (861) and Searcy and Brenowitz (10321.
9
6
3
2
o
Red-winged
Swamp sp arrow
blackbird
Song
o
Red -winged blackbi rd
Mock ingb ird imitation
Song
Red-wingedblackbird female
uct of this historical process, which raises ano ther complementary evo lutio nary q ues tion, one that focuses on why some att ributes have persisted to the present. Why is it that white-crowned sparrows living today have a nervous system that ena bles them to acquire a distinctive vocalization diffe rent from that of any other living spa rrow species? Has na tural selectio n bee n respo nsible for the evolutionary changes that have resulted in tod ay's proximat e mechanisms that prod uce a species-specific song in male wh ite-crown ed sparrows? In the past, white-erowns whose songs hap pened to be especially distinctive migh t have enjoye d a rep rod uctive adva ntage becau se highl y recogn izabl e singers were able to communica te their spec ies' ide ntity more effectively to listen ing fem ales. Sexually receptive fema le white-cro wns currently respo nd more enthusiastically to songs of their own species than to songs of other sparrows [10881, and the same is true for other songbirds (Figure 11)(1031). If in the pas t fema le songbirds gene rally reacted more positively to especially dis tinctive singers of their species, then natural selection d riven by mate choice would result in the spread of the favore d songs. We have here an example of wha t is called an ad aptation ist hypothesi s, a possible explanation based on natural selection theory that attempts to identify the adaptive (reproductive) value of a pa rticu lar attrib ute, in this case singing a song that announces unmistakably the species membership of the singer. More than one adaptationist explana tion exists for why different species sing different songs. Species that occupy different habitats may evolve different song prope rties to overcome special environmental obstacles to being heard. In forests, for example, the dense foliage of trees absorbs sound, making it harder for forest birds to broadcast their signals a long distance, especially if the song contains trilled sound frequencies above 4 kHz [208, 820). The songs of forestd welling birds often do feature whistles, not trills, with frequencies below, not above, 4 kHz, whereas species that live in open woodland or savannas are more likely to use trills and notes above the 4 kHz level. This is true even for different pop ulations of the same species occupying habitats that differ in foliage density (Figure 12) (559). Thus, strong selection for effective pro pagation of acoustical messages may lead geogra phically sepa rated pop ulations of birds to produ ce different kind s of songs. In add ition, one can devise nonadaptationist expla nations for the distinctive so ng o utput of white-crowned spa rrows. For exa mp le, the spec ies-spec ific na ture of the voca lizations of white-cro wned spa rrows could have arisen as
Proximate and Ultimate Causes of Behav ior
Woodlands
Forests 8
'I.
Swede n 0 J:
8
~
>u
,sr•c
•
~ ~
,. ,.
- - -
.
r-
12 Songs match hab itats. Greattitsfrom dense forests produce pure whistles of relatively low frequency, whereas males of the same species that livein more open woodlands use moreand higher sound frequencies in theirmore complex songs.After Hunterand Krebs [559].
Spain
,
",
,
, l
•
- \
Norw ay
~
~
--
• N
•
Iran
u,
0 8
•
- England
0
0.5
1.0
Time (sec onds)
, \.
, ,• a
....
\. ~ -.
"
37
,
~
Morocco
0.5 1.0 Time (seconds)
an incidental, nonadaptive result of the effects of speciation, rather than through selection for song properties that could be transmitted effectively or that facilitated species identification. This by-product hypo thesis suggests that whitecrown song was shaped during the period when white-crowned sparrows were evolving in geographic isolation from some of the species that now live with them. The gene pool of these isolated ancestral white-crowns would have been influenced by a variety of events, including random mutations and the aceidental loss of genetic variation from small populations. In addition, natural selection acting nonrandomly on features other than the song per se wo uld have also altered the gene pool of the species. As assorted genetic changes accumulated in the population ancestral to modern white-crowned sparrows, this population would have become increasingly different from other populations of sparrows, genetically speaking [775]. Some of these genetic differences might have had developmental side effects on the kinds of vocalizations the birds could produce, altering their songs as compared with their ancestor 's songs and the songs of other species as well. As a result, when this population expanded its geographic range and came into contact with certain other species, they might have already been singing different songs . Wecan test both adaptationist and nonadaptationist hypotheses for the unique songs of many songbirds. For example, if song distinctiveness is the product of selection for the ability to avoid confusion about species membership, then we would not expect closely related species that live apart to sing particularly different songs. If, however, distinctive songs are the nonadaptive effect of genetic changes occurring during speciation, then closely related species that have evolved in isolation from one another might well sing quite differently. In fact, some pairs of related species that occup y different regions do sing highly recognizable songs (Figure 13). If we could be confident that, say, black-throated gray and yellow-throated warblers did not overlap during some part of their evolutionary history, these species would provide evidence that geographic overlap among species is not necessary to produce species-specific songs . TI,e nonadaptationist by-product hypothesis also yields the prediction that the songs of species with partially overlapping ranges will not be more differ-
Great tit
38
Chapter 2
Black-th roated grey warbler
Yellow-throated warb ler
13 Geographic distributions and songs of the black-throated gray warbler and the yellow-throated warbler. Althoughthe ranges of these two closely relatedspecies do not overlap, which means that they probab ly have not exerted selectio n on one another
for distinctive songs, their songs are nevertheless very differen t.
en t in the zone of overlap than elsewhere. In contras t. the adaptationis t species identity hypothesis yields the prediction that when two species of spa rrow o r warbler have partially overlapping ranges, the songs of the two species sho uld diverge more in the zone of overlap (where confusion abo ut species membership is possible) than in areas in which only one of the two species occurs. Two closely related species that coexist in only part of their collective range are the blue-winged and golden-winged warblers. Frank Gill and Bertram Murray reported that in the area of overlap, the songs of the two species become less variable, and thus more distinctive [432]. As a result, the potential for female confusion about the species identity of calling males is presumably so mewhat reduced in the places where the problem of recognizing singers might arise. However. the two species regularly hybridize in the zone of overlap, suggesting that the differences between their songs, which are very substantial thro ughout their entire ranges. have little to do with preventing hybridization. In addition, two other closely related sparrow-like songbirds, the indigo bunting and the lazuli bunting, do 1101 sing especially differently in their zone of overlap in ebraska . Indeed , where they live together, a male ind igo bunting may learn and incorporate song elements from a lazuli bunting neighbor, and vice versa [364].And yet hybrids between the two species occur only rarely. suggesting that females have no difficu lty telling the species apa rt despite their song similarities. The few other bird studies on vocaliza tion and spec ies identification also fail to support the hypothesis that song differences are the sole. or even prima ry.
NsOo for Itw .obibl)' "t ~.-.t ~ A 10 idmll~' ....drs.-.t ~_ A 113, 2lYI 1 n..... thrre il; ........... IdoubIlh,ot tural ...-I«b<Jo, for ~ ~ _ hal. pI.a~ 1Wlnl~·. Ald>ough morl" "'".... lSll'qUifl'd I ...>rt OIIt m. ....rious rJutior",,y hypo"ho...·" thdt "'pl.lin thIl mut:.ahont in m. pet that ~ ~ ~. on InnaJ,oo,; would disruptN.-.....J ...·arUn do.'\-".\(lpmo-nt. Of~ p"-" d ~ Of TN _ I cal\' thaI mr,.- ........ """''t>.'d a~;nst. <JpiG. oing "labor.l and comp.... 16'l, 242~ ~ INI tIwft ..... no inoup< rablo> de\~1 constraint> ... dw pr0duction oi ..... ....trol ~......... in "",,,,1.0 bird bra ...... I pre;rnI >nadapIationist h~ pctt>t_ henT\.'h, '" dbl",l lho.'i, fighting ab ility, w "ming OlM "",1",,1 could ..",e bnth the signak-r and hi, ne il'>hbnr time and t"!It'rgy. If the abiUty to learn the ",mgs, ur ekments ul lhe """,-term npuldtion, ""ng m"tehing and d iol,,dick'd 10occur. aod lhese lca mi ng-p m/ici.m t mal.... dn have dia lf:l ing efft'ct!< ol tht'St' highly "",,'lured. evt"'ls ,,",ull in the production of a song ct"'ln,1 sysltm . The w"y in which thes syslt>ms can ""'p'md It>e.peri""fl<e ~ Ind . x_ "'nc p«>vided by i' s eviton""",t, The """. dilf
_ ,< 'p'''' """",...
!
diU....n' ... mongind;v;du.l. ,~..__d ," d ill,'''''''''' in " '"' " lUnd of ...."""""'. Th"" "n~
...
. ., • ..
~ r..e-
0 6
Pinkcockatoo ~
..
Galah
.~
-
,
.
.-
',
~
0'-------- ----'-----------' 6
5 4
Galah feared
by pink cockatoos
..
,
~~'----
3 2
Pink cockatoo
O L - - - - - - - - - - - - ' - - -- - - -
J
2 Time (seconds)
3. We observe that a white-c rown ed spa rrow's spec ies-specific so ng is more similar to that of his neigh bor than to his father's dia lect. Catego rize the following hypotheses as "proxi mate" or "ultima te."
a . Young ad ult white-crowned sparrow males try to match their song as closely as possib le with that of the ir neighbors. b. Whi te-cro wned sparrow males possess genetic information that influences the development of a biased song learning mechanism.
c. By singing the same song as his neighbors, the young adult male more efficiently deters invasion of his territory by those neighbors. d . The hormonal condition of the young adult male predisposes him to lis ten to and mimic the songs of his territorial neighbors.
e. Those males with the song flexibility to mimic the so ngs of their neig hbors have in the past attracted females more reliably than males wi tho ut this abi lity.
Pro ximate and UI\lmat e Cau.e. of 8"h.. io'
4. List "",'~rol w~lI - l<nown f.atun'> oflangUdIl" learning in hllltW'lS that .... simiI., 1 tlwsequestions, infonnation in an y of Iha>ive some differenl informalion from the othl'r IM""'t that h.ls difu,n;nt dev~loprnental e!fental gent'S has the ron""!....""", of prod ocing a compromi.., d..vio>, which cau"," the bini, tn 0";""1 halfway brent speno,.nd as a result. DZ twins ano no m"no similar lI.......lically than any other pair of fuU .iblings. Anotht.,. way 1n' the d,')\"", of !':'-'nctic similarity of twins i. 10 con· sid", the pmt>ability lhat DZ twins. as oppus...... '~t"""l ~ IItftu. IPnCl'd nrol <W\Iy by II""""" bul also by ""'-'nwi".u'.,il, ..-hidl inhir wrists, n ·.>d "",,,,,~i"' fn"" bad . to front dip bu",-.....J 1"... 1 in tlw-ir roIf...... nd h.lv.. hiKhly .imi!... P"'"""",htio:-s" t5J01A -ruJy ut mo.",' Ih.ln ~ pooirs of \tz twin> ......n-d dp.lrt d,""'_tra "'" bt.-yond ......... ""' b~ d""hllh.lt !\""" ri, difft>rt'oces an' n 'Sp'",.ihl,· fu'" .i"" ificant porlion o f the d ifl.·n........ alTlt"'KI",rna n "'-'inKS in pt"""""dity, It'rnpt' r.. lTIt'll!. and social .tlitutl,.. [1:\1). For eMmp k-, when twin./ilkotl ,,,,t ..Lobor..tt· q.....linn_ ""i..... d... iK",..:lI" rnl\'id,' '1" . n lita.ti ,·e m ea.~u n.. of p" """", lity I... its (e,g., ~ C>i ,,,,,p,,r.ri",,,,,,,,,,. ...ri.-.bility. and "" on). thto "",,,.. "f MZ twins "-,,,m:l .. pa ri w.........., ~ mo.""similar Ihan tlw "",....",>1' lJZ twins. whctht-r II..siblinK" had ~ rt>d .part or logt"ll.". Tht-~ oIlt>UUy un....Lared pa irs oi ind,vidt.tolb w.-.... mud> Ir... sintilM Ihan moo- of lWim. "f .ny sor1.
..
5
Iden~
twin. _
....t . t birth:
Jo livro in adopliv.. hc1U"~ hc,ld. lh.ll w...... 100... similar than th05; could haw chan· nd."" Ill
""tali,,,,
n...
TABLE 1 Famil",1 COrrelalions for lQ seo","" PrediC1l'd value . ba sed on the genetic differences h)'pothesls and the aClual corr"lations "",,,,,1 medi.n
cOfrelltion Id""lic.1 (lt...1,1""ti
0.1~
Sooo"",,· !loud .a Rt and il-kG"" (137); 8oud",RtII :>l1
57
ilies of ",,,,,,,"' live; pnw id es "" opportunity to dop! ~ 05
i,
O.
" O.l
"' T~
AI>enolYPmoso" 'es of D""""I>hila mrlaN08a,11'I" [301>]. Man y olhe , single·gJId with
ha,-.
%o,
eJ 10 th.,- 'p,,·.d of all"les .nd assoc iak'lhe ....prod ufli'·e su""",," 0/ individ· ua l, livi ng tod a \'. Th~ i""I'S typi· cally ",,-'CUrs at I"" ~ xp""'" of nth..,- . 1I,,1.... wh.,,,,· dimi""tion "odoct'S !I""ing to d iff,-renl pia ....., lho;- population, a"oid cornpchnp; for wlnt"r food wilh bla ckcap' el",where, which «mid imp"'v~ their cha """" of m"king it lhrou&h tile (and lis . nd,' of th.. dgl g,'nc) could be' at all advantage, but in low-densily f"'p ula ti,,,,, whe", It."f i, abundant, tho., ,ill,-.. (an d lhei r diffe"",t alJelpI,;, rlrgou;, whim "",upi,,, mU
70
19
Chapter 3
100
Response of newborn, naive
garter snakes to slug chu nks. Young snakes from coastal populationstend to have high feeding scores (e.g.,a score of 10 indicates that the snake ate a slug cube on each of the 10 daysof the experiment). Inland gartersnakeswere much less likely than coastal snakesto eat even one slug
cube(which would yield a score of 1).After Arnold [441.
• Inland • Coas tal 75
-
~ -'"
•0 •
'0 0
50
ec
s0 0
~ 0 c,
25
o
2
4
6
8
10
Slug feed ing score
Arno ld then did a heritability study of the sort we discussed earlier in the context of human twin studies. By comparing the tongue-flick scores of siblings, Arnold determined that within each population, only about 17 percent of the differences in responsiveness to slug odor stemmed from genetic differences among individuals. The low heritability of tongue flicking within either population simply mea ns th at th e behavioral variation that exists within ea ch population is largely ca used by environmental d ifferences.
20 Atongue-flicking newborn garter snake senses odors from a cotton swabthat has been dipped in slug extract. Photograph by Steve Arnold.
• lnlond
• (""...1
lhan Inlan
,
!
,,,ltOO ,..
Coa'lal .nal<e1lO rn>m the two populations should 1'\"""'01 .... ulling gnlUp 01 hyt>rid oH';pring Arnold c""duc!.-d tlIt- appn.. prialJ'undant food """,,uree in Iheir new habitat. 1/, as a ....sult. thdr ....producti"'" sucn'," wos as little as 1 perrent hll':h: of di""'W""'" fn>m the inland populati"" in Je",; tl\dn lO,lnJ yeal'>, II is easy to imagine why .lug-ac"llUn:.. of p"'h'l1hal food. But why w'lUld slug aCCt'pt{)f'!; be ""arly eUmin.,!lif"rnia bul plt'l1tiful in inland laks. Leec'hes can survive ~\''''' aftt'r ",-,inll ,wallt>""oo l>y a garlMlt phoen< ltyf"'" in the two a",as [.wI. Ilecau..'ie !\dlUral ",k-ctin has act.", in diff.....,,1 directioru; in the two populations, ho.,rroilary and beha vioral diff"""""," now ..harad,'riz.. s.n.lkes from II>trate thot. particular .Ilde eontrihut.... t'" the d'-"Velopmenl of. heha,·ior.1 ehoracleri;he i; ""t h, ..y thot the l ra il is "l'\t'oehc.Uy delermined. The statemml, "1l>e1l' is .n .nde lor slug """'plfor e.ample, is .h"rthoO lhe d",-'eu'f'ment of the physiological mechani.m. needed for the ability to ~ni1e .Iugs.s I.-.d. " H
''''''',H
2. R""",..... hers in heha,'i", genetics ho"e d"""h-.ped many w.ys 10 I",t the
hypothesi. lhat s"..,..ifk hehavior.1 difw""",,,,, betw""" indi,-iduals ..... cau>;-------Qn heha,-~".I development ha. be of C.lifornia .p......r 10 have 10.'tenliaJly re""lt in • difft..renL" in rnounldinclimbing beha•• >r betw,~", Iw o pI'Opk'?
S. Two diff"""" ,,",'haviorallraits somelim", ","" , that tho.'Y sought out? If "-', d..,..,;it ""''''' .."..., to ca tegorize the beha,;ur~1 diffr'rnct's ~ffi("'g propk, 0-gy, ~nd eeoIogy of go"''f ""''''' feedinp; bt>h''''ior is a cLtssic IHI. n-.., altemativ... h )1'...... h,mn"""l dlll.."'''''.... th,'n ",~lal.. th.. """ul ling d~velopment ollhe ,;ong nm,ml d.-.:u it.y in th bra in, 01 ma l.. and fema le birds, The ,;onf: conlrol syst..m of lhe Ilir "'-'Ul\X\S a... not ""f'C"'Of to l,,,,tost,,,,,-lfl(','arly in lit.? A, a n'SUit. adult f""",J..", a", not ",..dy "0 'AA"""lve a, mal,.,.. '''-IT d" they attempl k' ">pula '" with ",tmus I..ma\e-;. althuugh they will ""f",nd appn>priarely 10 "" ually in_kod ma le;. If it is lrue t:h.'1 the- ho.monal envinlfllllt.'nt within ...,U" d,'!t'rmi",.,. !ht' d..""I. op m..ntal f,l t" of tho.' m,'mmalian bTain. lhen th~ ,""x "I a male's sib lin", in hi, mo lh,'r" un-rus ran \>I' predicled In afled the d~g""'lo which hi" ..mbryonic bra in will be masculinized , In a litle. 0/ mou"" ..mbryos, som ,' m,l jc cmbryos will by chanelWS c.",,,-'n>nr""
_'ti,,"
Th~ D ~ vel o pmen !
of !lehav ior: Envi'onmenl
79
1 Effecto of hormones on the de~_nl of m a le behavior In m ice . (A) leYeI. of e .t ' od;ol, a lem.~ ho<mone, a,~ higl>erin lhe amniolic fluicl 'u', rouriclir>g e mbryonic oM maleo (..ndwid.ed bet .... " two si",on) ,han in lhal ,urrouriclir>g males IbelwO'en two ,",01""").(81 At l month, of ~,oM males a,., Ies. likely lhan 2M males '0 . ",d , ,,,,tl>e< mouoe wt>en ~ed in a" .,.",a wilh !he fof e ighl lo-minule Ifla l' """ad _ , 16 days _Theoe res" of , ggre>sio _ condles could be attribul.:d 'oldy to tlw- effects 0/ early uterine p'",ition on brain d,'wloptrl.1n did O~1 femal... (Figu re 2) [1287].Si"'e m,ll" OOU'"' mice typk ally """1-'1.>1)\'" hom" Tang... INn femakos, lhesI-' n.,;uh . ,ul:I;,"'1 lhal f"m ales balh,:d in ",lati",,]y high cnn,entr,tions of It'Stostero,,,, in m.:ir mot ....' ,'s ul,'TU' arc beh.WiO',llly ma'lCUlinizlopm!lCI-' these chemicals ha.... ""trt of its mtemal ",Uu l.>r ..... vironment. ThI-' ger",-h",m,,,,,, intetacli""s lhal lak pIa"" within mo"se cel l. pn>Ju'" ,'il"'". a lTtd'lCUlirtild or a kminiZ""''''
.."
.... .ao
s
,
;: .1.I: i>ed ""'bryorIill of. ' in gle q"""", who lays mo,,1or an of the eggs in her hive. At first. ttlt' young wo,kers feed the larvae thai h.1tch f,,'m the qUl'
~ . I OJ>"'4'I'I
of WOfU< N hav;or in honey bl!e..
1M 10> up of " .. Iy youn[o\ w". k~", . Thit tt... d"""lornwnl 01 {,.....ging h>h.o, ..... b;oa.- tr.""f'IIInb of )""'..,,,,,,",,,",, hII,... no f'fk-c1 nn Y"""K ...........1t-s_ n..... tt.. ...... I... ' ·irorvnnu of ~ ""-Y 1>0. ~ inti ... ...-..:."'!I tho;-;. h>h.o"iorAI .t.....1opmnlly wIo•...J l>lad " ydk,w. N ue. iU\d It'd mall- thai m,i;"g'oIo-. with d>ange!; in neural stru.lNIa!I)r w,th ib poft'Ttl!,. .....~ . irnpon.vtt dn .... 't",wntal and btfy,ior.ll ~ KDnradLo........ ht-If""d •••I..oh.,," this point by ..... rinj!: a clutrt> lho: ttiltal ttl'Sl odor, .nd to behave I,,,,, lol placed in an a"'na in pairs ,md !\iwn a chart"lUnd"'lui"..ls 1543J. But pem"ps the most ..."",.Iulble finding of Ihi. study ....... 1""1 biolo!,>ical sisk rs "",red al'art engaged in lewe. agg ress ive interaclions than nonsibling. reared apd,t (Figure 13). In otN.'1' words, thU"•.,
Si"""
1] ~ jn diocrimina. ion in B.lding'$ ground 'Clul" "I.. "",red apart di~ signifincr' 01 sharing a mother and a burrow [542, 544[. n", """"hanism lU,derlying l in discrimina tion by female Bddin,,', I';TOund squir",Is and other animals [;l,' tlwm ha. I;,.,,·n laho,l,oJ p h" nutyp" m at" h in!,: by Warn'n Holm,,, and raul Sh,,,,ano.o w ....... Kiv...... ch.ooce to in!;pect flank K!d.nd ",,",,10 'rum b",lh uu,,"""l rub their Rank. glands CI'\'« the oot>IIn« odor. lFigwe ' '-),.ppIying their """"IS w."""l! 0Ip0lI to r t olIwr iridi,id..... not II;> rome _ them. ~ m eop
n
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Evolution and Behavioral Development Our ...·vi~w has cov~r-~'rl\'ironmet1t intt>ra1: be pnwamJTl ,·ff,'Ch when lhey ma lfunction. For exampl,' , animals ..",,,,Ii,,,,,,, use ""pt.ri"",-" It, modify their be"'",ior in a way thai lowe... nol raises, Iheir fltn,,,,, Suppose. for e.ample. Ihal an individ· ual ,>bserves others and . dopts their solution to a behavioral problem (e.g., the palh to I,'kc- to a ft'Cding ,in') wh.·n it could d" better by adopting a di/f.·...·nt ",Iution (".10\.• it could Iravel t" the slle moll' economically by another n",l
Given lhe co>!>; 01bt.-havio,al f1~~ibi hty, w~ would ""pt in 'pe' the "" me-,iz,'d living spac,·. When te,led in a varicty of mal''''. which the an im.lls had tIl ."k~ in "rde' to "-"itic ",laliw, of thi, ,.",c;"", [105(1] (Fil'''ll' 25), SirniLuly, a~ the South Am..,kan ",wbirds, bll'l'ding !pe'ant> (m nning. turn ing. ,.aringl m., _ r. oq ua lly rewa ,d«ll' "-e ,a" _ '" "'" m od «l when !t>oy ~ ,Iormed ~ a ppm p. " " opene' .tJnd upn!;h! in the runnin!; wl1nal to (1) the inten,ity 0/ lhe ,""ulling ill",,,,, (2) Iflci~Ii,,,,, thi>t neeur in ""tu...,
The Evolurion of Developmental Homeostasis Our ~nalpi, of lhe 'ped~liz,'un..-l "'luim'l, ht'lL"..i in an enclosure dllring U", day without II..,;, mothers n'aCt with int"",a......J \'Igil .....:" 10tapt...l "l"rm c~II, nearly a, often as yOWl!:"te", who haw tho.' """"fit of Ii'in!,: with tho.';r in Ihe "'''''' k.ind of e",,"...ul'lings
"'' 'I':-
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104
Chapt er 4 (A) Normal
~
_
Visual cortex
(B) Rewired
Superior
~
_
Visual co rtex
Visually responsive auditory cort ex
colliculus
MGN
30 Rewiring th e ferret brain. (A)The optic nerve normally runsfrom the retina of the eye to connect with the lateral geniculate nucleus (LGN) and superior colliculus;the LGN then sends messageson to the visual cortex of the brain.(6) In some experimental subjects, researchers were able to reroute the optic nerve to the medial geniculate nucleus (MGN),which normally receivesauditory inputs from the inferior colli culi (these connections had been severed in the experimental anima ls). In the rewired animals, the now visually activated MGN sent signalsto a part of the brain that servesasauditory cortex in unaltered ferrets, providing thisstructure with visually derived information rather
than auditory information.After Sur et ai. [11, l l-
wh en less than 2 days old and fed artificially for 3 weeks still approach scents from the anal excreta of female rats, just as naturally reared rat pups do when temporarily separated from their mothers [415]. Male crickets that live isolated from their fellow s sing a normal spec ies-specific song despite their severely restricted social and acoustical environment [91]. Captive han d-reared female cowbirds that have never heard a male cow bird sing nevertheless adop t the appropriate precopul ato ry pose when they hear cowbird song for the first time, if they have mature eggs to be fertilized [623]. The ability of animals to acquire the correct prox ima te foundation for normal behavior, eve n under subo ptima l condi tions, has been called developmental ho meostasis. This phenomenon has been dem onstrated experi men tally in several ways. For example, a team of neu robiologists managed to manipulate the de veloping optic nerve of a newborn small mammal, the ferret, so that the nerve split and grew tow ard tw o destinat ions, the visua l cor tex (its customary contact region , which processes visual informa tion) and the auditory cortex (Figure 30). The au d itory cortex typica lly makes sense of sounds, but it could not form its usual connection to the auditory nerve from the ferret 's ears in those animals manipulated by the researche rs. The question was , wha t per ceptions would the auditory cortex provide in response to sensory signals from the op tic ner ve? The researchers fou nd that the rewired ferre t used its auditory cortex for visual analysis, not for hearing [1040]. On the one hand, this result is stunn ing testimony to the plasticity of behavioral development and its potenti al sens itivity to experience. Cells that ordinaril y would have been emp loyed in the pe rcep tion of sounds were ab le to change their apparent de stiny, becoming pa rt of the visua l sys tem of the ferret. The genes in the cells of the presumptive audi tory portion of the brain clearly responded to visu al messages relayed via the op tic nerve and subsequently dev eloped along a mu ch d ifferent pa thway than if they had been exposed to signals from the auditory nerve. Both the structure and the function of the "auditory" cortex in the expe rimental subjects differed grea tly from the typical pattern [1040]. However, the study also paradoxically revealed developmenta l
The Develo pment of Behavior: Enviro nment
lOS
homeostasis at work. Brain cells tha t wo uld norm ally never receive a flow of visual information from the optic nerve neve rtheless had the capacity to respon d to that information ill a [unctional mallller, forming circu itry tha t provided the ferret wi th visual images, not chaotic gobbledygook. The ferret's developmental mechanisms had the ability to ove rcome a highly abnorm al experimental environment while generating a brain system capable of carrying out an important task, the visual analysis of optic nerve signals. The same ability to cope effectively with an extremely unusual env ironm ent is eviden t in the development of the social behavior of young rhesus monkeys reared in extraordinary social deprivation by Margaret and Harry Harlow [493, 494). (The Harlows' experiments were cond ucted in an era when animal rights were not the issue tha t they are today; readers can decide for themselves whether their harsh treatment of infant monkeys yielded information of sufficient importan ce to justify the research.) In one such study, the Harlows separated a young rhesus from its mother shortly after birth. The baby was placed in a cage with an artificial mother (Figure 31), which might be a wire cylinde r or a terry cloth figure with a nursing bottle. The baby rhesus gained weight normally and developed physically in the same way that nonisolated rhesus infan ts do. However, it soon began to spe nd its days crouched in a comer, rocking back an d forth, biting itself. If confronted with a strange object or another monkey, the isolated baby withdrew in apparent terror. The isolation experiment demonstrated that a young rhesus needs social experience to develop normal social behavi or. But what kind of social expe rienceand how much-is necessary? lntera ctions with a mother are insufficient for full social development of rhesus monkeys, since infants reared alone with their
31 Surrogate mothers used in social deprivation experiments. This isolated rhesus infant was reared with wire cylinderand terrycloth dummies as substitutesfor its mother. Photograph courtesy of Harry Harlow.
106
Chapt~r 4
Socially i50l~ rh~bi,'S ,t....1 lo pl"y wh,'n th]. [),oalh.~ In,m sLlr\'dtion were c
homeostasis in
h"man•. Ma'e.-nal .to""lion bo' ,u,pri,ingly _ on in,@iIo Dutch inl~lligt-'n",' n..t administered todraft-age ""-",, Child",n t'om ~t low weight' apparently suff.. retl no perman.'nt intellO'ctual dama!\" [lll%[, n- "..ults dl"ec'au... our devd"pmental systems ",",,,lvOO in past ""vi,,,nrn...,l, in which episod.sful."'vironmt'f15 "-,,tifies to lho> adapti"~ly ~id...d. stTuctun'tl nalure e>f the p"""""~, whidl can bt-th,,>Wn "if "nurst'only by e""-'mt'ly "nusual '-'"vim",,,,,,,"'1 shortf.111. or . .." ...... gcil)' 10 ((lfI'I""",,,lry_ In the bun $wl-1low,ror ........ ~. f1."ftl.ole§ I\a,... bHtl ... pooto;d to p,""," ma~ "'''''-long OUIrr uillNm...-.. ..... t\wo ....... ~I\ IlC7I. ,,'hi.ko Iom.oJool. of the IbnWn roc~ liurd -e.."" pI< futiltiaUy ,,-ith ........ mdowt'd " 'ith .. ~)...... mr1rir.al distribution of pht'OOI .... W-"*-ing ~ oro thrir thiKhs [762~ M lor I\llfI\aN. 00iIW ,""",trlwn 1\.0,.., lepot It'd Nt both ...... and ........... find $)...... -uy in 1...".1 INIll......f'f"NlIng (Figu Tl' :H) 1557. 'N>71-l'ntwf"" p""'f"""'li... malt'5 in t/ww and othrr ~ respond J"'!'ib..riy 10 body or 1..o.tI ~)mR'W' try to«.a...... !hew .lIribub:o ."""""'-" the individ..... l·s c. p.oocity to "".1."fCUIt\e ch.1lIen~ 10...........1 dt'\eIoprnent 18101. o;""pIh_ to dto\'~1 c• ..-I by muution> or by an inability to """"'" cribciol malffi;tl rJy in bl..... thoughl to gm.-r.lrtl.'d • ........... ~ "1'jc>j." matinj; .od,..... ~ in _ ~ I...... abrJo,' ej, in othrr ~ no ouch ad.- .. n~ "'" t>e.>n ot-r,'ed 1t.'l8. IU7J 1_ also 188111, Finany. in """'" "f""cie.>n '"poo.. 0. t\wo ditt. , $ beny eIinunoollng infotrn.ltion.aboul l....w _pnll'll"try, n-.....wls ""AA""'l thot faci.oI sytnrTlt'try must~ ......th ."trW nttwr fNturr lhoI-......... -...tty .- to m.k IhtV judgmonb 11021 ~ ~, ....... ~ ... OO piotofbo.. and ~ et>or- ~ I rn.>Ies withoul ........ loo>t."'!i: .1 thorn. In;b>ad. tht'Se .......... ls ...1Kt ma ..... "" tht' b....ts of po'""",,,,,,,,l or ........"'.. 1"11;',,01. NI ""ppm It> bot nP
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only "f tho.· t~r;., l n.'!oOu rn-s il """,iv", ..nd I..... m~t.bo,l ic rn>ducl•. '""I'dUAlo. In .._ c.._ •.....,; in the' ACI" 1' ......1'.... &,\ .. I",p..w.,ul pootllw.., .. lNding 10 di~' ..rructu l .and twIt.o, ·;o..J phdA......t.oll)1Ild"idu.als ...mg.....uin lutid. oI ....~ to modi/)' thrpbmOI'""',""...... " b. n... ~.M tIw
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Sugge§ted Reading R" b inson di".:"..- the int,'gr~tion 01 molt"",la' biok>gy, vior 1m, 9741 · Da"id I'ft'nniK and raul 5I>'K-w t..... fa"';na ting subia"'! of kin Jt' [~101-
{";ene
The Control of Behavior: Neural Mechanisms
hire-crowned sparrows sing because they have a song control system, a set of interconnected neural modules embedded in their brains (see p.28). In fact, every aspect of the behavior of a white-crowned
sparrow, or any other animal with a nervous system, depends upon the operation of its neurons. Some neurons acquire information from the animal's environment, others process messages from these sensory cells, and still o thers send out commands telling the body to do something in response to these inputs. Fig uring out how neurons and neural networ ks complete these three tasks is a maior goal of those persons interested in the proximate mechanisms of behavior. Some phy;;iologists have tackled this problem by focusing on how single neurons in the chain of sensory, integra tive, and command cells ma ke their contribu tions to particular behaviors. These researchers have asked questions such as, what stimuli C.1O a single receptor cell de tect, or, what gene products are produced within a given neuron
.piOO>oC would invari.1bly acti\'at~ its ''g,g ",trio.·val=pon"', And if the """'archers """""ed the obj''''la, it was t.eing "'tri""."j. the bird would coo·
tinue pulling it>. head """k i"-'I a, if "" "AA w,,", still b.olanred al:airu.t tllt' und~r 'ide of ii' bllllllJ6). From lht>so> results, TUlbergen and u,,,,,,-, rondudt",,1 mt'1'nT I\'lea",r, in""t
"'"1""''''''
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4 ... relea...r. ""......n trig'l"" yawning in o'he< human, lllal _ tho yaw"",. f'hotO<J raph by Ch ri,top/le-r Small.
.J""
The Control of Behavio r regurgitation of liquid food (an FAP) by the an t. The larvae eventually metam orphose into adult beetles, which can still elicit food transfers from ad ult wo rker ants by producing the right releasers for this situa tion (Figure 6). Likewise, the chicks of avian brood pa rasi tes, such as the Euro pean cuckoo and the orth American cowbird, take advan tage of a simple rule of thumb that parent birds use to make decisions about whic h nestlings get fed [487, 1228]. When an adult songbird returns to its brood wi th food, it favors cheepi ng youngsters that are able to reach up high, with head moving an d mouth gaping. Cuckoo and cowbird nestlings grow rapidl y and become larger than their hosts ' own offspring. and therefore can generate these releasers of parental feeding better than their smaller nestmates [695]. Because the parasite begs for food very effectively, it ge ts more than its fair share, eventually growing into a demanding youngster larger than its foster parents (Figure 7).
119
Releaser
(visual signal)
SensoryReceptors and Survival Although resea rch er s today ra rely employ ethological ter ms such as fixed action pattern or inna te releasing mechanism, many behavioral biologists have studied we ll-defined responses to simple stim uli in an effort to figu re out how certa in neurons contribute to an ada ptive behavior. Conside r the classic wo rk of Kenne th Roed er on the ability of night-flying moths to evade predatory bats, something that you too can obse rve on warm evenings in temperate North America if you hap pen to possess "a minimum amo unt of illumination, perhaps a lOa-watt bulb w ith a reflector, and a fair amount of patien ce and mo squi to repe llent" 1976J. With all these item s in place, you may see a bat burst into view and swoop down up on a moth attracted to the light. But you may also so me times see a moth turn abru ptly or d ive stra ight down just before a ba t shows up , evide nce that at least som e moth s are able to detect and avoid these preda tors. Moreover, yo u can so metimes trigger an abrupt turn or precip itous dive by a flying moth sim ply by jangling a set of keys as it flies into view. This response suggests that the moth is de tecting a simple aco ustical cue that provides the trigger for a particular beh avior, just as simple visua l cues are sufficient to activa te begging beh avior in a baby gu ll. As it turns ou t, the hypothesis that aco ustica l signals trigger the tu rning or diving behavior of moths is correct, bu t the sounds that the mo th hears when the keys arc jang led toge ther are not the sounds tha t yo u an d I hear. Instead , the moth detects the ultrasonic stim uli prod uced by the clashing keys, which makes sense when you consider that hu nting bats produce ultrason ic vocalizations with sound frequencies between 20 and 80 kilohe rtz (kHz}--well outside the hearing range of humans, but not moths. Bats use ultrasonic calls to navigate at night, something that was not suspected until the 1930s, when researchers with ult rasound detectors were able
6
A code breaker. This rove beetle mimics the begging signals produced by its hosts by tapping a worker ant with its antennae before touching the ant's mouthparts with its forelegs.These actions constitute a releaser of regurgitation by the ant. which provides food to the parasitic beetle. Adapted from a drawing by lurid Forsyth.
Innate releasing
mechanism
5 Releasers,innate releasing mechanisms,and fixed action patterns . The red dot on a parent gull's bill isa releaser
of the gull chick's begging behavior.The chick's nervoussystem hasan innate releasing mechanismthat respondsto the releaser with a fixed action pattern- its begging response.
120
Chapter 5
7 An exploiter of instinct. A young cuckoo begs for food from its foster parent, a reed warbler, which provides for the cuckoo at great cost to itself and its own offspring.
Photograph by Ian Wyllie.
to eavesd rop on the steady stream of high-frequency sounds produced by flying bats. Don ald Griffin su ggested that the bats made these sounds in orde r to listen for weak echoes reflected back from objects in their flight path [459J. This echolocation hypoth esis for bat navigation initially had man y ske p tics, but they were convinced when they read about Griffin's experiments with some cap tive little brown bats, a common No rth Am erican species. When Griffin placed the bats in a dark room filled with fru it flies and wi res stru ng from ceiling to floor, his subjects had no trouble catching the insects whil e negotiati ng the obstacle cou rse-u n til G riffin turned on a machine th at fille d th e roo m wi th hi ghfrequency sound. As soo n as the machine-produced ultrasound bombarded the bats, they began to collide with obstacles and crash to the floor, whe re they rema ined until Griffin turned off the jamming dev ice. In con trast, loud sounds of 1-1 5 kHz (which humans can hear ) had no effect on the ba ts because these stimuli did no t mask the high- frequ ency echoes they listen to as they fly in the dark. G riffin rightly concluded that the little b row n ba t employs a sonar system to avoi d obs tacles and detect p rey at night. As Roeder wa tched moths evade echolocating bats, he guessed that the insects migh t be able to hear pulses of bat ultrasound. If he was right, he knew he should be able to find ears somew here on some moths-and he did (Figure 8). A noctu id moth has two ears, one on each side of the thorax. Each ea r consists of a thin, flexible shee t of cu ticle-the tympanic memb rane, or tympanum-lying over a chamber on the side of the thorax. The tympanum is attached to two neurons, the Al and A2 sensory recep tors. These recep tor cells are defo rmed when the tympanum vibra tes, which it d oes whe n in tense so und p ressure waves swee p over the mo th's body. Roed er decided to focus his atten tion on these sensory recep tors, using a cellula r ap proach to ge t at the p roximate basis of moth behavior.
The moth's Al and A2 recep tors wor k mu ch the sa me way that most neu rons do: they respo nd to the energy con tained in selected stim uli by cha ngi ng the permeability of their membranes to sod ium ions. The effective stimuli for a moth 's aco ustical recep tors are pro vided by the movem ent of the tympa num, which mechan ically stimulates the recep tor cell, opening stretch-sensitive chan-
The Control of Beh avior
(B)
Tympanum-
/Al
~~~~?~F~=
8
Noctuid moth ears. (AJ The location of the ear. (B) The design of the ear. which fea-
tures two sensory receptors (A1, A2) linked to a tympanum that vibrateswhen exposed
to sounds.After Roeder [976].
nels in its membran e. As posi tively cha rged sodium ions flow in, they cha nge the electrical charge inside the cell relative to the cha rge on the othe r side of the membrane. If the inward movement of ions is sufficiently grea t, a substantial, abrupt, local change in the electrical charge difference across the membrane may occur and spread to neighb orin g portions of the membrane, swee ping aro un d the cell body and down the axon, the "trans miss ion line" of the cell (Figure 9). This brief, all-or-nothing change in electrical charge, called an action potential, is the signal that one neuron uses to comm unica te with ano ther. When an action po ten tial arrives at the end of an axo n, it may ca use the release of a neurot ransmitter at this point. This chemica l signa l diffuses across the narrow gap, or synapse, separating the axon tip of one cell from the bod y of the next cell in the network. Neurotransmitters can affect the membrane pe rmeab ility of the next link in a chain of cells in ways that increase or decrease the probab ility that this neuron will produce its own action potenti al(s). If a neu ron fires in respo nse to stimula tion provid ed by the precedi ng cell in the ne twor k, the message may be relayed on to the next cell, and on and on, sometimes producing a chai n reaction in which action potenti als from distant recep tors have excitatory (or inhibitory) effects that reach deep into the nervous system. Neurons far from the source of the initial action potentials can be stimulated by volleys of relayed signals. They may continue the chain reaction by providing a message in the form of patterned action potent ial outputs tha t reach the animal's muscles and cause them to contract. In the case of the noctu id moth studie d by Roeder, the Al and A2 receptor cells pass on information via relay cells called intemeurons, whose action po tentials can change the activity of other cells in a large cluster of neurons called the thoracic ganglion and in the brain (Figure 10). As messages flow through these pa rts of the nervous system, certain patterns of action potent ials fired by cells in the thoracic ganglion trigger other interneurons, whose action potentials in tum reach motor neu rons that are connected with the wing muscles of the moth . When a moto r neuron fires, the neurotransmitter it releases at the syna pse with a muscle fiber cha nges the membran e permeabil ity of the muscle cell. These changes initiate the contraction or relaxation of the muscle, which dri ves the win gs and thereby affects the moth's movements.
Receptor cells
~ A2
121
122
Cha pte r 5
9 Neurons and thei r operation. The diagram illustrates the structure of a generalized neuron with its dendrites, cell body. axon, and synapses. Electricalactivity in a neuron depends first on the effect of certain stimuli on the dendrites.Electrical changes in a dendrite's membrane can, if sufficientlygreat, trigger an action potential that begins near the cell body and travels along the axon toward the next cellin the network.
/
Direction of message
Axon terminals synapse with dendrites on
target cell
" Axon
,0
Neural network of a moth.
Receptors in the ear relay information to interneurons in the thoracic ganglion, w hich communicate with motor neurons that control the wing muscles.
Thus, the moth 's behavior, like that of any animal, is the product of an integrated series of chemical and bioph ysical cha nges in a network of cells. Because these cha nges occur with remarkable rapid ity, an animal can react to stim uli in its env ironment in fractions of a second . An Ame rican cockroach, for example, can begin to move away from approac hing da nger, such as a hungry toad lunging toward it or a flyswatter wielded by a cockroach-loa thing city dweller, in as little as a hundredth of a second after the air pushed in front of the toad's head or the descending flyswa tter reaches the roach 's body [191]. Although the neu rons of many animals share similar features, the acoustical receptors of noctuid moths perform very special sensory tasks . The moth 's Al and A2 receptors are specialists, finely tuned to collect information about ultra sound, as Roed er determ ined by attaching recording electrodes to these receptors in living, but restrained , moths [976]. When he projected a variety of sounds at the moths, the electrical response of the receptors was relayed to an oscilloscope, which produced a visible record. These recordings revealed the following featu res (Figure 11 ):
The Control 01 Beh.vio ,
'" '
A2 """'F"'"
N"",,'l . ,'tivi' y Low.in!cries of a little bn",,, bot gen..t in spa,,,,. II • hunting bal is on the moth's [eft, for """"'I' ll", lhe Al rt'gi. ~ ~ ~ uI of ~ oct"..,,·, ~'. Of not .. A., .-.It. Ihr u-ct do,... not kno'hrft il is gang-but ""'tiler do... no. puAWf'tg bat, ........... inotoiliry.' "" ~ no. pooth of its f""'r lNy pt'm"t Ihr n.m "" """"'P"" ThO. c_ ..u)" in annlho.·,-in..." t. tl... cricket Trlrosryllu, ,~''''"'''U '' which .11"" fI",,, fn, m "Il,-. .. ,,,n..! pnld .......,'" IM3I· j".I .., is In..• fo' Ilnm lht-se """'1'tors tra "id.mor.-in_ .......not in the-6ll-50 kHt r~. Uw mor.- action poIt:ntWlo no. Ct'IIt prodUr Ih
. . ."'m.....
Loto·ftft s1imul.... and ""'f't""'t'two p~ Wt o:ucth' maid> u..- '" the Al I«....... in noctwd II'IOltb. n...........m. ~ tNt Ihr iJIl ·J IP'" UwIlary J""di.... ...... pt"rilllt'nt> nlOwino;inKly ." tat>ll>oh a ca"",lll'ldtk>r...t"p "''''''C)' (kHl)
.
"n
"lH~1
Tho:> i,,/·1 c~lIs ,m' ;nlt:rI'It'uton" part of !he ",lay ap paralu' 1h.1t "",,lrols which ",'n",'Y ""-""'WS move ftln'>'ard 10hi""", pl'OC\'S5ing """non;; thest(~ ll, do no' ;nlll',va t" th.. c,icket's locom"t(lr~' mu,d", dirKlly. Whal i. Ih" pmx;mdle ",,,to, ml'Ch,ul;,m lhat ,-"ablt... a flying un.." of ull.a-y ,,"'dumng a r, fo r exam ple, the escapt' ocM vio r of a "". slug of the ""nus T,i'""ill. When it comes into con tact wilh a ",I,·. ""r--eht·mica ls ._>d by communications """i"le 01 oeq..ent..l excitatr09,"m _ a"" two mJeIv with the oonic motor nuclft. First t to....rn n",,~ ~. ~ of J-ftN ~ m"ltietwr prodlQ' .I humrnir'l8.......J INI.
The Proximate Basis of Stimulus Filtering mined e>-ompJc-; of ~ ... the .tlribu_ of indi,·id... 1 ......"""'.And r.1 cl""""" that on' inH>l,·t'd in the drhoction of ceruin lund, of .."".,.... inlonnoti n>Ioying of K"'!' 10 otlwr 1. In the ....... 'yolt1lt..nd tho> rontrol "I motor rornrn.mdJ they • ..,. t 10 m.....A urn'·ft'f'S It, the dh;lity uf n"" It, ignrI by "I forms of st;mul..ti"n . M"n~"',... t......' 0.'11. romr ld ely i"", ,,,· "'>l,nd. of l.u i""ly low fm:j"'.....,y lin thto ran~.· thou you .nd I 'dn liN,). Firwlly........., ... lim the A I ....-..ptl ultr....>nic l""'l"""";'' ' 0/ the ......... inlt.....,ry I h""",n ~ud i tot}· ... ,,n""",t-b-u t "'>I """rv. sound. As pn-d i "f ,..."luti"......... . biok>t:i"" , l:Mn iy <Tie much loud.-r if they are to ;\t'fI.'luency 0/ 1d by ",r· win "i,ual 'limuli, proximdle mechanisms wl navigatiOOdl S sky as a dim.iional guide [606. 1175). Even we can do !hi, to 5OInt', ,,k'llt knowiJll!; th.,t ti' demonstratt'd by Ira~ SOIll, . fu'}' h.w.. compenSuKh thi, me" ", th"l 0111t";. 4. The p mximate mech.lnislt'l> of stimulus fille'ing. ", the b,»is for .d.pli"e f"'f<epti"" and .d"pti"e ....,ron,-..·s. By di"".rding some poI,'ntial inform.· tion, .nim.l. a,.., .ble to locux "n the biologically rele""nl stimuli in their en,'ironmenl. incre••ing the odds of a pn>mpt .nd effectiw ro>ctiooto tI....5C key stimulI. lk"C. use lhe ob.t.c1... to n-'Producti "e . u""""" d iffer . m ""l\ sp~d.,. . ..,!n.4ej.,"" When the ears a... fully t'f""". the ....tydid·, a"ditOW might ""lectK>n p.....ure /n>m par.sitic flies n.,·e Cltl1tributed h> the "",~ulitngraph on the ne xl 1"'1"')' H,>wwUld roo It'St the hy'
The Contro l of Beh avio r
pothesis that fiddler crabs hold their eye stalks in this pos ition in order to use the following sim ple rule of thumb: Flee from any moving stimulus that appears above the level of the eye (at the top of the stalk) and approach or ignore any mov ing stimulus that appears below eye level? After answering, check [687]. Apply ethological terminology to this system by identifying the releaser, the fixed action pattern, and the innate releasing mecha nism. Photograph by John H. Christy, Smithsonian Tropical Research Institute.
5. Cortical magnificati on occurs in human beings as well as in all other mammals. The drawing below illu strates a represent ation of the amo unt of co rtical tissu e
devoted to tactile inputs from different pa rts of the hum an bod y. Provide some hypotheses on why differences exist betw een our cortical map and those of the insectivores discu ssed earlier in this chapter.
c
I
151
15 2
(naple, 5
Suggested Reaaing Kenneth Roedt-t' • ." tttt 1111. and In Sl'd BthmIiot [976! is a das:;.ic on how to ronduet """,rch on the pllysiology ofbellavior. Mod,,", lexlboob on the l"lI"Uf()o physiology of beh.>vioT h.>ve been written by Jeffrey Camhi 1191 L Peter Simn\OI\!; and David Young [1063L and lhomas CaA'W [194). For anal ysis of a lIigllly specialized Stmariarl an! ready ra rIla' 'hoy """" al""'" rIO in thrir b/oad.PI!ooi<jraph by FrIl~ 1 Goh/6
r..,,,,ttr_
wa y. Instead, a male moth usually aborts his flight toward a source of female sex pheromone when he hears loud ultrasonic pulses (31. Thus, the mille gives precedence to avoiding bats, thanks to his neu ral networks.
The .ability 0( ..........Ol».ond endocrirw sy._ ttl molo.r o:hc>icw oIlhi!>!IOft is ltw and adjuolltw pnon_ 01 compe!ing conurwnd <Wftf'n"
......m
How Neural Command Centers Organize Behavior Il«auw moM ........1o Iw"...1tw ~·IO do.....-.y diiteRnt thqp .. 'Hf'O' .... 10 1n/II'l)' ~ otunuti. .I..,y gi\'e'l momenI It..,.- latt Itw ~ o( ..-hid! to.h.o'ioo- \10_ _" If' At .., ultinu.1Ir' .....-..1. it is _ ). 10 undf.nound why anim.ll< r.rriJ.·Ir)· to do M'O ltunp .1......,... BuI.I .. rro~inw'" e!. how .... ..nnw.' ....-n...... "'~ ~ 00 that maIadof'b'''' n->llicb do "'" occur' ar... w:'y to ....t.obli.h bdw,ior.1 priorit .... i.. 10 ha,· <Jm .y~try t" ,·~min ma ..... '"; with i'" front pair 0( kog... Ro..der rr<JPd prii\k, ral90n91"'"and ,"-'
"""'~,
De'_9Ong l"", are
cu~ ,"-' ",~a l90n 91"", ...nd, a ", .~m of "",c"a'ry """5a<J'!' '0 the ....."","'al ganglia '" ,"-' 'l\oI'a. alld .bdomen; ,"-' manti, ,twr> attempts to do .......,.1compe prot manl~ walks fotWard, OT . It"ik;,s out with its forelegs. or f1is il p""ibl" fm th,- m""tis 10 do just one thing al a timund,nK"- That such "'Wironrrt1 """"-Id be p!.usibW 10 ""J'O'W who .... flo>o,.., .Kro66 ....·.......1Ii_ WIWII MIdthm lri...t .., adjusI imMl'd"lrtloy an .,n"i"mme"t·ind.....'nd,·nl int.'",al d ",. d i. n rhy lh m ("cirradian·· nu'aos "about a d..y~l, !';ow k~·. pi...... "'" crick.>ts in. regimt< of 12 he"'''' "I IiKhl.OO 12 hau.. 01 d~r~. The switch Ir"," Iighl 10 d~,k off" ... n u! hghto
in"""
"",·,,,,,",,,,,,,w
pe-r."""
«If
*',
cy,'"
u
" 5 CIrucIWl rI>ytMd in mnH aang __ lor. bcl< _ _ ""rtw9'>:!' 'n .... 1Nf:-" '..... won .......
u
"". 2..- _
ouIt.~ - . ondiuoIe ptfIin ..... GnoI,~ThtU.Mrtw lOP_ _ 01rtw t9- _ _ rtw IiI;JhIiII9
odIoI~
""_ lNnl
w
tl-.Ior rtw lInlI12 .,.,. 01 thio '""-'" crirtlt _I<tp: in.--l9tt
.-
lli-.cl b rtw _
thty _ wlljtnne! '''9"lat... 1M m'lJ'Y otl>« me< ha ni"", controlll nq 7
..,."., sp«if.
Sunl i~' at "'"'"
"",·;""""""..1"""'"
which was Known to be. key regul'lory .rea of tht> hrain. n... hrrothal.1mus con tains a stnJctun' calke! the .upraclWsmMic nuc).,us (SCl\:). which ronsists of a pa ir of ""Unlll cl",t Cllm,' from other parts of lhe n,tal hamsr.:.. b.ain [3101. ['em.,ps the seN clock Of""ats via rhythmic chan!."" in 1; ~db/) ....J-!:SIY
d,.. ~ (-!:SIY
,
,,
,, **** C~IE? (tall )
Deg raded
Nucle us
Nucleus
8 Th e g en etics of biological clocks in mammals and fru it fli es. In both groups, a set of three key genes produces proteins that interact to regulate the activity of certain other genes on a cycle lasting approximately 24 hours. One of the genes (per) codes for a protein (PER) that gradually builds up inside and outside the cell nucleus over time. Another key gene is tau in mammals and dbt in flies, which code for an enzyme that helps break dow n PER, slowing its rate of accumulation in the cell. But du ring peak periods of produc-
tion of PER,more PER is availableto bond with another protein (TIM) coded for by a third gene (tim ).The PER-TIM comp lex does not degrade, so more PER re-enters the nucleus, where it blocks the activity of the very gene that produces it, though only temporarily.Then a new cycle of per gene activity and protein production begins. After Young [1275].
tar only during that part of the day when the flowers they seek are m ost likely to be resource-rich . Foragers have almost three times as much of a particular chemical in their brain cells tha t is produced as a result of an active per gene than do young nurse bees [1146].
1-
24 ho ura--r-e-]
§~~3
Wild -type I I
___ Arrhythmic mutant 0 0 o
0
---
c::J s
c::::J c::.==:J c:::::::::J 0 c::J 0 DO
- - - Short-pe riod mutan t _
•
9
Mutations of the per gene affect the circadian rhythms of fruit
flies. On the left is a diagram of the DNA sequence that constitutes the per gene.The locations of the base subst it ut io ns present in three mutant alleles found in fruit flies are indicated on the diagram.The activity patterns of wild -type flies, and those associated with each mutation, are
shown on the right. AfterBaylies et ai. [811.
164
Chapter 6 The fact tha t the fruit fly, the hamster, the honey bee, and you and I all have the same gene serving much the same function indicates tha t we inherited this gene, as well as some others involved in the regulation of activity patterns, from a very ancien t animal that lived perhaps 550 million years ago [1275] . In mammals and other vertebrates, but not insects, the per gene plays its role within the neurons of the SC ,which communicates with the pineal gland, a small organ tucked into the brain. Here too the communication has genetic effects [398, 1095]. In brief, chemica l signals from SC neurons activate a specific gene (CREM) in cells of the pineal gland, a gene whose protein product (IC ER) is presumably involved in some way in the manufacture of a substance called melatonin. As the IC ER pro tein builds up in the pineal cells, however, it begins to inhibit activity in the very gene needed to make more IC ER. (Note that this is another case of self-regulating negative feedback of the sort that appears to occur in the SCN clock mechanism.) However, the sensitivity of the CREM gene to feedback inhibition from its pro tein product varies depending on the ph otoperiod (hours of daylight in a 24-hour period) that the individual has experienced in the previous few days. Animals that have been exposed to a series of "nights" that are 8 hours long show peak activity in the CREM gene about 6 hours after the lights go off; in contrast, animals that have been exposed to 12-hour nights for a couple of weeks reach peak CREM activity about 10 hours after the lights go off (Figure 10). In other words, the pineal gland alters its biochemical output in relation to the recent history of photoperiods that the animal has experienced. This ability enab les the pi neal to adapt to seasonal changes in day length, thereby helping the animal adjust its daily sched ule to these changes.
(A)
Long
L:O
photoperiod
YT!Y?? TV!!!
V!! I
21:3 !
16:8
II
12:12
! IT ! ! ! ! ! ! ,
8:16
TXT! ! ! ! ! ! ! !
321
Sho rt pho tope riod (B)
LO
Time (ho urs after lights off)
-
;:E":
UJ-
~ ~ "'< ~Z
16,8
o 12:12
8~
-
t 3 5 8 1113 15
5
/ " 5 10 15 20 (hours)
..
8:16
o 3,21
10
Night len gth
0 2 -1 6 8 1012 14 1618
bythe CREM gene was present.(( )The peak production of this mRNA occurred from 3 to 12 hours after lightsout, depending on the photoperiod that the animalshad recently experienced. After Foulkes et al. [398J.
15
", '"
012 46810
10 Gene activity varies with photoperiod . The numberof hours after dark before the (REM gene reaches peak activity depends on the number of hoursof light an animal experienced during the preceding days. (A) White rats were placed under several experimentallig ht:dark (l :D) regimes. Samplesof rats were killed at the times indicated by the arrows. (8) The rats' pineal glands were analyzed to determine how much of the messenger RNA coded for
7" i1
01.53 4.567.5
2],3
(e)
2 4 6 8 1012 14 161820
:.~. - .
, a3 q.""" ~~~~ .~~~~ : ' , ~ ~~;l~ ,t ~l~~~~'~ ~ [J'i~~~ll ~ ~~~_! LI~ 71!~ "I:','i!~1 1'!'~'I"II!I'~lt '~I,r,t';'.i"lll~ e ! 1 :{ s5"r :!iltll!rli -'~Iil 2"1 ;~!lH ~ '.0 0
~ 9- 1>.
t .. ,
~
~'
~
~ II ~ ~ ~ ~
fhl'[
~~.5= ~;- fm sprig h t mnon lijl;h t. ''' r('ri(.;o [3791. Ont h ~ on how >Udt ...yowm IT\ittht work P""P"""'" th.o, tlwdoclr. ........n.ru.m of whi~ nhittilu dail~' ~lic..1 ~ In ........ ti'·it)' to ligI>l. with .. cyc'" thoot is ~ ...-h ""<M'1\ing ..t dawn. During tIw inili.ill13 hnu.. or ... ,ftt>r \he
'0
r.r-ea PW' [378t stimulated teslicular growth by e"po,,;ng c"pti..... bi'th to light duri ng th.. hypotht'Sired phot"",-""ili" c phaS
.
SO
N
D
Month
F
M
White-winged crossbill
• • • ,6 A
M
Food intake and reproductive timing in the white-winged
crossbill. Breeding populations usually occurin areas with relatively high food availability. Nonbreedingpopulations generallyoccur in areas where the birds have low food intake.Note,however, the absence of breeding populations in December and January. After Benkman {89].
170
Ch.pter 6
17 PhotCjHrlod offKu tMIls .IZIY _re MId """il. n!. Ths. In .ddition. some .nimals possess physiolugic.J mech .nisms th.lt ",'rmit th...m to .djust beh.lvior.l1y to ch.lnll'" in tho.'r 01 d.Y" ,"nee the "",Ie la,t cop ol. ted . If som • sexu.lly acti'·'''>tidII
..
~
-
__ _
------I
-....l AItc
m lUll," 1hip signals. Shoold "",-t.. t...n.lr 0"f\Cunb:!" an adull !l'rrilt"';al m. 1,·I.....1 tla~ hma le anole', estrogen-produI "'It'ogen on femalel\'Sp<msiv,''''''''' to male courtship di.plays.
, Do.'ul.olioCrI">ei, rNd i".... to S a means ,>I «1ffintunicalion betw""" an animal's eXh!ma1 ""Vironmenl and its v.rious int""",1nrgans of "'Production. Acrording 10 !his theory, ",rtain hormones providlicit copulations. pnn-idt'd Ih.t h.. h.. bt-,-n ,'xp'-.l to I"ng photo?,ri.." h [Sin]. Mo"",. t't".•on,e p''Pul.tions of whil,-,"""rowned sparrows rac.., mot\' than otl€ brood f"'r bt>' "",I" whil """""ti.l for m.k "'"ual beh.tvior in this Sp""Ies. r.;or is tt", whilo .. ,,"og
c.,o.oIltot _ _ __ in ....e "" ... r.. - _ ..... ocnncUing._· _tw ",t)do. tor>e_ _ der brood of
.>t+oprinll' The. p....tictio" 100 has """';vro OOITW supf""11(54). h'm in"f'«;'" in which t? Ilec• ..".. Ie5to6l....... ' - I multiplicity 01 e/kct!; (Fit;U... 23). dw .........,.,.. may carty I pri II certain timoBor ",anam Nnwti291, Hip, ".,.10"1"",,,,, mfIn'"lr.,tions In.'y "I", contributt- tt, hip, ""m",,,tt-,o..., """",,,,IT.tit,,,,. whi,h m..y ",mtri!>uh- I" 0,. be refl""tiw of great'" physiologic.l 11257)...nd thlL' g""l'" vuh'lt'r.bi!ily 10dl"'.'".,.....lISing OI):.misms. In .>dd'iion. the dircd b"h.wio••,l dte"t, ,>lI,,,,t~ I,'ro"'-' can be rostly. M ..I", "nd," th" infl",-n",- of t,,>I,,,t"nm,,, ior ,'x"mpl,,, "itt-n ho.'1 they b ,"'q"i", herd. 0/ k'1llal,,,,, Ih"y b."ome ,"" d i'IT",tt-d th.>t th.-y oftt,n ....;.:I,'Ct to W"om Il><m....I '>. which tht-y """" to do in ",d~r to """",,~ d''''gen',,-~ tich fru m their bodi IRI7]. MO"-"(I\'er, in 5O(;"lIy monog..mo", bird' wh05d in m.my modifications of horm'm.>1 mt'Ch.1ni"m. of bclla" i" ,. If illU 25). fn the song spa.row. for ' '''am pl'', m.I,,,, ddmd I,'mto,i,,,, lon ~ aft", the b,..,...jing "'.,,'" i, m't'< and gonadal "" hr.,"""..", haw ' ...... nti.. lly di"'pp"ar. IA) T...t"'t~ " ..Iod ""'Ie> _1 ""~ bg, bY! in othoef bird, lbon"", lWQ ponelsL""'1ft ore 1... ,1100.1 .ll l~.m.,n 'hrt ha"" lin'" Of "0 c'«ul,'ing le.'o~, Att./ WlrogIifld f>l " .[1255].
""""",,," 'l"rfOW
m
J'u ~ .. ~
whi1!"r demonstralion lholl h"nnonal 'y'K>tnS of ""hav;"" « Kltm l ..... not the ...me for .."cry ve,tro,alred und""W"und hibern.Kulum, which may hnu... lhuSilnd, ,>f """ k"" . On warm days in u...la", spring.. the snak... begin
,,"
'"
,, "'"'
so
,
,
,' ro
~
s
l"
!
I,
W
,•
Control
'"
FAD~""rog.n
26 Eotr<Jgen _
territ".gl
t>e.."I,.
Mal
••
tt,.., _ .
,,,", >till pos""sed !hei, Ie>t... Aft... C'ew> [2621.
anL~ms wtderlyin!\ n1"ooucti"e betta,i", in lite ted-,id.,.j gMlter sna ke, a, il d.... in so IThlny other ",·rtebrales. E,'iden.,e on lhis poinl comes f",m experim•."ls on "dull m,ll" ""'M-s th.lt hav" N..." castrated, Wilho ut their tcsk'S, these indi,jdu.,I, ",lnn"l pmdu;, a"othe.. ~..,mpl" of t.....nJl~ th.lt tho.'rl" i, no one hOrrrK>n.11 mecha"i,m tha I "'lI"",te. lhe ...·xual bo:ha vim of all an imal" or ~"en all vertebrak'S, in exaet prio";· ti... for their d ifu.",nt behi",i",al oph,,,,., On" such pro "i ma'" oystem includes beh.vioral ",mmand <enters 111.1 mutually inhibil 011 not try I" do ""-eral lhln;:s ,imolt';"""",ly.
""'1""""",
2. 1\, lhe •.",'i"mmml chan;:,,,,, the nato'" of tlte inhibitory ",la1loo,hips b.'ho\"t't'1l 11urs '" 31>5 ddy'. G",adidn and circannual d,x:1<s ha\'e tTlyin>nm""t-ind'-'P"ndent components, bOllltey ach w""ld """". fo,."".mplt" wl\ m.,"" w ill ejao>J. t" ... hen g,wn """,... tt, """,.. live f""",".,.I",.. ; lanJard period nt timt', One hn'oth....b fur thi. "ari,al~", ;" th.t mal< "," dri,w "",",,",1 ... ith cirrulating ron,:""ll'ati""", Whal p"-"\"w p"-,'n,,, d.... on .n t"J't'I'imrnl ...ilh m il' ..TUb jor.odull!l ~,~ in Ji7"YJI'S '" lo'hidl II.....-~... adult t~ ...do.'",.ond adult ""nbn·.·d"'l!: hrIpn'o ~ IIw t>r-dlnji; in "'*""ll Ihpring(""" p. 4.36), o..-.-dop a holnnun.lI h~ (b.>sed on !"UW" .-t'"l': c11hi:o m.pwrl for IIw I ..... ~ B ... 1k'.",1Iw worid ... .oduhiIogiaI doc~ '" ..... lOJrt. but mi«:ht tIW; cb;~ t>rt ,u IIIurN out. """",,';01 of tho'tor.... 01 a - ' moIh doroo Ioi tho ~ ",",-laJllf~..... 1DaduIthc-out
'9 . ._
.. . -
186
Ch.ptef 7
TABLE 1 Three _ SOnS wfl y rlOt . Il current traits are adaptation, MOf O
I. The If",' ~,'01,.,.j und",. rendi'ion> 'M' no k",~ ",;"' , bu t perot'" inout/icien' 'ime 0< the absence o! 'ppropri_ .k' mu'.tIOi,
exom ple .
An'IK ground "l",rrcl' Ii",. wl'>.n· d" "''', bu' WNm II'>... ... " pe rim.... ' .Il}' "'P"'"->J to ""'''' 'Ik»i ,>I ''''' • '.lIn. resrbc bdgs, whKf> .......-ntolo jellyfi>h fhcKontly tu trigj;OT' fet'd ing "'"P''''''. In thr 1"'-". ""', ""'I"""'" wOllId t..ve!«l to 'hoe od.p"'" ingelK dtobris [6721,
II we are to apply the ""'I-henefil approa.:h to m<Jbbing by gull~, w,· mu.-t figure lit how tit d~i"C"ahng div,,-bombt.,.. O"t·rh"ad. Although the pt'l'dalor di'lractinn hYP'>!fit,,;is mak", """''''. we must 1n;",ardling for gull
"''''I>
Adapla tion a nd
A nlip,~daIO' B~havior
181
3 1)00.< mobbing Pl'OteUnlin;; tho.· num"", "f ,utviving of/'prio;; produced by individ ua l, in theit !if... Ii"",,", Krouk loo ked in>te.ld at th¢,ts ,lftffi ha,'''to ""'tit>fo, ,10 indicato, ot currel..tductive ' U':'''-"'S in the la,t a""lysis is m...surt"d by tilt> number "I nfkpring (or ~omelim a!\" 01 reproduction produced by an ind ;"iduol ,,,,~,. ils Iilt>lime, and that corrdal.'S nl Ihis mea,un' will b.:acruralt' 10 "arying degree;,
The Comparative Method forTesting Adaptationist Hypotheses EJ<J"'r1mlu h,m " I ~n int~ ,,'S lin g trait by looking al anilTldls O\ht,r titan tho·spt'rit-havior, which is why thry are all placed within thJ m,my I(er>es , This anc",lra l ba ltery uf g"fl{'S gra dually chang,>J-a new all"ie ""n', a ."'w ,' llele there-in c'atiou, gull JX'pu lalion •. The chang'''' cam" about Ih,..,ug h Ch"Orts), and thn>u, ""Iu'al ",'!e.:tico, which ""ltod upl'" !h'ting
bffi",.....
4
Gull phylog...,y .n"two sl7]. The common.....-" ~ 1 and gun. .>cnIJ"ft'd ....... Ior'qt ago, "'Ith the ....... 11 tlwt the ~~ the , ., K""'P" h.>\~ "'·01'·..... ""'f'Ir.!IO'Iy lor.............,. lact ~.,.J b,' the pL.ocnno.",. 01 ,,,,..110..-5 in , dltl~....,1 l.mi!>- "I birds (tilt' Hirundid...,~, H" ....,....... &'''1'11.· tllt'i, ","'oIuti<JnI'Y and lI'-"",",ir dilt...............,. fmm gulls. both I>.om and Nuk ,,,,.Ik,,,,,,, I'o.""'\~
;0'""
h~~
c\,,,,,,,,
gull, ... 11< it tu t""a. ing Ihso. oquirTeh hI"e "'OO'N!iUbow1tial bOoctoemic.al ~ I the ''4!I1lJIn'' the r.... tl*m plol;ifit ratt\nnl tho.- 5p? It I", .......... ",loni~1 ~ in which ",,1Obb,n~ und.ont bl«kdoIwd .. ~ lonn in lht pn10d from.about 18.'010 ]'Rl1'&51 J ~ 10). Mo;t ~ ~T.-d.... ~ hot,·........ rd thr .Wnd.lrd .. ~pt.n.""" thr uul'LlJ ~ (If .... nl(wlic form (and dw sptti;ol ......... ~lird w,th it; mutant rolor pal\lt'm). ThO' idH waIIlhal industr'ial soot Nod da~ Ihr rolor 01 "'""" '"""
I".
Inlnks in urban nWite 1" ,"'11 In I t - pw.ee.. to ~"tlrOlJS b;rds, ... hidlalt' !he .. ·hi'" fo, m ,onJ tl......try ........" ...-d!he ,r;t -ti
moIh__ ",nned fO lfft 'runk> Of limb pnl _,. ~, likl'ly '0 he found .nd ,emowd by binJ"""",.11. ........n>c Iorrm dl,· by bi,d< ~. ott..... "' ~M"" Id.... ened) wood~ whit.. typic. lloI'm.",u'· vlwd" bl'll~ In non~Iu1"" wood'. Aflo< Iiowk'tt .nd M'iM'.IS5l].
n,
w""
e""",""
Typic, 1
lyr ic• 1
.,nd
-
• -...
...: ,
-
• I
•
...... . '" ,
-
12 (ryp'ic colo" lion .nd body 0.1· ......' ion. ~ _lOtlo thai whi,h~,'~r IOTm w", m"....",-m,piw"u, 10 hum.n, w", I~ken by bird, m""h more ~ukkly lhan the other f,,,.m. 11"". p.le. individual, we,"" at sf""Clalrisk of attack when the")· p""chN {Ill d,lrk b,...,kllnltmds, It is tru~ that in no",,... tht, m"ths m~y not oil.'n p"n;h on tn", tTUnb ond in_IWId may It'nd to ... k1,,,,,' the i<mtt and !>t, E. S, M"jcorus lllU.· moth Sy lr~i",-d the bl"" jaY" I" ""I"Kld 1Sp'>ci~lIy Jikly t(} ow.look tho.' moth when it w~s ori,.,-,t.> tht'm....lw" subss "I"il>l""t 211 """ aw"v "n .,'~r.)!;~ [S12). If f.k",,,, .•1"" find dirty purmi·
"""iru.l
14 Conoin .,;ldition. MI~ tm...- , hit u~ 01• p
• C"".fu,,,", criminate .mong them, rom C.m k.med tha t ••olitary g.zdle will smnetime> stol when. cr.e,.'1.h appn....","" an ob>t>rvahon that helps elirnin.lte tilt in order 10 . ttract disl.nt gueUO'S to join t....m. But il thZd a 1o'W " xampl,,, of traits th,lt inc,.,.a"" tho.- prot>al>ility lhat a predator will either o"erlonk a prey or ch,)O;;me is ,;gila~~lying ak,rt so as to dk,,,, action promptly. ",'en thnu);h it apf' l>ird, [95-tJ. The awra);e I\'"ction lime 0' thte solo l>ird was abou t a 'n
'"
.I
"
l
._-
L •
j
25 SociaoIcom _ ......... _ _ fits. ........ IPOfTOW' _ ..", loWly to
25 _ 2 ..........
-
l~ _
Ad,"",,"'
1''''''''' '
.... fo< c~It>...... ........ .c I food """". ............. ......e of li"in!,> in ~ f!;'oup rom... from owrwl\lming tl\ killing c~paci!y of the 1rr\t' maytlit'>; synchronize their transition to adulthood [l1lS]! Mayflies.ore appan>tltly tasty m-ts, much '""~')'t"d l>y ,,"rious pnodators at all '~lg... 01 life, but "'p"'iaUy when they cltdn"" In"" aqualic nymphs in tn wingt"d aim".".. adults. This m.1amo'l'h'lSi. is one tltdt ""ti.... populations may undertak.. over a Iht tilt' OOdi... of f,'m,ll,,, that h.ld laid their eggs and then died a natural dealh; a lemal,,'s IiIcialil)' und,',);", W. D, H.lmilton's characterizalion of some g"'ups of animals a, ...lli sh h~.-d. [-JH-S). lmagi"" a population ,>I antd"P" grazing on
n....
• Juno 9
.."" 26
Th~
dilution effKl in
","yfI ~.,
The mo.... ~~mayIH ... ln.1
~ IOgflhe' "" & Ju.... ~ Ing, .he 1M. Ii..,!)' &"y Individu&l w;n '" ~ ~".. n by . pr~""" All", Sw
a ~d A ~,;p' ~ d a t o , B ~ h a " i or
~
x roonl"",,,,
al", ,""'although mol,(' ing of. pn:Jator is more likl~' III 'lCUll in tho> .....,"·r of the colony, peripheral m.l", also som others? Pres"ntably tho>re 0'" erI"in 1r• .1....... ffs th.,t c"n lThlM it ad\'.ntal"'OllS for some in bl"" k widow .p;d.... tha t live in my h>C>! ,h.-.:l, l. hk" m",t Arizon.ns. t",.t thN srinne"'15 or 5Om... 'riders. Who..'f\ attach,, tho."., individuals rould nol defend If",msd,",,,, with ;>;. Ahhuugh Ihe ,pid.".'. glue L, notto~ic (coru.umplkm or the viscous substance did not aUro the mice), it is stirky, foreinl': the mou,"" to remov... it at or>ce or suff..., d"mag... to its fu,.
A Tactic ofL ast Resort? ar.c.:, a black wid"w MS Nt.'t\ bitt...n by" d,,," mou,"", it's "II owr lor the spide,. Bul somc'tim,,, P"'Y con surviv.. fo, a hnt, lur e",mpl", "'spond 10 bein" c"rluA'd in Ihis lashk"" d,'Spitco the racl IMt Ihey.'" no,mally the <jui...t,,,,t of "nim"ls, Surdy th,' >ca'am is simrly" non"d"pliw "",>eh'm to ,hmulali,m "r thc pa')"s ""in "'Ct'ptms m i, it' In a ""PC" "ntitlt'd • Adaplalion unto o.,ath,· GOta" Hi>gstt'dl t""ted mulhrl" hypothc'S
many .p«:..... ju • .".,ile> a", 1\0 more lik.-y '0 9;.... !ea, ""earm whoen handled Il)' a human man are iSdull>, Thi. OO"""a'"", "'99"'" that thoe lunct"'" of thoe ,anno! be to enlist parental..... ,lOnce. Aft... flOg,""'t {SlIJJ,
to"
210
Chapl", 7 Th~ ~\'iel"",,~ ruin!>. 10 "fourth hypotho.-.,;is: namdy, ,h,,! tho.' caplured ani· m,,!'s se"",m. aU'a; h' tho.· "-":orekT. (On \ht, other hanel, in "nothe, study, when royot'" aUractlxl to sta r~ng d i'ln'S> ulls came Inward a feUow coyot,- with captured slarlin"" It"" allac ke, in l' '''s ifi' xl its d fort to dispatch Ih,' bird. whi,'h ",as not g,~xt ""'' '', for the starling [12-'r! I_) Fi""lIy, Ihto dltraet--cnmpt.>ling-pn>ctator; hyf"C'll"o of many fish. t"throd minnows ltwt h",'" bo.~'f1 olt¥kecI n·le""., che. p'ko. ""I~
T..." p iko. 1""""'"
"da pUlion . nd "nl ip,edllo, Beh..io, in 5 ..1 13 lnal_. ~ 1TlJJ1I'IUW """af""l. at \e«.t It"mp""anly. """'I oId.rUh.-_ d'~lgnctl to
ml~' Ih,,; 1I k,·ly'. ['hWArllnK tlt"''CIin ofl.'n in""h',,,, cry r lk he·ha,'i",. in w hit:h .... oni·
m.,l ...,h,,,,,..,,, lhe' dfi.m m imic>, P"", may rn'\'.... 1lhe'i, ca plu", th""'Kh "ilo\ll."'.... lhpl.'"
Disc:union Oue-stions 1. , '-'" f'">pW lhinIc tNt ... ~Iion 0.1 traot Ihal "."........... ttr
.. c:hIrouw be • k,kd ~ '
2. Fer ........ e\-.-.IutilkM''''lI: ....... lion (..'im than", 1o.."", Rul " mul.>n! ~'pt'S M:i~ IN t arch oul 011>0.·.....-.:1 ..... tho:m • • h inlI ""....k!, ,#,,,.1 r ""'a""". The m uldn" l. ke fin- tn"" tht wtl"ld -he
2 11
212
Chople,7
...,lild')' types by making them mo ... """'f'iruou, ~, t""" I""'i,'\t.'d 0/ t",,, indi,'id"al, r.ther th.m one. Wh.", Iwo ."c;.,llyl"'S in· !Tact, we ",;11 "'y Ih,., IhCb A I:d"'" Iheor" d;.,gram ("" h'low) 5-Umm.ui.les I"""" int",-dC!iun>. 1/ B c, g.... I",. lh.Jn C. wh.Il heM\'i''''aJ type will ('tlfll(' to p,,>domi,.'te in the popul..tion owr tim,,? N"w c"mtI", '\,"'-.f," pay" ff fe.rindh·;.dUoll, in p"l'ulall""" romf""'"-'ther lI\t"\t' ca""" In"" h'e cr>rl' "'1','f1I....·olution, d i,·"""..,.,t ....,olution. or "'-"the r. a Almo,! all o l""r ,pt'Cks of IIOCtu id mOlhs also hil,'~ "drs tMI ""p'",d 10 ultr.",uod, b. !'1lmflSt all t"" 'pccie> in ....... " .."Juti"""I"\' lin.' a!;" lhal "'clud"" the "'-",luid m"th. and m an. ' ,>ther moth; belonging 10 ..... ~r.. 1 sUf"'rlami lit'Salso ILl"" '' the dusb.'r and kill, ..""" bt~" .., tho" .n' "''Illing d"wn for lh.,' niJ-;ht. o.'Vise al 1;....'1 Ih"'" al"''''''I,"o h,.puth.ost.'s on lhe I"",-'iblt' ..nli.-in bUI; "aluo "j the\.. pt'rl"" tcoJ ad.l pli'·o pn>dUt1 of ""lural ...htt"n IU'I). who.", In ",'.lity "",ny atlrirouto" ,>( Ii'--ing thing; aO' not ad.pwtioru. b ...• TdhJe I). ~to""""" r, in thoir oago"""" t" ''''I'ld lfl ....."')'.Ihing ... an adarbti"", ..bptati""i,ts haw, ....-ron.linll 10Gouki ..lid I..""mtin. im'""ted fabk.. ,>; .!>surd as the fictional "ju,t..,," , t"Ti,,, ,>I Rudy.,n;!
Ad.ptalion .nd Antip,ed.lo,
K' r i,nfl, whu ma.Jt, up .... ~ v.pLanobpl.ltionisls dl'lfl:~aII..-..I~
.-.d tooI\a>_,o/ dd
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L.-r'.... ..
.1._,,,
tn.. .......
2 17
2 h imoll'" "'"-"ion il> I'" .I......d . kunll. .....1wnId 911'''' e_~ r " 1"91' _
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4
A c1adogram of lizard prey detection mechanisms.
Orange branches indicate t hat t he members of t his lizard fami ly are olfactory foragers, which flick their tong ues to de tect prey odors. Blue branches represent ambush predators, w hic h employ vision rather t han chemoreception to find t heir mea ls. After Cooper [243J.
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The Evolution of Feeding Behavior
2 19
occurm:l as spt'Cies C .nd O....ch gave rise to !woor obrlfonled witn ""'l>"rt I" g ravity SO mat I!>t>d 90" 10 the righl pf ~ Ii"" bo.""",'.,n II>on to' food source they h• ..., f""nd All'" tr.in log ~ 10 oom< '0 • fet,di"9 " .. ion at F, von frisch ' trained 10 two feed...... th,'1 wo"" giv"" the ""me """"'I bu t w...... IOCin'ur nf the pnlposition that WorM'J'S I;ain u..,lul information from the mowrtleeo poeriofm a ""oggle cIon bCod saurct',' worker simply orients Iwr w.ggle run directly.t it. EIcc.u"" this is. Icss sorni,ticatcd rna""u"er than tild 10"""" not belonging 10 u.... !\"I'us AJ'I" 10. rd sul,r !,>I,nd,. As the bee ... turns to!h\II' ~ed
.,ero"
......, """h "" 'M _ta'ion !'longing
from 1M ~ and q~jdly ~ " ' - , to l!>ejr fond. Photog,""" by M.n in lind."",.
Ch~pur8
224
5;"", Und~u....·s pione; ,hat haw aness to alllhn.-e sourc", of information abou' the I"calion of a fI"w,r patch will be abl,' Ie> narrow their ",'arch still furtl>cr wh.>n within 10 lIl a signal (the w"ggle run) on..ntro ...,tali".. Ie> gra.'ily.
""".",iCl/.
Ii"",
11
Acoustic.1 communic.lion of the of . food "",ree to)' 1M tift
h ~ i !lh'
~ipotlQpanamiaJ. When.
",out tho' ho'
t>ren "aino.th the bees). Afm IIr ,raining fftde< tlwn • to",,," ~ ~od ., tI>r 1>0... of the II.... Aftor ,,~ [8-111.
The Evolut ion of feeding Behavio'
22 5
The Adopti ve Value of Honey Bee Dances Ilaving ,"'Ilined • f""'SSit>1e rustonc.-.J '.' lU ad ,'ph\'e \". Jue ,,'Ihis boo>havio" Tom s....,j"" ond KiT!.. Vi,,,her prop" ,."j Ihre.. hYF"lh,,,,,s on how Ih.. tim,- an cl e""-'!)\V ",,,,I, 01 dancing millht boo> "WI"ly thei,- mulher (".•, p, ....I.'i). m,,,,1 possit>ilily is Ih.,1 0 d,'oong ","ul ht'll" I"" "",trn"tt-. find ,o"d ,uj>plit'" m"", qui,kly than Ilwy wuul d "Ihe,wi"", reducing the costs ",Iood loca· Ii"n I", w",kef' and !hIL' inc","," lg the ,aJ,,", ,ost---bt"",Htralio fo' Ihe ",lOllY. Th is hy polhesis predicts Ih.,t OIl a,wage, a """ut be..., whe.' hunl, '''' IWw f,x>d ""un'",; without Inlormalio" fn'm uti....., be........ will ",..>d mo'" hme I" find filOd tha n willa n'c.tiQg the waqgle-run compo""nt of "'" d.nce, Afte' Weidenmull", .nd Seeley
t""
(201).
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Th~
Evolution 01 Feed ing
Ileh~viof
227
II tl>". It, get a good mmL An ob>t'r'l'~nl nwm bo.', of" colony ,>I ""'ting birds. for e.."mp"". millht monitor tl\t, forag· ing 'lK'C5/; of retuminll ""i!lhbo.,rs ~Ild simply lollnw the sucrI dt'f"'rtu"" d(\{'§ not ocror, or if the binh head out in all din' folk"" [,';(l~l. Mon,o"e', the dr'partinf: ""',11k"", t.'Ild to ~,l"rt simit~r b.·aring:>,,uAA'-"ling th.11 some individu., I, ~n: followinf: otl\{'r>;. If til(' inf,mnali"n "'~'It'r hypothsis i" roIT; "h<mld b.. bird, thai ha"e do"e ",ell Jl'fi'llUy, This p""Jicli,'" failt'd lt!;t,'St for ""'. I"'pulah,m of bam "",.110",",[503]. Bird, thai call1t.> b,>fk "mptvb.'ake.! from a fo,aging trip ,,,,,O'no m(lr!her f"'''ginl': lrip. "''' d id lhey tt.>nd tl, fly in the din.'me ,,,,,.. t.. 1a"",..-do w.tch the-i, ""lonym..tc'S to INm wh~", 10 hnd c~rt.in kinds of fi,;h; nam"ly, Iho".· IMI . W.r here and lho:re in 1.'"1': in gm".... "f trt"''''' '0 d~p.ortu'.) I. k. much longe' to find _ "" ",I>0oI. ,h,>n inIom>ed ('hose Ih.1 h""" ju.1 0-1>...._ • rNurnir>g neothrr...ft> ,,-t. den>rl''''''.III~[ SO why add !he ,pecidJ ,ilk to. wt"b. if pn:y.'" ltoso lik.,ly I<J ny into w.-bs with d.·..."rdt"ms' One rn bird, "'-~, tilt' bri;:hl d''C'lfd h'',,-,, tlln1 mat hiKhly ·1'«:1;'· .. dboUI ..'hal It... y ....IUdlly ...onsume, fur ",ample, in h .. ~ Iudy of howl,-, monkep in C."u RK., Ken Glande,
~oI~~#o1t.,.
232
Cha pte r 8 discovered the follow ing ru les for leaf choices made by these leaf-eating primates (Figure 21) (437): 1. The more common a tree species, the less likely the monkeys were to feed on its leaves . Instead, they spent consi derable time searching out the scarcer species . 2. Even among the less common tree species, the howlers refused to eat leaves from most individuals available to them. For example, the monkeys took plant material from only 12 of 149 specimens of one acceptable tree species growing in the forest. 3. The monkeys preferred the scarcer, smaller new leaves to the more abundant, larger mature leaves. 4. The monkeys often ate only the petiole and dropped the larger leaf blade. All four of these choices elevate the time and energy costs of foraging for how lers. Glander found, however, that there was a reason for each of them: 1. The mos t com mon tree species had leaves loaded wi th alkaloid poisons or indi gestible tann ins. 2. Among the scarcer, preferred tree species, how lers sought uut just those individ ua ls w ith especially low levels of alkaloids and tannins.
21
Food selection by howler monkeys. Although surrounded
by leaves, these monk eys forage very carefully,avoiding toxic leaves
and leaves low in nutritional value. Photograph by Ke n Glander.
3. N,'w young IN"~s wnl.lin mo", waler and Ie.. nonnolriHve fiber Ihan malun.le...""s do, When lhe monk,'ys d id eal motu", 1,'o....s, they ",I,xtoo spedm,,,,, wlK'6l' lea"",>had a higl",r (12.-l """"",II pmtl'in Cl"'tl'nl than the malu,"" 1"0"'.'" "f Ih,' 1Tl'k Wl're abll' to ron-s!nJc1 a m"themalieal m,>del-a hYJXlthesis-------b.'l5ol'd. on the a..umplion that It-., crows would ...1",,1 a dil't lhilt ma~imi7''elecli" n in . elat;"" to prey . iu. The 'M "'I""_t. the PfE'CI;ctM po«ent........ of .",,11 10 I"ge Ina! ce tM'd' onompl '0 maxim i'e 'he'r ra'" of _'gy gain ~ unit oItime ., directly. !""read , they rnt'",unod lhe ""I """rgy galno>d while crows were for.ging for dam., on the assumption that by maximizing it. ,ate 01 caloric int.ke" crow would g.in more ........rgy for lhe production of "fr'pring "r mon.' time to ,po.'fld on other filn''''-promoting activities. lltis ."umptiOll h.l.. been !Sled "xf"'rim..ntally with captive zebra finches , which we", all given the same food., but und..r diff..rent eX f"' , iment. l ld [407L and wdl·fed orb-w~"'in","rid,.". produce more 'WI ...... th.m poorly fed individuah. [10431.
How to Choos e an Optimal Mussel The "y'!se p.... y. In thei , init~11 caleu/alion. 0/ prey prolltabilily, the ......an:ht·fS!lad roru.id· enod only tho"" pn'y Ih.t Ih., oyslt·rcatc!lt·". actu.llly openoo<e mu,,." to .tt.ck !Nt ore lo,ger lit... lhe .verage .. oIloble m~,"', bulltle)- do not COf\centr.l. on lhe very lo'goKl m~.""" After Me«:l >Ole/)' "" , .... ond. to ugh eo.>t of b.>m..d .... which ""' k.... tho- mussd .., im pt>.wlrabl.. thallhny calories in the rrade-ff hetl.'""" k....1finding and rmd steahfll\, As tht.'Y I'\'UW older, theycan open m ..... sels on their OWn more dfick"'lly. reducing lhe ",lali"e payoff for thie""ry, As Ont· would predict. older o~'Slt'rCatdwr:sspend 1fhapt'ric gains for Iong-lt'rrn "",;\all"-' L \l!l4]), COIlside, the followmg ra..-, leaf-nJlter a"ls rollt'Cl plaJll malerial thai they ,,'" 10 mak,- fu"!!us I\d for tl"" a",umption that the ""'" are worlt· ml\ I" ma ximi,,,, tt"'ir lood intake. How""e', . ltrn'uKh th" anls could also incre".... the feoJ Imml
(I". \/3). A .omewl\dl similar ca"" involv.'S Ihe r-:cw I>-kxico spa ddool to.>ct ",hc_ ladpo!.'s abo Co,"" in two form" a .aridly d.-vdoring type lhal.pe,iali,.'S in e,lhng "maU inv c.,-nobTal,,,, c.lled f.iry .hrimp, and ••Iowly d ,,·e!· 'lJ'i ng lyJ't' thai f...-d. 0" odd. and end., bul esJ-""-'cially on bits of d".d algae and l>Jht,r d."!.i'", on tild wpply and adju,1 their feeding beM"io. aaurdin,;ly, If th~.hyptllhesi.s i. co rrect, then an "'J't'rimental sltift in lhe ratil, of carni..o", It. omnivo'" tadroles in a pond should ca'L'" so",", 04 lhe now u"nalu.ally common form 10 ,witch 1o lhe otllcr lora!':ing mOOc, brin!;in,; the ratio 01Ill h"'"
Consuming What You Select to Eat It i, one tlung to se dalo, tht-y cak1Jlalt"d two d i!'ft'n'Tll m,'asu,",-," of for· aging Su,'"....., (1) lilt' 1J10li:rams 01 meat ga ined p." wild dog t'dI\S as w.. lI,
How to Open a Whelk One.- p"'y h.lw Pl't"tl d.·teelt'd, attodu-d , and captured. lhe job of a forag,'r i. not
necessarily OWl'. Even alt.-r lions bring down a wi ld ..b.-esl or Zt'hra_ tftt>se
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Group 'W! an d let!ding .ucc~.. in African wHd d og. , WI>en """ coo"",," Il>< ""''' a> """I ., ,l>< ~r>eti" of ""aging in 9' '''' 1'' of dl!fe<en' .. ""~ ttld. '0 bo(, 9,"a'... 1or individual, thot hun . in 10'9'" p.d... .Tl'I> ci".... aro "",an ••1....., w i,h , l>< .roa of ,l>< ci'C", proportionallo ,l>< numb.-< of """'IVation, lor pac ~, oIa 9;""" .ire. After C ,~ 30
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pl't'dak,rs often h.>\' a dam. ""ail. or whelk. il oftn picks it up, Ai",; into th air, and then dn:>p> its ,-iclim. If th.. mollusk', shdl ,h"Hers on thl' rocks. thl' bird plucks out and cats till' l'xpllSs rn.my cho',..","" to make: which whl'lk to ,,"''''ct how hi",h to fly bdon' droppinll thJium. and l"rg,' whd ,,-, ~nd d'opf!'-"d th~m irom diff.,""'t heights (Figu'" 3]). H., found, first, thallarg., wm,lk. ""luin>d ,ignific.ntly fewer 5-meler drops befo.... lhey broke Ih.m ,' ith culinary trad itif>n' vary so I';"'atly from rulll,,,,lo culll'"" Billinll and Sht'rm,l'" I>
3~ Th~ .nli·microbi.1 propem-.1 b)' tho: p.onolS linl' tho: ~trd.· d~tiw lJ~ ,.,. 11000...., and bind with .t ~ .,..., pl.>nl .Iuloid. ~ protecting tho: MI3 "f tho: g.o.m>in1!.'stin.tJ lining fn.... tho: I,,~i< off_ of thi~ d>o>mi 10 u....J e~"-"";,,ely In the .tuJy of h....linK behavior, Aithoulll> """'" f",.ging .ni.... l. d" behaw in w'y" lh.ll ""'tmi"" ......rgy m.. i""~.,I",,, '" rtdua' lhe ri.k of prtd. tory .ualisl'i. (l\:le: Individual. 0/ all sliclJ...back "f";'cies ,-ary I" ."m~ ~d""'l in their dit.-bry speciahl.bol'l,) Check your predictions .gain" the .I"", in [1022, I023J.
4. In ."m~ pl..>ce., A"""",..., m>W. ''f'"'' walnuls by dropping tIwrn on h.lrd surr"""" Un1ik~ nonhw,,,,Mn crows ""","kin g ....,th whel", Amt.-ric.an emw. Jp. .I"", tilrg, 1"-'llflSyk.ni.>, fly allihe wa~' to Hondu,.s, only 10 tum arOlmd in a few months and fly .l1lhe way back ag.in' Thi, chapl~' will ,huw hnw tt...".. pUz.; invt'Sligaho'd.
Habitat Selection The rul,' thai "",lain 'p, h"lpiIlf; Ioc.l populations rebound, This eXpio4ogi".
to >dy Isla"';, bui~ with d,«Iqed "",,,,rlal~ ha' att,actod many pa ir< of .-.ethO.T """,,",',tiP1 ' I ~ on tt... p......i5~ low OUIIl26.~1- An~' ~ l .rn.m.- dr>i. '" iny popul.llioo. will ~.....w ",,,,,,pk,,' fin, "".. Io .... p'" II.... ....bit.o" ........ trll tt... pd not rvOor;';' t with the ronch .....med by Sfto,'e f _ l I """ Ius roIlIIo«>qr""" tJy l(Irt< VIHctooJit.1ti.... w.y 10 tlw h.lb'J.lt dIoit..... ....,.j., by hpMting .w.nn..-tln _pora"ly in. "",", w"-' the ~ h.ong hnm • limb in. mM&.ruund thrir q.-n ( F>gUJll' 2 )_ 0...... the ......l ...... dlys, ocout workrs .....rdl /or dwnbon In the ground, in dilk. or in hoi..,...· _ Of the y....:h siln within rolRfl'" of IIw ",.. tong ~w..... ~· '"""" " 'ilh a cl ~ ~60 Ii..... c.....l'O'tun'lir'ltl ~ f'""'" iorm.dannobodatth.. _ _ [I033L ..-hidlromm about thee..- 1Ct'. and quatity clllw f""rntMl tlornP( p. 22IJl. 0tIwr .............. around • ~ """'" ma~' br 'p"t, ';;nc\"oowtinR .'n", • t..'W hu ndn.'tl """"'" c~1ed
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Habitat PreferenuJ in Q Territorial Species Honey bt.. colonies do not .ttt'mpt to defend a ff! . "".-
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age numbo... thaI .re Ior. than the gall at the prj_ \ocati,,,, """r the IwII J""iule. If the ther aphid i., already "nd"""nd calories not only while movin;;. bul even befo... dispersal. when IIwy mu,t invesl in lhe d,'\"dopm~nt of locomol'Y musd,'S, Con,ider. for e'"m· pie, Ihat if.
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AIlOIh...,. spKi'''' in whi,h ""m,' individu.l. di.per<e f.rther than ollK'rs is wound "Iui""l Young m.l.. squir...1s travel dboul}5(l mct"lund squi""ls th.l t R'main n&lJ" tl-...~r birthria..-.. I b".,n st",n fi);htin); wilh old". ""'-" amund lhe hm~ 01 di,per",I, tho> i.1", d,,,,,,,,"'" 10 be ,.".,led in olher Cd..... lillllS, for ir .... tin: liv.-.; wI...-.... tht·), w,'n' born (Fillun' 10) 1942]. Tlw sedentary le"",l"" bendill""" !heir la mil;drity w ith g"od hunting gnrunds dnd ",Ie bnwing dens in their n"talli'rritory, amonl-\ othtor
""",. The depdrture 01 "",ny young ma le li",~s ~oindd"" with lho,am"al of nt·w matu", ma lin of Atrlreover, m.1tul{' m.11,,,,, that have d,'imed a pride som,>!im"" disper;e again. ." pallding th~ir range to annex a ""'(lfId prid .. of f"mal,,,,,. althe lime whr"" their r1aughl...... in pride nl1Jllber onoe an' bl'comin", sexually tn.'Iture. PfOX· imale inhibitions against inbn...-din'" appan-ntly exi'l in lions and cauSo.....t~ dlR'l1ly lo ard their ~"'l i;oo a.....-.taint'd by ..t.:llin: brk-mctry of tun..... o"lfilR'd w,th romp.>ct ..di.. tra""min.....; Fi~,",,,,, 12) 1m). Tlwrurtk... tt..,d ry mult'!>....... ,....,j in a oingle sll'p llOO). Onl' of dw __"'" of ho.try is Ih.ol pad.....1""""ullOl\U\' m..ng..." "'" far """'" ~ 1I\arI .... abrupt ;WOp hum 0fW 1r.1l ,.. .anodwr ,"ft). dilfenonl 0fW IJ04I ll\al ntIfV.lUt)· abtllly rouId ....-01-.-1' jU.aduall' ... pia"""",,, gn'm Ih.ot tod.o,., nwrly bird~.~ 6alIv .. dw 1ruptCS. ~t .hort-<J~ tu •• lbot d 1IPmpft". air ~ Thl'.......-.cno ry abililiry c"p.1C'" ily mu,t haw t>t... n adapli.... , .... ,'h the he-nt'lil' "~, the modih,..,J Irai t Oulwd~h",); th .. c,,,t .. ",...>ci"t.'d wilh the new "bi Ilty. Th., pn>bl"m w,th ,hi.
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Migration os 0 Conditionol Toctic Ilr,lh migratury and ",,,,miwal',..,. individuals OC'"\lr in ..""" "P'-"-"itel.. 1110: Eu n >;x',m blackbird is an e.arnpl~, 'i"'.... in pry ..-d awgtft _I'lOl ~ ~ ~ pw. uI the ..111 1Iuman'! otten plo,.. but ,.n- beN,'ion! tr;ait> that dittw ~ itoJi"iduals beca..,..uI th;,;r l'oere
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territoridJ pairs do ~ lhdn l'Irship" tho! qui· etly utilize allOlhr, lI migrant sungbirds, early arri"al' a,.., known 1 mel caTher il1 Ihi, chap"'r, the fCr trr"ilori.1 individuals c"m.. nul a""ad requires a certain amounl 0/ malh... Frank Gilland Larry Wolf show, one Can rompa'" Ittht,.!.~ai"'l the costs of defl'flding a rich patch a,;ai".1 inlTUde,..;. F.ath hour of deIertse /light bums up 2O.\l more calorits than would be spm pt'T day wrnle for-cinj; other .unbird, to ",.-age in with flowers that yielded I m;en,lih;>r 0' nectar per day (net ""Ioric g"in = 2400 2000 = + 400 calori.,,;) . But Ia>ing intruders to protect flow"", producinj; at the ).-micrnlill'T rale when Wld..fendt'd paid"", with flow..... g""""alin,; 2 microliters 0/ """ta, pr production is unifonnly high throuWwut a large a",a, the birds a'" no t to>rri,orial, But if nrri''''i.... altr.gt>ther, Thus, sunbirds have the conditio""l capaOty 10 .wilCh from d..f..nding a ,erri,ory to foragin!,> in aT1 undd,>ndOO homerange whene.....r they can gain mo,,,,aloties by doing",' [4]4].
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Territorial Puzzles The pi,,.! wal'!ail, a Eump"an songbird, ~Iso defends lecdinj; It'rritori", dur· ing the non'>r..,.uing "'a"on 1288[. In sollthern Brit~;n. t.. rritorial wagta il" d..fend toOCI-met,'r .t""tclws 0/ riverb~nk in winter in ord... to han·..,t aquatic in",-",I. wa,h,'mld.y) F"r.~mg """'11-0",,,,) ""lu,,,>d '" ""'" cal"ro.: .....,..j per d.y
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Un a",umption th.lt ind ivi duals de fend f....d ing terrilo,ies in ord,'r 10 monopoliz territorial birds we", "''' CllT1lperu;.>ling by eating larger pn'y, Firsl, w hy ... ",lIiles ? As iltums out, ow.... rs lO),>rate ... tellites on their lerri· tories only on d aY" wl>n food is. abundant . nd , 11"-'"-10",, !he cost of having • Ior.ging saldlil\' p"'8tum to a...as th.l \ yield "'"' pn.'Y than the undct..ndt'd "1lions ,'isitl.'d by Rocking birds. In 01...." word., why b"lher to be k..nto ria l when the hunting is better eLsewhe",! Davies sUID;""IS tha t when snow """"rs lhe "",adows, the ri\'
Why Do Territory Holders Almost Always Win? Mosl stud;". "f territori .li ty ha"" f.:I,futely, (SimiLu al~raic lIliUld 10 thil; hyp!hesi>, any It'rri1,,riaJ species shou ld "'" . s li""ly k, haw '''ir~'..,.j the "in truder win, " rul the "",""dent win," :\'kk [)avies tested "the =ident always wins" hypothNi. in his study of the 'pht on t..... im,,'1 Aonr, w..... "'!hey may ,}('('a,ia ~n!,> in inb."'''', l'SCalab.'s in an in""'" net until a new male had arrived and ..!dime""" up and fl,'w away lFigufl' 25). Davies saw these H~lS only when he maniput,'hvdy ..n'a k"J two "n",id,,,,ts" tfl.,t hdd the ""m{' tr,rn!u)" ha wk " .....ps 1l51. nd !K",~ird, 1...0;.1]. It for ~""m ·
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..(livity agai" "nd "~i,, until fj""Uy onemdll'--- "-'Pla«'"",,,t wa.."f"""'"'1\i""s up .nd ~ i "", ide,,!. In this .... y. JOC' Tobias w.s ..b .., In mdl,h un.".",..y "",l " m ",," ..~ain.~t l'l'Sidrnls Iha t h.,d bt".... ht·ld (aph"" fur It..... d..vs, ..nd Ul'I0.' ~~- lt.'I"ril"ry Im ld~rs ..Iways won despite their prolonl'\t'd (aptivity 111421. In (onl,as!. whe'll e~- .....id,."ls thai had bt~'n c.a"t"d fm ....... days went up againsI ....pl.,"t'TT1mts lha l had bt...... on tho: ,mt""y fo, len d..ys. the oril'>i""l lt'lTito.y ht,ld~n; .lw..Y' los'. ~"" ront....ts bt't...",'1"\ "'PIa,"!.""""" and ..~-""id ""N we", decidt'd by how lotljl; t..... "",1;"''''''''1"\1 hild N"'" on ....rrill'ry, not by Imw long tht' '"'loIl ~ tIwn indi,·idu. . . . . lO «:Up)" piO"" 'td h;obit.>'" """"'d n.no hip pft'diction ItYlMo bftn 1!O'Olt'd w i!h .Hinn.olJ'''' fftUI'" numbrf 01 "f'"'rito-.
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3. M,p_ io . "f'"b b"';1","" il;" suP"'ir k\ . Ilpm.lh, 'p "'•• ,,~ th.11 ha,'• • ppN....J b~' m" W i...n;n tho spt......... liNoiIono . tdotfil hy. F....... _ on.., Iht...-..lubon 0I ••• 't....ili< 1trT*lnIIiIy,
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2. In Arntn of • ,andomll' ,","""eJ .ubo.lmplt.> 0/ ne.lin~ robi"" and lht>n romp.,n>d Ir..i, n'lum ,ai,' In tt.:, .....~t y,'a' wilh that of 0IhN robin' whos< narurally. bul had in.,tulteJ in the pl1.' I" employ the nonl.'rtiI<Jl'ia1 rout "'l'ulady inspd to hiilh I,'wl, of andn'!,,,,,," in uliochtw ical, a"" perhaps !hey apP"'red long ago in a p,,--gllanl spoll,x1 hyena "'h" SUb, nexl g......·raliun 01ropy_ ing.. ag.in with a fuw ."-n",,, thmwn in. Tho,- ,...,t,,1l("(' in this group thatl. mo,;1 ,imila.to "fl1iI~KS.. .i. ",iectl'd 10 bc copied, and '0 On. Wh,'Il U.wkins did thi, with a nurnb, '"und that it look only 40-70 gffit'rati"n' tu """h lht'targ,'t "",tcnce, r>ol milHon..upon million.' upun million, 0' .t!ably ",,'ny othl"rlat,'!"-appearinK mul.1nt ~,......", as well, Together, th t,,,
The Adaptive Value of PostChanges But why would the original mutanl fumal,· hy""" whose doughl"'" had ma5,'ulini7ecl "xtt,'mal l',,,,itaha have h"d m"... dI Ild /mal- "f lhP !\""". St>ver.1 ~1It, "",." id".. on kow f""",I", could bndit from a S""" that "'f"""oI'd lht-ir f"tu""" 10high kt .. limi""I, ""t fitnt.o.s gain, ,lUI' 10 the h.-ighlened aAAn'S,i,·"n"" uf rn.",uliniz",l f"mal ,'S or their nc'Onal,'S, On"" it had (lrigin" t,od .od ,pn·.d. ",'w,',w, th" p....'udop,'1lis may then h.1Vt ben..nls miilht nxeivers gain by p.oying allenti"" I" this inf""",,bon? Spotted hy"",,s he in Ia'l'\ It.'ilmt'~, rightl . On.. "In dt>tnt 1Il.strak> that ,>thet w hL,lling moth>. lit'., and n',}(t lt, tht>se ultra"",ic sIgnal. by playing a taf' vL,ited by ",,:epliv~ fe"",J ..., Bo th male and kmal.> whisll~ moths P"'''-'''' Illchot>s I" the thora~. lhe whi.tIing moth is .. noetuid moth, a Jlletvat.. the ~ Not. the . imilarity belWN'n ,he _ I n the two mot"'- The branch 0( ,he ~ Ia_ fUN1b' ca...... infonnalionabout the pos~i
289
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of m",hanon" v,,';',tion5. thus "'thng!he 'ldl':~ lor the nt'xl ,li~t in\pro""mmllo .pread thnmgh the ,p",'i", via natural "'-']('(tion. H
""a, ..
The History of Imeet Wings
Lt>t u' 31--0,>1 the cond"'ion thai ",,",' .ta!,>" in tilst'fll in lho., imm"lu'" f"nn.~ of SLlffiy w,'r n"w adults as Ih"y floal alltw bnwl cllJ'P"'d Itw ..~ 01 f1ymg Sk......tlr "f'"" p.o. "".'" Ih "l\I'I they did not «.,ft... lho.' ahillly I.. fly 1745, 740\1· ""'" ",,,Iml( win~ Md bt>corne s"'nd~rd 10' ",'Ill w..It So""", m,"",", .t"r...-fl..... d""""""'ate how tJw tr.....,"•., bat!heir wings loath....... ...,t/i(1o>nl lin ... lhdl~· the two hind !two "...... 'n in ronl.>ct with the waM IflK"ft' HI, nu. ru"tiCJn st.>hilu.", tho- ino«t whilo: f'l"'I'UttinK it lo TTlO'''' i'" ..... inK5 "'...... much idt'I" ~'" th.on '" f't-tblr f.., u..-.....-fIit>< that J.lumrrwn about -40 1""""""1:"""""" INn hind.Jrox~. ~ ....... muWlt indt, 01..,...,..u'itl.. --., ~ tIvt 10 o-Itw 1und--ltoK It'dtniqut> might h.1,... ~-..d , ....-.:ti,... 4dv. . . . . ll6t Ifrom hInd-1fK ~ it ... ohort add,tioo.al ""1' 10 fun f1id>!, wttit:h ....-...ld h.1,... "",...-;I'd Itw fi.... trur l\irn. 'W.~· from inw ping ...... thLo.lr. do tho- modom hind-Wg wttit:h drmttl. u....· I" loslt!fl lo tlrit pn..ldll"", A ""lIh .,,, that can """"" the "Itr's"und ..I ho>ts "'"" ha,'.. o.-.r ,ur";,,,,1 h.....·fit.... K,onn...th Rpet.... AIt... Krame r and M . ~ n [6Slt mlg..
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Sensory Exploitation of Signal Receivers by Signalers Acmah.", '''';l':i''''k'-0 A.....kor ~
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Sen50ry Preferences May Precede the Evolut ion ofo Signal If "-'fISOry "~pklibtiOfl i, ~ m.'I~)f /"'-1or in the origin of rltfhauSry p~ even lhoullh the y no lon",'r e~hihit the com pie, ' igrtdl. them... lv,," [loot]. Thi. conje la~e blue .,Nominal p.ltcht'S of many other membrs 01 its genu'. TIlwta ilsim ila'lOlI'>o' """ nat,,'ally by ;!S ""'tl~, 11'>0' owt>ftltoN la~).{Ri\Jht)" ....._ I.." ..,klf!! wit h." a"iIie'" 'tf!S,anache0'00' Photog,ape. by (left) S,~ Ka,iani. and lrigh.) Ian Jonf!1" 12
tf!'C" I~r< ~ 'efta;n "an. ~ thou9h !!ley do
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abdmn"" ,-i,iblc. But althou!\h the s;~l has been loot in S, vi~lu" lht> bo>ha,,_ ioral "-"fl'O"S'" to u.... lnI'SI>d.~e has no', a, shown wh.,,,, SO"", cxpcrim.'ntal subjects had bluc patches p.>intro on tht'm. Liz.rds thM """"""ro a ri,'al gi'ing a threal display cnhancrd by lht> blue pa;nt we", la, mo", ~ kely 10 b.d, off than we", liz.rds Ih.t ...."', a d ;spl.yin»; "ppone"l thai did nol ha"e blue patchtt> c.ud.l 1m (a qswordta.il"l. nor is i11ikely thai its anct>stor had one (fil\Urt' IS). And yet when
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Th" '"' PO''''' f I".. t a u kl" " ' 0 , h, .... "'ilOd.1 oignalo . The frO''1Urim.....lS, whkh involn't! outfitling zd",. finches and long-wiled fincht.o with ra' he r ridkulous-I"""ing while It'athers gh>p, "",It'S ea",bl,' of producing exaggerated ",,,rt,hip .,ill"" l., w"n' phy,i,.. logically cap.>ble "f helping t" "". a ,ho",y f"male', of/spring. If il had b1
rourtship "'lQ"'ls, 1"'_ " ...... k-s in tho.-,~ tlwt Iwl'f""""'l to h,we~' ~Ulf""'"'\t ..-t.lnl 1< ,plulit.>tion would .......Uy ho> " had hIgher n.-prod"". II" .. ~ lNoding · tw.lly to tho.- n.,.~t "f r-JL~ to be I.okf, '" by t"'-oir 1p.>1'tnI."P~ pi«'t't>y~, Bying ~ .... .-nd\.1ngt'. wrtiI iI ~adtWI~' ~ , ".. [JIll]. nu. .. how ... oIutionary _1MJr6 must uenar in l\iliure bo:a...., loeift:Iion CMV>Ol .w1 from oJ. r.and.as ....·o!o.·oo trom"ml'~~ "........ ftm dill-II had M"'''' .an in"'Kr.u p.>rt 01. fonda. bo"C."", ""rbi.. on>US b;lmboo ... t Inste.d. 1li-'ItctIon.o<Wd OIl ...rullion in the p.>nda·. "'ri>;t bt_. "'1,,,,11 "' ' I"ob and <Jdoe"" .. ""' ximum of sj, offspring pfUII'0 which they 'lI,""ted by. yelling companion. Photog"ph by 8emd
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Chaple' 10
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20 Yelling I•• r«'uilmenlsign.1. C.. explOited e~he, by """yelling .."ilotial iing"'lon, and pain 01 by lo'i1" group; oI .. _~ ...."Y of lhem yeliIng. mo;t 0I1hem nonlEf,llOl;,,1 .ut>ofdi""eo. Tho' g,.p/1 ""''''' lhe pef(""I"9" 01 day. on which <arca" ba'n W0"
In.tedd, hs who.'" thy first found IIx"", p..map". h yel.,r's ri'k of bL~ng tak"n by a hidIng coyote or 10•. 11,.. inco m ing bi"h ""ould bL' attract,>d mauShut up 10avoid aUr""ting more Cd"""-'. which would bd dat.l that .upporl....-l .11 "f ~ p,.,.ji,'ti",,-, (Figu'" 20) [51);,]. I Ie ~) It> "thet """I,'rritorial binis can include bmefits (1"'"""",1 ~ to food fo r the y"lI"r) that uutweigh th.' .....·rg"lic ('()Sis of yelling a' wdl .>s II> to individual, who giv" tl> call und"r titC loud chPt>po; and f""I1'S mi~1 !\ive tho> localion 0/ the ""'I away 10 a U,t"",ing haw k or r""co tho> renW1
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"'-"\e". (81 Expcri montdl " dybad 01" ........ t'" 1>og<J1",!caH. At art,fie,,1...·m placod on tIM! 9round ''''ukod 'n hi9her ,a '", 01 d i«"""'Y by prodd""" cornpa,od wit h a rtme"l 9,ound "". " -_sed" by pl.ybac k of 9"",nd-"",'er I>og<Jrng ; ",al hung~r dnd good hed lth.. ma k" in/; il w",thwhile for the Ii, tening pd,..., t 10 gi\'g mo", loudly lhan o'u.l--but so do their bell,-r·fd siblings [1071]. If 1"''''''1bird, use bo-'gging intensity to direct food to healthy offsprin)'; Cd? able of vigorous begging. then p.rents should mal«- food ddivtT)' deri>;i<JnI; OIl the b,1Si. of their offspring's e.11s [6211- In'''''-'d, if you take baby In:92]. In .nnlh", ,tudy. one of Iwo parenl pihost pa""'ts work as hard fOf ;t., they do fOf a rompleW brood of four wart>ler chicks 1622[, If you pl.ce another IlI'Stling in. ~ w.rt>l... . ·s ......t, choo5ing a .peei' d"mnslfale that this cxpo.'Tl'" is "''1)' small ",Iah,,~ to !he poh>nlial eal"ric gain 153[, lhere-
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""Ioodlrom. _ _.n-..... _ _ .. _ d 181. . . . . _ w_o". An ind....idulh in rn~~ his (11' ...... !V"""' ...... ho.·.lt«Wd~· ........ than iu'llus OI' . -n J"""O'"l .......>duo;t".., ......--lr ~15 ). n..- ..umalolhof .... nn Ihrir~ """'h\..,. may m I'ifuct toe d\ ,nK.._ of Iht>i.O\,.-n geno""-. Thn1>It_.• ~,nK """dinK tNI .... ppt"O P"''''''u.. bu. IIIht> e~rn- of i " .ibhnll"_mlltt" lt.o,,;or and a... "-,,worded amln:lingly. In addition, in those sp
llcts 0" tlw .."olution of communic,llion s~"Slems, For example, Mike Ryao wonden'd why m"l" tUngaralrogs oIt,,,,,o;;"" whining call" without chucks when I.>mal... of lhe i, 'P"""'" p,,'i~r mal"" Whtl add tlw chucb. To add""" thi. q,,,,,,tion. Ryan and his a_",ial," asked whether the fitntss cosls 0/ giving whiI'ld to ",hine-chuck ,ails than to whine calls al",,~; in f"'-1, should th,...., l;Ia t. "'l'r" mo ..' th"n twi ... as hkdy to in ';py "n 11I,,,,lhm,,te "-,,cive r ma y a l", 1;10.....pon.il>le 1m tn" di!fbbing ,iK""I ."The rapid atlt'l1-ual ion 0' the "",-",," call rompn>mL"'" ;1. effediv"ll wlwn·lht' callt..- L" More" w ., !ht. fno.j..,...,.,;",; uf the u ",,"," ""II lie uull,id.. the rang.. thai haw k, can hear best . whill> falling within lhe range of p"ak sens itivity o,!he greal tit (Figure 2l'!l. As a ,,-,"ull, a great Iii can "_ " to a family mW h.n...k unk» the pn,dato. i. It.... than 10 m..tt'n; di'lant If>3lJ!Jf the "_I" call 0' the grea t Iii M, evolved pn>pt'rties IM t red""" the risk of detection by its e"''llli..., then unrelaled ,peeies should have com'e"8rnlly """I,'ed alarm . iW"' l, wilh simi l•• P"'P"rtiN' _rod, in 1M D.H kHz .. nge tNt;mo f. i ~W I~~ 10 dB Iowo< in i~t""~lylltw~ lho.. Ihll g' eat tI" c.~ M..,Bul grN t ti" u n detKl I~ 8 kHz _rod li~ lhe '",ge at llle">ee\"U ll ! lhl lI, fo il)' JO dB f, ;",,, ,1wI Iny 8 klU _00 ,tw, I 'parrow hawk ~. body ...... tho' bHch 10 ..... wa"".... hilo> tho' "ic!or t>olk-. in .......v. bu' ~
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Prior 10 tho' ~bon thaI ~fnr-tho. go",d--.;lf-tlv ·ih....• h~l"'~ ha,... ...riuo 1oti;1C11 prob......., ,'-"' p. 151, man" f"t"T'" is toodled, and often the other ""'"' imm ... dialdy concMed the f'di., a ~'pcko', By .".....din!'> to thi, hrm...! .ignal---ht with him, ju.«t as. pan:nt bird C.n C'lUnl"n the OCAAin!,> or its chick.. tn indica,,' iU'1 hnw hun".)' and hea lthy they ....., I-\Ih.-n ,mall•..- rivals withdraw upon hea.ing an honst si"",,1 from. [.,rW:f male, both parti... gain: ........n mal... do not w •• I,· hrr,... .nd ,'n,:.-,;y in a battk they al'C' unlikely t" win,.nd la.-,;" mal"" sa,.., ti"", and I'flCrgy that the y would
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TI, . holullon Of Communluhon " Ihtorw,,... !w,'. hl ,po:nd struggling with annoying 5mall... loa d s, Im agi"" two kind, at ~w mdi"iduals in a populotin..- that ">ughl with ead> ''''I'~.,.· I unlll phy"",aU~' tk-lW1t.'\i or ttw oClwr thai cho'dy laW ~ -'ucinttlhP ,ahrat predl>cins IIwm. Thi&in tum wouJd ~ JtWeally to thr ~ at IhP gt.'ft"bc t-o. b an ~ ~ !hal muId ""I t... ..... a1uod by dMPilful ~ U tt. at)tUnwnI ... ror1't'ct. ..... an r-tict !hal tIw ttuw.t d at many un....... h.-d ~ ..... lohould boo~ .... to plOdIKE' and thom'1 diffICUlt /or ""k. .. ~thy mall». 10 imlt.o... and that tIwy lIhouId rrl iably infunn nnl!o ........t tIw
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n the two rompt'titors stand off at. C\-.n.,i d"""ptiV.out of the front of its head, On the end of the rod is a pale tip lliallooks like '."'Tl«,. ."", anirn&b. tlwt It'nd t\l iKJ'On' alaorm ig. ""loon lhal "'r ,nl" p..... 'isling """"""Y bia.""" ~'" mo. h ly, It......""' '" oIulit..... ". ,~ on .hr cummuniulioo oy"""" of \hrt' ~ than
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t"'w"'- oi~".'" n"tl'Ndll~ J"""""i"rJ try- ugh tIw 'P""'"
.and """',...... do-rwr _ h _ bonthb fmm lhrir parApplYing tIw .ad.oPWI_ .pprt>«h 10 rommuntllOd in tIw ......Iion to . . - purz11nll C~ of oig_ ........ .and rKl!1 ' ' ' ' - brh.Jvior _ 1 0 ~UA'. io......,.,. lhrir f i _ In....., ~ '"i"P'""""1l~ ...u--..lioonf; e-ununic.alion ' - brrn """"... IO«tu.IlIr ....................r~..-of""J""'d"""'fl:' In othrr ...... n-.tl~ toJh,o,-;",..u tr_ "",~ brrn ono..-n to OUn.hir !l'fl> fit "'..,....""'f'ids. malt>!I oj oIhrr "1"''-;'" in Ih IIn"'r COUnN try,>fI,"';n" (.llllit", "f an n l\ift-l\i'-inl; bt.-(A fairly r",-...~,t rornp."atiw """lysis of "mpid """rtship !>ollador app"an; in (271); f"r. dt"\.,iled ,rudy ol • b.lh>n-m.kin~ .peei..,,;"'" [1007).1
"",mkl you ""I YOllr hypolh ",I..." " hi> "f""T". whit'" a'" tau", up in lhe Ic",,'.,·, moulh. w ......... lhI""'is It, """"unl It" "'" 1'....1 thaI wht.-n tl>pulalin~ mab r,( sun", but!t'rfli,);,... tne malt.. the km'eT "'" d"mi""nt tn."llk'flC)' ,>I hi. m.t...-.ttraclit", calls, But "",I. crick! fn'K' will km' .... m.,dominant 1l\'tj.....'1"l0.'., • L''h,. ,t ";".J ca lling n",,,by {11R()) Thl. ab;lily may ."rpri .... }'ou in light nl ou, di""... i,,,, ,i Eun'P"'n ~.oaJ, Why? W~liam Wal""-'" 1t>Und thai wht.-n 1l'Id1t.. k,w....ro Indr calls in tIIi. ,itu..\· hon. 1M "','11' .ignificanlly """" likely In go "" to all"d, tho> 1.>"l\'''' c,'lling neighbor than whten th..-y did nt~ du "", lJ fintli~ help y'''''' ~"al"",~ tl\., h)1"->Iho.-si' lhal males who low.... their calls an' mgag.-'d in d"'m .wimming ~, fly-
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II'.... buI ..........-d "'""J'O""I ......... po«'egg>- In.all .........1~ (by' dri· initionl tI..- indi,id 10 thaI produce sp.-rm. tIv """'lItf ~ II~ .... .....- than a til'l of ~ in a pKUgo;- jusll.orgir bOOift ['I241-11v """"" of an rgg is >till ,.."lIy f\.....lr'r than thaI of a 'P"'""- IndrN. " .....Ieo. a ....(by driinitionl It..-... ~ tNI pr"ducno "AA". lhe Iargr g.o._ ,hid> in b>nf. and """" ll..-r animal. a re ...,,,rm,,,,.... I~ti'·r to sp"rm (Fig" 4), A .. ngl t· bIrd I M.""" sperm .'" "'YO """'I' ", "",k "",Ie ani"","" .1"""" )"'$ .... ' ·e ~ sufficio>nt 10 In,""",,,,,,,,, ""'''~ ~ Th Lid ooe. • c tho:, gam.·1e'S MallSgy) [88'lI, Vrm. "mall and hil\hiy actiw, are "upt',Ny d.,,;ignet'(au,",' "I inqual_ iti,.,; bo.'tw""" the "" xes in parental inv
6 ~_( .. t . . _n lhe ""e. in ""u,,1t..haviOl'lnay a,i", from fundamen,al dil'l."....,.,. in poo,...,.1;n"",tment tha, .If..:l ,he 'a" at whid im"" l. c.n produce off",""9. Th< "'. ,,.... con pot...ti.tly ~ more descendan" ~ain. from hi9h ~. of """"t Kti.ity. whe-rea. ,ho other "'. doo>. """, ~n 1~".llty In ,ho numbe< of 'Kept"" individual. of ,he two ... .... ~ to ,ompMilion fo.- ma' w~hin """ "'.. whl~ The oppo.rte un be c!loo>y aboo' ing.
Scien"'"-.. _
7 "'-Ie copul.o'ory driw I. Inlen ... to ~ 'his mole eIepIwn, ........,!I'Oul ImmoO< lim'9l1<m "';'h • dan 9Un.ln"Nd, lhey lured him '0 'he.o_ by ~ng • ,.ope recClfdlng oIlhe e .ni 1 ~ng dummy tem.ole 1e « will'" punuing ,he """'1"9 model. Phol"9'opI> by Chop Dedt>Cti'·.. 'ale. In ~ ni !he">fl ""'~. ""'.... contributions 00- ltwn "f"'"Jl ",",,'ani "'" 01 !heir ~ or m.,;,- ""'In 1>0:"idt· nUlrient> ;md o Wi\ffi to. dukh of h'nili,lllift, an "nO"Ill"" •.bably eanno.~ "",te mun' th.ln ooce. In I. It'1'J'ldW "",y be ab... to pnl lhis It....... ,.,.. n.......-......I. malifsotem to.n.n~ in. d...-rimiNtmg mon-
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9 ..... ediblenuplialtift. """"moo,cnck.. _o:amt1.~
..Me ~ _ ..... patt_.lUCt.d101w< ~s "nd f,mo ll'S r,] snu. l "" Il'dion.likt, .lm""I everything ~I,", importanl in evoluhon.,y In,..,,y, se~ual ",I.'C!ion was Ii",t "",ognu,>,] hy Cha,I." D.>rwin, w,'" d~fined it '" "Il", ad"antage which ""rtain indio ,-idual, ha'-e ",'"r "the,.,; of the ",m" ...x and spc'(i..., in c"d",iw ",Iati,,,, t" "'PnJduc'tion" {287J, Darwin Ih"ul\nt nalur~1 ,...l,,,,h,,,, ,,'Suitt>,] in the ~volu· ,ion of survl"al....,h,lncin" lrait>;, which pmmote titZ7I""'~ inught with biln. lid>o, .antloT Iocb. ;;Ow graPJ'io"'. ' - i bun........... """" .a.m. In ltv as' m., ......1' ,·\d 01..... "rdir\ilk..... nd pn.Jd..... "'~, ~ua~ "I ..llt..... ~tlomo 12ou. tN ......... ...11.. ....... nd« rt oL [201.
,ro
m.:my," 100 (much ."",u..r) ft>m.IL,; in 0fW brwJi"lt "",In " ..Ir.."I. m.>1es and t..."""lto-. ,'II m"n~"mu •• ...rn .os I.....h.>rl>t" 1. who..... moles and 1 1n h.>,.. only on" mallnl\ ""riner. a", m,,,,, ", '"" '''l .... 1 in Il'nllth and ' '~I b,."nh"U, tho.> s.une ppl;".. I..... gn""r 01binh lh.>1 inel....... the I\ull. and ... ndrlpot'fS- The "",k-s ol ....... ies 1h.>1"'" I'0I""I...lly rolyg,-. _~ (lho._ In .. hi-r .. "'8" than fftrwln....'''''''"' in poly ... drou. ~ In .. hid> .. f, C.. rloo o..-..~ lr..Jnd Ihat bJnIon.ohrout "'Y to .....n.-... ;an ~. , ..Iw' ......tI, t,..." nlTlO"< g ttwn th.Il ot InnaIro 13.\tl[ In!hi>.~ .......-........ Ihr "'f"\..t",tn.., , ..Jut" vi .....".. ..,..t1~. otruAAb lor dam""""",, is prot>.........1d initi.. lly ........mo."j l!wll.....mo.'", """........... k- """,'dU1es ~"lh. lIr triolJordin.l... mMrs ..... ""","",II"" 1JYlintl; t.loo> Iu """"'pdt' ~ >tn~. ~ ,".ok A"""'fIi: b.oOO=....
......, _l hun .... t "hrn
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~ ,th.>tho.or rnaJr;. ~ thr!ot """';lICquitwIa part"'-"". ft.....-inK hIm I" 11"'", ....... up......". lhuujth ..... is ""0".11\' domirwnl in ~ ....... ~. Thuo, fur.........ple. ~-.,I""". b.oOOt indi,'idu.ohi gaining tlw Iaq:e majority 01 nwlingo obwn'ftl by~lhdw,'''''''«niogisb Howe\·..... ~_olf"'!r'milr ....~ Ilwt ""'"' INn IuIlf 01 tlw otkpnng "'..... """"" by nw ..... otIwt' INn the domiNf\t m.Iln thal"'eft "'C'OR>p~' 5U(cetOSfuJ In rrwhnjl; on I.ond 112'"[. APf'"n:ntIy. nWto ."'irnmintl.n>und the boftdinp; culon~' _ fnn.oln in the "'....... .and rrw!t thlI,,"",utting thl-lalj; 'f't"'T" inlo"lIwcloaca""",, to any ropulatltI\oIllrl h.~ in ~nd ftomIlt-o "I m""og.lmou~~.~
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Ihe h.ort..>r - ' . "'ho_ m.o"'" ~nd km.oles h.1 .... onlv ,"'" ""'lin" p"rtr\('" ""'"' '" I......",oa] in length and ""~KI'I F"",-nILllh Iho-'",..,.,.. p""""' .rrl;.... lI;'ouP "I bud. that includes IIw !lu ll• .and ..."dp' ........ Thr nw~ oj "f""'Ws INt "'...,..lialJ~· pol~p;y• ...".... (thaoor '" .. hidI • may m.oll: " 'ith than ftom.aJool !l'-"""""Uy h.1.... " .....1ao. in pol y..... drou.. ~ \rho._ m ..1lidt .. ftom.aJoo trWy w .. ith than ON' m..W1 l.aflll" ............ p....- ,1lt .. ith ..... ",;oJ 111201·
It'.
..wo-
Social Dominonu and Mok FitnftJ &tot..._ .........>dwr ......mpie ol .. spo'cies m " 'hid! much Lorgo:r than Inna.In. .and hen> I"" .a.dult \to" c..mpt"k .it lly lor "",..I dominanrt>. C.. ,-u; l.JImut , ...". ., ........... ;an infur).' ,..It' """'fly t"u, """"" 11; than INI ol fnW.-.13.'lIl]. In thi~~ ......... ....... Iho-' "l"',..1o..ct" al of I t - "",tI)' ~tru~1es fof ~;" proDIirmohC, $III(\> man\" _...m.... h.1... found INI h,KI' ","";1;"" in .. ce !\wr.. rrn~' do... nOI.....,..".,.~·.......,]1 in ..... I' ...>rd..... 'Y mpuLoIO"i For .......mpie, " 'hen Col.... Ha"'t.t....."OUIIk'd ropulatio". in .. 100 g l st.lti.ocaIJ~' ..",,,Iic.nl ......ht"w,ip bo.:.uw v'lUIljI; . d ult lIWles han, ' ....... low d.JtnlJ\&l"O;X'.and achio>\ .. """ ..-ff....·t..... Ct'f'Ulationo 193J. For the full) .a.dulllIWlI' IfI('fI\bi.... ol .. b.abon lroop, !hi' ..t>d'f)' k,deft'.ot ri ... J:. in d,l\'d ph, ""al «",In",t.ot~"",.. onIv ~ly " ....It'd to dw n'-""lt'n,roIlecti>-ffi· ronhont • ~ maI thai .... «quiI1:d .. part. ....... """""l!- him tt, jti, .. htr up. ,",'m !h<JuKh "" is """""lIv doominanl m {n('-Qfl""" t1"I(IlIJfIlI...... Th........ ~"""""", in , ..... "''''I'(. yrllow habt thaI rontained •.;!o:ht .a.dult m.o".... th"", Iow·ranking ""'''''' (fifth through ,...' th in tht> !\wrar· eltv Il't'/luiarl)' l" ffIIrt with .. 1OIl.II.n-a!O'X" . ... ..... ~ Nrlief (p 2M l ..'1wn dNq ..-nh migrant and....odml EURJI"N" bLoclbinl!tU; on .".·rag Illto Ih...... 0.1,11........1 t.Ioctic!. d rly vilded d'lh 1fll""'" e-ach bI'/l.>'ioe could not be. "'-"f"'Calt' "'-"redit.l1)· 'tra~: (1Wmt-mbt>r Ih.ol if !ht> dif-
""-r-
nd
""Ii,
19
A ....Ie,.,., _
KOfpionllywitl>
in " ' _ Sctic:s giv"" them the 1ti!',ltehave like their ''''rilo'ial '" ",lellitt, lalh,·", [61:0], showinjo; lha t two diff",,'n!. h",,'dilarily dislinct reproductiw slralegi.., can C,,",iSI wilhin a 'p'"i,,,, und,,,- ""m condilions (Figun> 20) [I :1301. Anolh,>r unusual ca", of lhis sort i, surrl;,'tI Ioty a marine isopod, Pa''' marim> i",'pod ....'id"" in spoll!':C-S found in lhe inlertidal L(l"e of tI", Gulf of California. If you wen> I" 0p"n up a ,uffici"nt numhtor of ,,,,>ng'''', you "'''uld find f,'mal,,,, which .ll h'k mo.... ," I"" alikt', and mal,'S, which com,> in Ih"'" dramatkally diff......nt sizes: Ia,,!,:e (alpha), m,'tIi"m (ltt'la), and 'mall (gamma) (Fijo;ut\' 21), ,>ach wilh ils own l>ehavior. The big alpha mal"" allempl h' .. ,elude "th,,,. mal"" /nlm int"rio' ca"ili,,, of spon!:... lhal have Ot'" or more f.. "",I.., living in lh ..m. II a "',idenl .lph. menun!,'''' an"tt",. alpha male in a 'pon,w, ,1 b.llll" enst,,,,, !hal m,1)' Iasl hours bt-fo'" "ne male giv", way. Sh:mld an alpha mal,>find a tiny l':o'mma male, ...., "'_
20 Two reproducti_ '''.''''l~'
In 1M ruff. Tho: ,OOdi.h malo: [Io:ftl wi,h an e,.a ruff of fes' "f'ng a ·s ropul.-.h<Jn!I, will r>ot ................ hi.. fi!J'00:5s aet1l.at.·l\·. And in many~ . not all tr~ loJ'l"f1'\ Md"m•.'n. A "'Ct'f'live femalg "'~_ Pholov b,o "'" ~~.
338
Chap,,,, 11
Spe<m compeh th.- mal. bLo' [3-I'IJ.ln a flJ': fertili7"'tilllls, but acti"" play.", in IhI: [12521·
Ita""
_,lJ'KI
I'""""'"
Mate Gua rding Coml"'tition among males lor opportunitie, to I,'rti!ize a h'mal,,' ~ t'lQ;' has resu ll'"j in the evolution 01 male guarding, a strategy in whid! a male att.of" .... "f'"'"'I will rout
In CUtt\f"'I" with lht.....uf <Jthtor maII'lI
to:. Ihe "lQl:' uf ....
.,n;...,"t'd by sc.uing thr loorrW1.1., with . ....... in ordor 10"""" <Jthtor ......... .h<JUId ~' d..M.o ~ her CF'l';Ufl' 25) 1 1l~ n... 'I I$, dt_ thr bmr !iJ"'-'f'1 with an . I.....od~, in.olftl ~ rnuIt m It""",,,t ""AA h>rn1Iz.Iti 10 outw"ftgh tIw roob uf guarding. ~II~' .n. .... uf OJ'J""tl'nibrs to...n. out <Jthtor ........... > Jani- ~ .........N tha <XMt in thO' blue milkw'ft'd b.ri in whic:tl tt.. mOo norm.olI~' ....,...,. rnounto'd on thO' iftnaIe ·, back for h M ropuLolion. \\'hetI Ilri.inot... _'O'd from their p.utJwr"o. abo. t 25 pnn-nI oi thO'""P" ....wd f""nd · _ within :lO nunu_ Thus..............un mounk'd on , '"'-'r ..-..un.allng her ~ . ~ C'O!lI K. thO' guardm{l .......... displ.K'mrfil. of malt' "uarding in ith t"'-, pn,b.lbihty that ungu.mll..l will 10 and U5O' his 'f't'11Il ttl ft>n'Ii m.,i. ~ Ill--!. 3651. Jan Komtk-u. and roll...."...,,; u"""" an ingnUou" "'F-'mt'lll to cM l !hi, prediction It. thO' s..y"hello:o .. ·.rbIrr_n..y pLoct-d • 1.1... nunabon '-'J fertile p«Iod ( 1 _ 'IUI·IAI Con.roI paIr~ ... ";'ic~ the
""",e.....
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lema.... Ihroughout ' peord.IBI P ... ,"",ic~ lhe ~'. e._i"Ie,,,.lIy 1nduc0b,'iousl" aff""t 0"'" a"oth;. let's not f0'!lel
~boul
ft'males. The malo> choice com!""""'l of ""ual ....ldds that they will survive 10 reproduce 1429]. As sUAA,osl''om she also ropulats. Bul when il comeo; 10 fertilizing h \ "-, ptor.. in "" "AA M.l" cltaoc..- Whkh mal< or "",i •.,. will to" the ';~ht to to" 'p
llI'T, which 5hc ha, "tst.lined int~mally in tiny ,pt"I1T1 "")fag~ lubub in her ulen'f1t WdYS (117111- So"", females, fo, " ...mp\e. make it no< h. ... cl-tipped "'~~'.
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fI,.••h ....' n/ nUl"lol p..... lloemic:.Jl, in 099 production. ""ot"'l'.ph by Klau , -(;@, h., d Hollo
33 Sex".1 ."itilie in .-..dback op;d ~r, IN n.., m.~ .Iign, him1.pL>1 the .....lTal romp.ortmrnt , Fftna ·alli'll'ti tlr' "",,"I '"u"""pdy 'f'l"'TIl'd in a .....t .-r the ~ mak>, whim in natuft' would ",,*""bI\' W the l>cttlT falho.T of "" It'''''1lT uPM-ity 10 ...."... '1Ill tl~ Pft"i.'"....... In the h~ .....t . tid J "t>..d tnnaIoo 00 no! favor largo> males in " mila. ""f""""mrnt>. m..-t. tt.e,' id!. main thaI an" 10 proJuno lJ\oqurnt lx"d' w""-"'duringrourtWp, "l.aIf..~oI bo;h' wk· "'It aho fOO1 "" '" ""' . - f.onrlinK ..11o:T y bl.Jck...nd· ·hit.. "",10.." al,,,,,,, (all,·, . 'r1 "'·..101 ltw-ir ""'t...., kill..... tlldn that of ",...thn~, ' '' 0 ...:1 by dull rna"'" al",.." inJi'at~l~ that bl.Kk... nd·wh;l~ "",w.. w.'n' in,hod ,uf":,i,,. r,uh.'", [10101, D,i~h t pluma~,' ..1" , ,a,r;'. . 1/,.. d..y wilh ft'm.I., fi""h.... whl, prefer m.lo.... th.lI h..",- h";~ht nod ft.. t...., p. td...., .... ''PJ'''''''' 10 p.ll~r o.~ng por....ilt· ~ lllV].lf pud-...t.... do:,aflportion of ttw ~ "I. ,"",. The!owef the «01.., the . . - , the plu "'"9".The "'pem with lood o r SOffil' othe' similar J'.131 . The p",fe",nce /or intl'flSe courtship stimulation may e,,< stimul",;ng mal.. genltalial The """" eIobo-..te peni.... "" tt>e left which might p'ovl ~'nilal ,timulation Ont> way to l............ within )lroups 0/ dosdy rdatt>d spath,'c, "nil' III g lu,' il ,mlo anoll....r bird's tail. thereby len"llldcd cistirola, ""'''''' wllt_ \;IiI, We....artif"ially shorWned "''tJuirt'd ,upt'ri"" tt'TTilo",", and indua...by p"'" ,u"",bly pmviding gmltt>r ...·n'. .")· ,timulahnn tt, pUb..ntia! m,llt'S, (On the oths, and why are I.. mal.... ,."nt'lim,... p"rsuadl-'d by what Itwy ....... lIt'ar, "mdl. or f,,,,!? If mak's provide only sf"'rm to their malt's. fernales rannol use the physi, or their courtship beha"ior belo...., during, or alter copulation, as indi· cat"ll< of lho.' mal""';a] bt..,..hts, such "S h tht ma le courtship d i'plays .nd ornaments provid" information to f~m. l"" th.l ........bi..." tht.", to choose males wi lh viobility-promoling gen79)and Mark Kirkpa lrick (625J. lmal\i"" 111.11 a sli!,hl majority 01 IllCm.ales and the produclion of dauKhters that will ch",--" thi.. kind 01 ma l.. for lht>ir own rnal,'S. In facl, the Land....Kirkpa trick m,> start of the proct"SS. ftoma l~ p",f"",nc"" """'" not be directed al male traits Illdl aT'(' utilildr;"n in lht> sense of impro\'ing survival. feeding ability, and the like. Any p""",isting p ...Ierence of females for C
""t'T
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Testing the Healthy Mate , Good Genes, and Runaway Selection Theories Discriminating among IIws .ig.... 1g ood g .......1 ~O< ... witn m..ed In,mpo!' ""
•
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IJs.>quenlto mating wilh a topranked male 1m). AU of t:he.;e dlects might easily be attribulffi 10 the "good gtm'S" 01 the male when in realit}" !hey a"-",, from the female'. manipulation o' her own p,,,,,.'Iltal un-estmenl, no t the genetk contri bution 01 her p.>rtncr.
Sexual Conflict between Males and Females Brett Holland and Bill Rire ha"e pn'f'OS"d yet another scenario thai could result in the evoluhono/ e~tn'me ornaments and dL_pLays in males 1533). According kl their clwio---a way ...ll'dion th.... ry, e>uld drive the proc"'-S in the 101lowing rnannt'r. lma~ne that a rnale happened 10have a mutation yilding a novel display trail, one thai rnarldged 10 tap into a p"",~istinl'\ ....n50ry bias 01 the females of his specK'S, A male that could activate thol p"",~i,ting p"'r.,,,,,,,,, might induct' f.'males 10mate with him even though he mighl nol pro,-Ide the rna!erial or gtenehc ~lIefits offered by oll"'r malt'S in the population 1m). tl>c ......"!ling spread 01 e~ploitative males o'-er lime would create seteelection would then fa'-or mal"" abl~ to owrcome female resistance, whi"k>... tior> Dy male, rMu<e> /to",,1e f,t........ lhe .tog< I, set faS becau", ""'ir no: pamw,', "-'Produc!i,'e oU!pul ronslitlll,'
355
43 ~xual .~IKtion an;
holu tion 0/
,'w" though th"i' ""hon•• rt> d,'trirn~"I.I I" f~m.I"
fitn~
0".,,- the kmg ha ul C1I "f the planl rather than fo , aging ,m the ,>u t.". flow ~r.;, whe ... they will be constantly assaul l ...,.., ....".""""' tail ~.mn.r by """"'ll: _ modi' _ ' wi "" 1Mgn by ~ t.oMtwr ClI*>ltWtaib [!IJ4l8ul ~ ~poupin wNo.....,.;... "I' Ihi. """ bI' ad.p h" .? Pn>dUC'O' h Y p' >t ~ ~ nd al· liI "W frum 'OUrtLnlllmlales wt......, >kin Loo::b bLoc k orot" that ..... ca.-! by ~ pu.... t>;; In.'m.ItIxlk>m.1k>. W..... GunilLl ~andK.-n"" ~ r..",_.....:1 Nac ~ """" mlo tho> olin 01 ""p'.Mi~ """"'..... ~ ....pmrr«nlal. I}' .oI~ inoji,·ioJ nplUdv '"
wothrft~\.lI(1jird """",,1bffivio........ ~ "",n1 optg"mou. !ry (p. 327) sug;;,,,!s !h.,t mab ,hould generally try to mate with m..ny f.'m.. I,.., nnt jU'1 nno', ht.",au",'a mal..', "1'''>ductiw .U("'-'5" is u,ually ",bled h> lh.. nurnbt" "f f..mal... he ;n>ernitldl..s. A, a n"ull, mal", "um pt'l.. fo' m..ted in th.'SC 10'''''', mal... th.>1engd ge in gt'""tk mOnOl-\"my-'md th.'n' ~n' ,,,,,,,,it"' with thi' mating sysl ..'rn---.lrl' surpri,in!,>. V,lI10'" ..... pLul,lliun' hav .. bt~ "fu,,,,.j horwhy Sth.'t m.:>te, wilt",,' 'f"'rm would then fmli"" her eggs [362J, 'l.lat~ gu~n:l i "l'> i, "'peed I'drt"'" .noclied to lhe tip of ~ obGornen. Photog ' .ph' by Chn'tol Rou,ir partn~. """,",' an inl\'n'sl in a MKhbl..-llIi"I]. Tho> "'...... is InK' for paiR"d f..-ma"," '" I bur,,;nll be.-tld f 1 w"rl< ~ to bur)' a dl-.d. ""' or ""...........·ltich "'ill h"ir.~.....,..~ · bald> from IN~ I h-nw~ Ia~" on Itw> .......,__ But .....,.. tlw UIlhnlli .pou Itw> ....pm......,""l 1Nwd K'nII /or much ~!han contml..w,.,; that had \t)1 m,l k 10 infants. "",...1m in , .-.....l), n-quili"llINI , pn"'-'two ......... fnnaJn .. 'OUld run tt. risl< tNl intruder lNIr5 WOIIId 'i5iI ungu.atti
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1",,,,-, thaI r",sed Iht'm 19221- Similar ted"'i'l"'" "ppl;",.llo f1orid.. ..-rub iaY"
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. ~ ,"'.-no in<Jo:oN tI¥ off>pr1nR 04 tI¥ .dill'" tNt caR'd for tht-m ]'I!(II \\'hy """.... ld ....,;". 1 (.and got' "wWoww" f....... l... lNI ""rm'tirmos n'An-"ha'l'I1' redUCl"d tho: .tarlinp· will"W""'" 10 f.........t lMT broods (_ p. 171». ~ ""'bw..... Ki'·..., an anti-andn'K'-'f"lc dwmic.al whidl bloclOO tho:dl.'CtlI of lhoMr naturally citculoting _ . A n d led Ih. M,.. Mottono ...t [8181.
-'''9
I I .'------,';----,=:;--:--CA ("_'''~ T hpo-n...... tol '''''mir EPC atl~mpt. do no t "~p"__ lho>m to eudwldry by tlwir own sod.lI mate), but wh.lt might fffil to avoid cootaci with EPC ..,age. mal,,,,. In otllt'••pee;"", how """", Ie""'l'" app"'u to accept. or ....·c'll ",Iicil, ma ting. fn,m two or mon> "",Ics. [108]. As behavioral biologi'l> !la"" con templated wlldt /gamou. lemal", [453). Simila rly, in Cunni""n'. prai.ie dog" p",lyandrou. lemal.,,; beca me p"-'gnant 100pt' f'Cffi1 01 tho> time, compared with 92 pt>r<ent of the time for mon ogamous lemales [5461. How",·e., Ihpenn dono" .... _~ will improve ,>Il'p'i~ vlab, l,ty . or "",,,,,1 ......octiv M. ling w'ith """oral ""I.. in from .",,,lOlly har..... "g • t"",. le. More ""'leS me." gw'W< ronfu""" .buut f""""'ily ,>I • f" mAIe', oIfspting and hko."I1lO h> true fur lNI1 y btn:b. lndftd. ""iden«o has """-""";rds ft'lCularly cpUlate oulsid" ttlar """IS, mdudlnli\ th'0 !ICJCi.ll p.a ~ w"'- oIkprinli\ """ will ... ,.;;,,!, IN~' flTtiI· ;2
Mille Webn roul WaTh. lh.>t INd,' lI't..ir la t"'·.,; atlr,Ktivc. The sons 01 sexually su ."CCSSlul lit'ld cricket> a R' indf"t'd m ,,,... allrr mak' (FigI' ll' 12) [11'lS1, This !\'Sull sUM.'SI, that Icmalcs can gain superior quaJiti\a'Cd l>y th,' );d 10 mat.. a, m.ny.' 12 timds of tim bfo l.. y~ .. romplete dutch of "AA'. 111ri,,, (hllu,,-' I ~), A ft.m~l~'s hol dinK' may .n,act fi"'l ""~ and tlw" lat", anot"'-', rn. I~. n.., fi"'l nid i" ma"", with lhe I"mal" MId g"ts a dulch 01 "Uo' to incub.ll~ and rea, on his own in lw, kmt",y. which she "",hnu,," I" ddl'11ducinll a J1('W dutch fll' a " "" ",d mate. A, a result, ~ It·w 1"",.1.·, a lour'-'U maximum, a trait iJ1ht,tit.>J Irom an "".'male spoHro ",mdpif"'rs 1h.1t dc-sert their inil~11 f"1rtners can find "",,"' Of"" with""t h.'nnin)': the ,un'i"al chane"" 01 thei, first bTOod. On,.., he ha, ""'''' d",,·rtt>d. llw TIMk', optio,,-, a .... limiled. We", he ..I"" Itl d""'rl 11,,-, egg'. lhey would Ian to dewlop . and h" ",ould have 10 sla't all owr again. I/ .. n f,'mal,', a"" dc',""I,'rs, Ihl'o a ma le Ihal I"'rforms Ihl' rok 01 sole p.,,,,,ol p ...... ,umably t'~P"rierK,", )':",aler "1'n>Jucti"e 'ucc...., lh.ln h" would other"'i .. ,-",'ell if hL' l"'rtnt'r """lui"", another mal\> 10a"isl her with a '""""": s",-"",fut defend,,,-,; may .i", a, m"oy a. 50 youn)': with lhe r,'males in lhe """,,,I [7801. Simii.lrly. "",It'S 01 the '1·f.",lt'Luma ,m>pt'TI'iola. a I">pical blackbird. try 10conlml duslers 01 ",-"tinl': lemal",. which group their long, dangling ""'Is in Ct'rlain I""'-'S, Thl' domin"nl mal,' al" n,,,,t I"'" "-'~l.5~(?·~~
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Th. £Volulion of Mati ng Sy.r em,
379
Female Defense Polygyny: The Female Perspective Fornal.. dei,'flS mllili"r" " f fm..!it lrom ~,soci"hon wilh one 0' 100'" polygynou. mab thot t....'lp pn'tl'cl t1wir cul>s.
Ii,,,,,,,,,,,,,,,
Resource Defense Polygyny In many 'p"'Cit" h(~d" lhe 10"'" likly he i, t" a"'1"i", ","wal m,1!''S , In ,m African ",pro!OgU5 callipleru" a I~mal~ d,,,,"il' a c1ut,h "I in On ,'mpty """il ,lwlL then pop' in,id.. 10 "-'main wilh her ')';gs and halchlinl'S wuil wy a ......ady ,,, 1....,," tlu, """I. T~r ritorial mob "I this sf"-'Ci" un' 23), E!l.. I" all'" Ih" matin!,: sysl"m "I 0 'p""'i'" oy movin): n·s"un;... an.,und. Iht>n.';'y " lteri"g whew I"mal,,, are l"cal" d. Thi. predichon WaS !t'>t SClflg"ird. f''TTl"I,,, nUT' m" Uy COo,m ,we, sueI'. I",g" "",as huntin): /1"g g"v~ ",'m~ f"males suppl"m,>nt,,1 oats ond m,."lwo,ms fo' monlhs "I" time. female hom" 'onge' cunl,act,,J ,0b,lan tially [mI. Thotr!nern t""I,'
The ri.k of pted&tion Is ~&11!'d 10 attt&etl~ne ..
of. le"lllII'y '0 ....,,-
Ing _Ie g'''''1 _ watblergamou. femal ... whose n>lation.hip with a mal" Ia.ted the whole b.-ling .... """ had only ' !iKhlly 1l"'.le' "'produclive .ucces. (1.6 younll fledged) lhan fe"",lt.,. w ho pa r!;ic-ipatclumped in ,""aIL d ..f..n';bl" a""". in ma ny other species =d "" r. mbl. compelillon pol y ~ yn~. The """"'" "-"""r>tive females of a flighlkoss Photinu, Hrefly, for exampl
"ru s
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opportunity 10 ,, j, ",.,.tTi,t,>l1 th i, u'''' nij\hl, a few h ighly a~",,,iv,, terril",ia l mal", cannol monopolize a di'pn>porlionale numbe, of Ihem . Therefore, male wood lrogs "",hew t""ilo,ial hell.w io , and insl...,d hurry abo"t ir}ing to ,,,,,,,,,,nit>,''''''' or mo,,' cgg'~ld,." females bel",... the o,-....-night "'gy en,h (FigTe 211) [153]
28
An .. xplMi~ br....cling as...m-
blag... Amalewoodf''''9g ,a;psaflomale {uW'" left) be has found be lori' ,j;.~ ""'~ two of wr.om the """i"9
I"'"
.,e ....'
~" Nu...... ous fert ili: f'd egg ""'ss... fIoa'
in the wa'" """,nd .he frog •. Photog roph b)' Rld< Howald
29 L'" ~yny In tM ...._
I'd ........kin . Tho b*. _ _ .........
tiny di>Pllr _ lI\Ir _ dortI_ 1J:I9di.o~· bark 10 the rwch .. iltt. buu•.and m.n bId.ond forth . "" f.tol tat _ 10bo> bounconglnd"~hlo>. fu..crad • [llJ7'Il. T1w "";"ol! of .. ftouWp .. t the lri:. ~mam· ......... Io.hspW~· ~.pf..ducintt!:...,uprou.lfthe t.m.ok .. 1O'C'r'J'O" .. ....t d'ox f"'rtnt1'. ..tat fbr., 10..... pry hiKh in. t.......... he", he p ~ d ......... 1oud criI.'5 thlt .ound hlo> ". glass bo>ing rapprd hard on. pom-i.1in sink" 11-10). Re«-rll\ ~ I.. m.ok>s fly to tl>d ,,'u'e'" of lood of unpred ictable availab ility_ "'pemov al 01 thI attraeti,'e males will cau"" the cluster of subordinan,,; 10 dispt'''''' tn ,>!her f"'Pular m.tl... or 10 le,we the site alto)lelhersi" All... Rintat1Wkirt ai, [9701. I[1l1-SQu .,~mrt ...
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oimll'I 2ll ~I 01 rIw ......".., .. ~._ k-I< WOO"" _ _ than half the ""'ling> 17J9~ E.~. m, sUAA"'ting IM r fentdles gain "good gen... " from the ir chu ic... In a, i9 also f'If,prinK fmrn 30 b",,> 01 genetic >'ari.1bon in ""xua lly lected Irail>; are doubtless ".ried, but the development of some of these attribut is strongly affe.pLoy t-. """ booon iolOnUpt1'd by a n....l.now.n,: N ' t.m.ok> .....r d><Jiol" in this~1II1Notis """ ...wtOOlo h.Ir 1.'II .. ,oOdanc. [IOO8J.) 11 noIhin~~ . , h"'" COS~ 01 .."..-ching Iot-.and ~·.h.. ting ..... r-.dUC'Od by ~~ io " 'hid! groups oi.....w~ advem..., tbrit J'ft'W""'. ..,hidI ~· mU.e it ~ ...,~ lor ..w... 10 """f""'"a'" by IeU.ing .and for aullOln lo ..1~,
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nw ...'01,,"" 'Y ly... oI lrk~ing brN"ior p""-idos. KUod ill""tra_ oIlho pru.l UCli\"ity 0/ .n ad . ptation"t appft*;h 10.ni.....fbrNviot'.... hich ho....... bkod ........ "'ht.-n to idmhfy.nd inv",,,ROli.· .....·~.I ""';0. pu,.zlro ....,.;.t.... with th.. "",ling .y."'m••""h .....hy mok.. """P"'" in d"""" dl'p l.y .AA"'ll.ti"......nd "h~' many fwn.ok.. ...' nlt"n cl>oo.., tl-.< ... me pa rt. .m""l1 til1 ,,,",,,,,,n lt,,.'''''' ""'"' .onlho."., (l) tho.' I>.",~-.f ·n ·m.it's I.KliIc lhd' "..,.-ts!h.>l s\'md.rd [571>1 · UoJ...,. WMI rendilion, would la,:oc 1 bo.- >Uf"'rio." It' _ 2, a...J v"", ,-..".,? I It .....' rosI-bgamy in li!',ht oflhe follt''''ing evid""""" m.ll p"""""" do... nut afftot.1 th. sutvi"al 0/ th.ir '#,;prin!\, "",Ie> conre.Il the f"m.",', .",In"" condition by ",,,,,I.ma rlt,ng owr alllXlors d""""i!ri"" than IDt"">g"m afft'lny of a m,,"'? Also, if m.Hing w;lli other mab p n ", iJ... fem,,1es of a gi, ...... "P"";"'; pli.m.rily with lhe "f'P""lunil)' 10 trad;> up 1o" g"""'kally or '''''It'riAlly ,up.1"R>t partner [20'11, wh,,1 i.. tho, prt'Ji ,k... """,,Ii'e. 1Iw dUlll\OCo., in INt..., alpN Mod ht-u \00 ....)' bod> ropulail' ,,·,m Ihr _ f.m.J1o;.) b'ing III 1Iw ...".....,.,.. H,.... r\ Wllikr 1Iw d Ulll\OC.... "lpIY malo- _ _-o..,d""" the amount oi help they ~"e I\l ~ a..lhm .... ~ ol'woRo ·1wrNs the btu m.J.Ito ootIr pomIIl if>-.ry
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We will look at several o f these questions in th is chapter, starting w ith the Issue of why in tho'>!' species in which either parent could conceivably help its offspring su rvive, mot hers an.' much more likely to oblige than fath ers.
396
Chapl~'
13
Why 15 Parental Care More Often Maternal than Paternal? The firs, ''''P '''ward exp laining why p.u'''''al b.+•• >"iu, is ..."t II>" '0"'''' in ,,'""')' .pecies i. to rocogniz~ lhe phy,i"lug;cal exp""-'" uf tho> beh.wior, whkh can be lruly impJ'(";Sin', Think uf the male ""'perc,. penguin ,tanding in tho.' bl.. k",,~
"I the fri~d Ant>rdk winter with. bli7.-Zard in PnJl';""" whi!" O'adl"" an gg un hi. fet,t, The pen!':uin will not ~at for mo,,' than 2 m,,,,ths while he inmpl,"dy igno", the chic"", wh,'n they ,,",tch and I~,wc th., ",,,,,' M",,""e', why i, it that emperor f"'n~uin, and mall,,,, f"wl an' exceptiuns to ,he ",'",-ral n,i mo" of t~ f>a,ontal ca", hi. clfwA....1 In> ..-4..:ah IIlC..........I 01 """,,"",,"I "n' I§ oubt«t 10 SohouJ,d \cia,. _ ~"In!( ......--.nd.1nt> on ., ~ tIwn fo:rn&Io:,; tNl f"O'Iidt' !hi>
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m.any ~ ... Ir ,,'puin thrse in II'nnS oi !hi' in lhest' sptrit's-
"""""""I ""'""" ttwn "",_I CiII... s~_' M'-" '" "",k ...Lot" " /01,,",,", «>!,I> .nd br>nefib to "",I , , f ~'«"J'fM_1Utht ~ of ftorn,ak>-onl}' parmt.1 c f"'ri"lly nu ........._ ..m,,,,s h ....... CFill"... 2). H""·....·eT. """,", /ish "" d, fl l lrom m.t\r>!; of or""r ",,1fl1.xh del""" and ...role tile ough hi, .....1ot tile t>o... 01'M oqUOII< I'ion' '0 f"ovide _ O'J'9"I' lor Ih."'99' W~hin.IRight)The molo! Rondo"". jowfi.h l>rood, hi, mo'.', 1" .......... buI ....
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T1>t-(OnWInIt cicttlid . St. p...., 'S fu.h. in " 'h.id\ rithrt tho: mall' 01' tho: imwk- mov """ fur Il...u young b}' or.Ur m.:ubatit'lllhr t.omlizt.>d "'AA"- IloIh ....~ k.... ..'right ..'Nil' moultt brooding. "''''''' Ihr)' find it difficult Io .... t ..-iltt • m""ltttul " , baby fish . FtIt'thennon>, tho: in,,""·a1lortw....., 'P"..ning!' " .. " ....,.. for pa "-"'I.lliiolt "f b"tt. ....,.... CO dutd\e,; d ... r . pt·ri......"'tAlly "-'mo'o ed (Figu... 3). Hm. '...·.... tho: """an int ......pa...n in l..r,,-al is ~"'dt"r f"r br"odin~ h>tndl"" (11 dd}"') th.In for bn,, >dinK mab (7 dd}"'), ).,10..... m' ..... p.ln"'l.ll I.-"",w-. prod uct' fr...rr young in thrir ,....1 d utch th.In d" non· po, ,,,nlal f,·m al.".. ... h....ed' parental ma l.... dR' 1"'1 a••, b17]. So hy i> it tha.t kmak- St. Peter ', fish ."",.,11""'" brood thI'-ir young? r..,.hap" bP u". ",ar th,'ir off'pring singlehandedly. Male water t>U)!S in Ihd",t"matid ey:. are much la"",r than the standart! aquahc inst'C1 el':.'l. A 1",K" splwn' I\;,s a <malle, 'urf""'e ...... ",tative to it; volume than a "mall .pho....... Thus, as a la'1'" belostomatid "AAd,'\"t'k>ps, it has
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~ ,pt'ri;ll rn-lblom--how to MOHO c.rb " d .."Id.. ou, .oo ",oy!\"" in rap idly ..........gh It,""""'," tht Iu#l rrwt.>bobc r IO'qW...,j for nnbfy1l'm. which ~ tht rioJ< of de\.irootion N t IIw ~ r.n- wlwn thrv ..... "f'O""d '" ltw lion. broodint!; tor that tnOH'n lIw ~ ........,I'dl,.. k> poro-ft\l thnr drying out. _ tht ~ lor ltw f'\uutl<JnMy transibOn 110 l>od bmodmg.' IIw .au-walft" inIori~_ Wouldn 't Ihqp. boo oimpIPr if ~ sunply Ioid .....a ~ with Mrgr
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.............~r.-to.'To~whyw ..... bug>prod\Ueggs""~that thry.-d to toe l:>foo"kd. Smith point> oul II"", p .............g Itw world ', ~ 1f"IIi«tO..a1Jney an' Ioclr.ed mtn a five- or ...-moI1~,jusl as spo!tcre mal.. l>rood· ing romcs ink>play, an ancillary evolutionary.' d..vdop"",nl whost· fuund;,lion Ii.,.;in exp',,;ed aq""tk vt)l:ct.1hon. Why is itt!wt males do th~ l>rooding.. never the females' H~... tlw situation parallels the fish story closely. First, mal.. wat.'r bURS wilh ,lilt' clutch 01 eggs can sometim... attract a second femal... which means tha t ...maining wilh ont l....v ""me aJJd,> of Ill g....... that cod", for that t'l\Zyme , If lemale bats are indi-nimina!dktion that parents should "'F""'ially 8,,,>dilyact cliff swall"w chicks procluCt' sign.ls containing .bout sht""" limes a, much "ariati"n.s th., cnm.'Sp<mding calls of b.lm swallow chicks (Fi!,>u", 8) 17881. If cliff sw.llow adults .... w eJl!'>er ,.,I""tion loav"id kcding ge",-"lic strangers, !h
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9 WIly IHlc ~ paroon111 GuI cl'Ol~blv tho> risJ,; ollt\d.lr f"'I"""'" bv .l'PP""lll no....... with <Jthnd.w 1&31 ~ Wlwn .>do.'P"''' ' 'UUf'O, .... oddo.-.ptI<Jn " r...... ,,·,m """.... than 10, .....'. . t oI.>dult rn>&-biIIed. .sullo W-Irfi in .. !>lr""V" in "'y ,......117i~ T1w 1Tlk- for tho> "'... "'" .. more f.. vor..rk> l of the ""'pcnmm... I1~· ..·id<M·ro fEomo....."""" .. ttr"'-""' on~.n.oJ mol.-I 317I. T1wobsr."..lion thai ltko po l rep"""""""'t """'" w,..... t...._ · thIII I,>und .. fEomole "'hi\!> .hU Lilving "AA'" (and thus both ...., Ud lly dnd pot.-ntidU,·/t-rtik-J 'UiIlI""" Ihdl bluebird. "",.{'. p""irrI.Il,· all .."·""",, d ...i sion-"", li"l\ """"h.uti-sm tn..l "'lI:u1>tt-!. tht>ir
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406
Chapte, 13
10 EffIgher !hei' hom' off<pring, which ~ why ,hey ........ h-igher probabilrll""'>raUy. bul nol unive"",Uy. adapli,'e rule of thumb may expl"in why b.-ling .dults of v.riou, species devo'" them....' l"... to caring for !he young of ~iaJjz.ed brood p;I1.cilcs. 5uch., ""r1'lin (\I("kot15.nd Cl,,,,l;>irds, th.1 place their '1tIls in th,' nt'5ts of "tll,'r t>irds, r.",nt.l ,ongl;>irds lypically dil;tribu!ner tltdn the young "f the ho,t sp..o..'5. which cn.,bll'5 the !",r.sill' to st:.lrlgruwing """,..,. .,nd get larger than it, cumpt'lit"", in lhe nt"-l. Ilff.u,.., adult brood paraSil'''' a", i'\"""r.lJy lal'l'er bird' than the 'peci,,, they victimize (,.... Figu", 7, p, 120). ttlt'ir ""'bi", ..."'" ","",ome much larg,'r IlI.>n the ho'Is' ""'n young>! lor """')' milli"", "f years ,ince the ""'set "I their ",tel"po;ijiI: para_itic bef;a,'ior, Thll.S, 10 d'e",k this pn.>dietion, w" n...>d to find brood parasile.. thai haw a n.'lali",,!y recent origin. Th., lamilia, cowbird, 01 Ihe Americas .... one such gn'up. wilh the f,"asitic sp''';''-'; having "riginat.-d ""nly"' 3 10 ~ milli"" years ag", wlwnoas"uek",,,, evol,°.-d al l"a"6O milli"" y"ars b..fore I..... p.-..-.I [293J. n...li\'in!,> cowbird sped", bi>lieved to N' dOSeltmgs 10 the ""me sen,," thaI il d,,...; the ne xl .~ to the ancestral f'.lra,ite pa,a,ili"", olhe, binds bi>longing to its ~'n family (Frgure 11) [6&1). n-.e.... datil, if Ihrry ha"e ben in"",· pn.'1d pmf"'l'ly, providd by c,,'. tinK"some '-"'p"rim"nlal b",,> irx;fN,i"9ly 'I""","lizoIlt~ining tht- p~r_"ilh'. tn-~' ing Ih~m ," il they 1'0'''1'otl p.r..,itt'S victimIZe only d v"l)' smdll mino,ity of the ho.t P"l'llliotion, th,,,, ,-v" n . small ri,k (If",..tly n'CIlm''Il1 option impost'5 hre 1'lO3]. As eXpm"
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pl""'l" im e.t only in Ihooir_n ~ ~. lafd)' diI).. ........,.... to ..,....,.J~_ Thit _ on booIow I'holgr'ph by Dougla. ~ k
412
(nap'''' 13
17
Wupon . of . ibllclde. Vt'ry)'O'borns, usually twins. at tilt- entra""" 10a s"",11 lUlr (Figure 17) 1402]. 'The pups al"" fight wh,-" altemptinll t" suckle fn,m tht.-ir mother, T1K' vio\rna· bdw'ffl siblings som,'lime'S n'Sults in lho.- d.....lh of ,)[l(' pup, g,'ncrally bdol'.>\h...- ther I4ffiJ. In som,' other ani"",ls in whim ,iblicide ocrurs, ""rents "f'p"n'T1t1y can ,,00 d" ll.'Si,lthei, P"'!,:e"y'" sihlicidal ""havio'. hid""", «>< Ihis claim ""m
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stud ....." f roIonY1Iy rwsting ~~ c.uro bo....-.bw" Only......... of tho-\(> "f"ri'-"s ...,hibli •....rl~, ",!>lirido',· in ..,h id> "n ol.kr · A" eh"," d.'f'OW'I of" young.... - 8" .chic.. ,n Ihto fiN t.-w day;; of il>. ,;;bIutg >~.tIort w unh.>rVy Iifgin U1CUNt"'IC il ..1,,.,.... nd th..-n ,,""'" d ay;; Lot>-r Loy •••,.;,,",, abk> '0 p"'''ent them fmm immt'diclt'.bl}' "", another ex.mple "f the female e""rcising he, ability I" influet\C(' the altributes of he. "ffsprinll (..... p, 3-f I). Second. as soon as a "' m. le '1I"'t 1.1y' her fi,,;t egg. i"""bah,,,,, "'";i,,•. just .lS is to,.., I", boobit",. Ilt",au"" I or 2 daY" "'1'"rate the laying 0/ """h egg in a th...... egg clulmMirrn,,, ray- off, Und." condilions "f lood scarcily, howeve,. a "->du,tion in the brood al'CllmplislteJ by sibli~ide ... ,.... the pa,,-""ts lhe time and """'%. lholt would otherwise bo> wasted on o/f-
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'f'"1'« ,lli httko, .. no chaftoC1> of fNdUng ad"]"""",,, ....',.,., It ''''~r >i~lings Wh
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~I· I .....Ilhis ,"~i, is to "'"'It' urlNtur.uJv S ) ~~roods of ... ttle "'1':"'"" llllll_ In , _ "'-f"""iment. 'l~ t>nJOnouo;bIo."ds noIl..-..l) ""'ghI ....... and sunn'1'd " wril, l>ut ""'luimJ _food pir 01 chid..s [f!bIl]. n" ttle~ p.> ......ts and otho>rs Iili> Iho>m know lunan.ciuusly) whal ltIl"y a doing wlwn 1twJ.. manipulate tt. """"'- n>nll'nl 01 tfwtr '-"gp and incubo> Iht'll'l in wa~~ thai """"'" ditlu",,,~ in ...... and IightlJlg al>lIil)' """""& lho>ir chio:b So~ling "Ialry and siblicide ""' Uy ""Ip pa".... ~ ddiw. theiTCatt' only 10 "ttsprin!! 'ha! MI'" a good ...lia ot e-\·,..,l.... lly "'Tmdudng w liil" .-nabling tht' pa.." llI l ko.l' their td d d i rJ ,,~ I" ~ mInImum. Although ...a,,-'!1 l>f llii. ""rl "I1,.. . tn."I1'I lhdl ~i .." , hei r ~lJoca lin ot fond " ""' '' ''"'"'' ' "wa rd l' ill"" >I1' off, p rinll " n' "",U y pr,...-li...inl! ;n l"nticid,', , p'...... linK tt.... d...mi,,-, " t tho._ p~....y unh~dy '" "--p,,,dU u.., red rok...mouth lini"ll. ~ gmeraltthing "y.>; ~m..rgd"mn the d food c"",,"i"g_ N" ' tli ng< that received two dfOI" oI l'1'Uow food d ~ aft"" "'" '",a'"",n1. AIt"" saino '" al. [101 2].
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2. When !he cin:um,ldrlt"t.'S a",,;uch thoUlhe ........,Iib "I parental,.", ex,"""" tilet' lather> thai help bnK"/' 0' mi xed parernily gain ko." Imm lheir patcm.>1 ca.... Ihan 0.1" mOlhers, which are us"any gnetic.lly "'lated. '" all lhe "fupring in their brco:>ds 3. Malo fish a", unusual in tbal they' oil .... pm.'ide unip.""".1 ca",. The ""t-bendil ratio of patem.>l c'''' in fi~ m.y bm~ animals 10
lle~.", 010'" li~eiy than "the.. 10 ,un.-iv"10 "'Prod"",.
Discussion Questions I. Gary MIlK.·h.o"ior of this ~ is "'" adapti""? U>aUng kstrel, bo.-havit.'" (1) tho, ..... t· ,w,tching nesllings we.... "'" in poor condilion M"", ""\\'in~ (2) in !ho> new ""'I, th. adoptt'd .......!ling, w~", "'" W .t a h'gher ra',' th.on thcj-' h.od bot"'" prior to !he .w ilch. and (3) !ho> adopt".... did t1r .""k in th1 ct""I"-,i",, mu.,lht> ........ rd>.,,-,; of th" 'tud\' h.o,'~ n'achod '''' the b,,ome 01 II> besl .."olulionary binlogi,ts in tl> w"rld. including IJ.,rwin him",' II, nus CThlf>t.>, f",-'Uses on how altruism and 011>, hoelpful ",-1' can be a""IF.t'd fmm an adapl.,honi,t plpful behavior;n d..tai/. w" hl'St n....d 10 ... "l(i.. ti", rep",",'nt Ih" (rown;ng a(hit'v~rn~nt ol""o!ution, But ju.t a' • cosl-bendil . pprnarh demon'tral"" that pao"'tal ca rl;' is not always adaptive, n ad"aflt:' 117]. lnd ....d , if group Ji~ing Wt'ft' Ih" uni""Th'lly ' upt'l"ior lif,,,,tyl.., we would ""pt'(1 ...ridl 'f't'cl;,inl; cud,· old~d , and f~moli, own 'f"-"Ws 1551. 8051,
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,h"wn Ihdl ani "",I, in gnlUp' d" gain by diluling the ri.k of bing caplul'I'd, or by .potting dangt'r 5OOIt...., or by "'P""lJing their enem ies mort' dfecli"dy (I" 202). In the m,lOmao, a "",{ fish with a w""d,.,.ful Lorin n.u"e(Ab"dtjiI"raMomillil/i,). indi"id",,1 rna".. in ,mall """ling gmup' a,.., f,>tC1 "",1", derive mutu.lantipl'l'd.tor bme other n."",,,, (such as II\,,,mg othe, foragcrs) is an un""",ln..1 is!;uc. Thus, we ;"'1"1' mo ... 10 k',lm aboul lhe pn'rffd ing coI""y of \Ia n~" "cmposed of ~"ing pa i" tha' def.-nd tiny lO.. biol"l':'~I~ luok he lplul ~!w. inr f". Itr.. nl..."l berwfil 01 me 'f"'cio'5 .. . w "",,, Bul WIth """ "'-"""g1Ilb
ry· nrlal\o1OCn, ",1110...,' rho>l muluilli."" is b.""'It_ C, ....;d,.1' Itw roalit>orts 01 "",k-
hom Itwl j"nn I" uu I ri, al maJo>.li,-~ w,th .. prid gt'f'tho.-rs_Why dn 11\0.' di..,d".nl.,~,oJ m"I,.. tolerate Iheir sil".,ti,,,,' l'n>b..bly b..>cau,," they muld d .. "" b..'I1 'I). Tht-d"minont bright-plumagsod ..w.....~ dri' .. oth.-.1 or tnlnTnrt.:l"tt;> plunwfo;" ."" .. v Irom Iop--q ltl' - I£'I1iICJl'ioo.'S ..'ith lII';,>d ohrub",,,,.. 1-1..... tIwn-fon.> abI~ 10 "'9" lor btIgMly ~_
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IinlIse;,-. el _ 1.lo61 ~oph> tour tkan the ident maw, but the ri..k of cud.oldry /or bri,ilhI ..... 1n WitS only IWf as g , as for dull ont'O. "'kick om-d by the dull ..............." .ooor no>tghborsl,\56I, Gi,n'l t t - fin,hr>g!i. whoIt do duO..w... g.>in by ~ng 11'm~ nNI' bn,ilhl males tNt ..... hkly Iorudold tht-rn' B.ca duO oul>ordinalr bunlJnll5 .... py """'" hkdy 10 acquin.-' oocial ma,", than maJoos 011 inll'nnono ........ tNlltwu lIOrilIa"'al""",wl ,Iron>tIN_ . mu .........". Bul w , aboul the nwJorcoalibllm 01 tt.-long·tailN INNIun oIudwd by o..id ~1c1Jonald. in wlUd> only ..... oIIwOOXJf"'"'.b. ... main 10 "'J"'Oduor' In thiS biN. ma .... fonn pai .. and sing loud dU"h O\'O'I'.nd ........ 10 .ttract fftnalrs to a display court 1393. 7821_ VisitinK fftnalrsland on the pair 's display f'rming.n . slonishinKcartw......1d"play (figure 10). Aft.... a ......... ,>I thr ~~, 1-\n.....bou male b« ••, 1pN. ... usu..lh' ~ ,,, .....'" WIth ....... y of It.- s.>mI' 1t'm.II... tNl ropuLo!eilt-d ""'''''kin, .........,; "" thai "'-......... f"I"i1cially ...u..........
rn..n.-.-.
rifKin~ .-.1i..", .-.1 lIy ,oJ,.onct' Itw "'Product",.. of lpfuI individual., An..lhlt· , ..... of thi. ",,l .......u Atric.1n mam.....l d"'l f''''d!\'-' ;n /t'O"P" Fn"" h"'" It' h"",.• _ 1t.>1 will ,top d igI'lnlt loll' ;n...~1s in tl... ...,il and dimb d I..... 0. .. 1t...",IlaUon,hlp Ih.· labo-I ~ , ~rl r n", . 1 . lt ru i.m~ [1152) bo.'.-au",· tht· ht·lpr, P...-h.ops tht' 10,,1.,"'1, IwH' full bo.·l1;.... ~nd I" .:limb. In,,· '" ,>n.-I..., tt, l>cttt.'T "pol injl; on,
~lIlhe ,till·ft
dw.",.,.,
12 A ................li""" on the'" lot_ _!'long ",td.oton. _O<j,aph b)I ~~ J. 000i, hing in ooIy when the animal it ""lped Il'tt1mS the favor. In bands ofbaboon.s, pai... 01 fem"I,',; do I" ke turns in srooming and beinS groom,>d. as pn-dictl'd fIum the n'CipllXal altruism h~-potht",i" 110581Reciprocity is nol particul.lfiy ""mmon. how,-""t>T", perl>aps because a popuI.:IliOl\ romf""S"ughltt> mak
I.,..,.
4 32
Ch.pt ~'
10
The p,ison~ ,'. dil ~mm •. The di"'.l,.m lay. " Both "'>opera"''' > "Bolh defect" > ··Coopct>;," the ,>pti"",l ""'pon...., for s>JS!,,-'C1 A is .Iw.ys to d..fC'Ct.. neve' to "''''I''''.te, Under these circumst.mcs, if sU'P''C1 B maintains !heir joinl inn",,;, then!fore. lliat lI'CiprocaJ CO('P'''!".tiort """"'Id ...." 'er ","~"e How, then. can wrmanently [OS orportuniti,,,, 10 n'pn>duce a, a ,"""ult of helring anoUwr produce 010'"" ,ur· v;,'ing "rr"pring, A[trui,tic actions. if they ,,,,i,t a", an ""1'l'Ci.>lly ,,,,citing puzzle for adapliltkmi", bffau,,", they violale the "ru[e" that traits cannol 'r",.d owr pt'a"xl on lho.' pnwiSduce can pnwide an ind i""'l roul" to the very ",me end. To understand why, w" musl Mum to the concerl of the c""ffide,,1 0/ "'lal,xl",,,,,, lhe p'''bability tha t two individual, both P''''''''''' the ..me ral'\" allele by "ittue 01 inheriting it from a ""'Int mmmm, aoc",I'" (_ p, 55). [ma~i"", lor example, that a pa""'l ha' the genotype am,of /.my', and thai .my' is a rare fenn of lhe gt"''''' in th" .u,,'iv.1 of lho., .id,od off'pring m,m·than mmpo>n"'tes a parmi fo, tM loss of '!J'portu"iti... to pnlduCt' .dditioo.l offsp,ing in lhi! future (""" p. :l'I7). In g,.....,tic terms, pa""''' con gotin via parmtal in" ...Im..t\'>,,'t'rl p"n'rlYI "fft.:ndanl kin [tr>llj. Tht>!t'1m Kin ",Iff/ion is. how"wf, cum.ntly \l.,...] very wid"ly by evolulionary biologist. ",' a 5)lTlI the din:ler by con/using ()l" deterring predators. MoreO\'..,., the pdnss helw""n f'o'rml ~nd o""pring, ',) L'
"""
lh.in lhe indill'C1 fitness g.>ir",d by II>I ",loti""s thai exi511hanks 10 Ih,' ~Itrui,t', ..-tion, 'h, lim", the mean coellicicnl of rr inm,~slnl'; th,' fn"lut'nrv of any distinrtiw aUelt' ._>riat,xl with ii, . Itrui,tic bo.-h""io'. Thntla'Y ho>lpmal they hdped tho.· p",,,,,'\-ling yNr (Jt) oj 27 in R"y""'s .. mpl')'
B......J""
s.c."""'Y
fu'lf'I in tIw fi~ ,_• .on
"'f"""iuno"" lhnr own in tIw ~ :tN•. if ~ 1lUr\ i\... .ond find ...........
Pntn.ary .... If'rtrwr (T.. ble 2). But '" tIw '''''I 10 pri""'f)' twlf"-"'" of O,H h,l unils 0' do""'" f i _ (D.!l-l - OAI • 0.-1-') in llko......-.nd )',,,, offwt b)' .. gilin in ind i""'" f i _ duri"ll!he firsl y....r? To II.... ~","'t tholt Ih..,... mdl"" incn'..... !heir pdf""' ''' n1'n1du(hn' """"""", Ih.i,I, indi ...>lho,·.. And ,,·ilh .. rodfi(inll 01 l.ll•.,j"' t>f 0.5. Bu l in n!her pan.,,1 had d;",i And lhe ,>fh:rhad " ..., .., tlwl !he off?pring 1'.... d",,'" ........ onl> hoolf..oblings (r ~ 0.251. Thr ~""'-. COl'fficiml of ... L1"-'t1rwo6 for """" ho,>lpUoK ~ l>l... ing thooir fut" ... ,lu.ncn of ..-rmduIll, '4'1, 1121].
4 38
Ch.pte'14 Each e~"" of helping ~t the r>d oul, h; in th.' Me~ica" jay and Rorida scrub j.:Iy hove pn,l.1chn 1"",,1, Ih.l mdlch th.- of Ih jIy .... pon M rho< .... t on lhe ~uetiw """c... of rheIr p«..m Ind on m.Ir -.. ~ fit,.,... P_do _ _
- . . , ••,..10ol",»f If' In • • pen......nl.1 ....." tho' lo'llhei' ~per,.nd in unmani~ I.'ed
.1,..,
....." dunng • l·)'e.' ""peri."..." . Aft... Mum......1826j.
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us
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hdp'" untoud"-"d. n,., "'pdu(tiw 'UC«.... of I....."'p"rimrt\Inll':' of lheir <M'TL On IN .........anl ioJand of Aride. IN trolROf'lanlo'd ...~ bred so •• '"' fulh'. "Ad I""" "Ad !Mi. oftsrrin", began 10 fill up "pp"-.pn.olo' bn'o.'.... 1t>f _
t..-
_I0....-........
-------
'l •
11
T_.. . , .....,._ 1he
21
_ _ ..... . . " " ' _ '..'110 ...
bud to wm.ioM' ~ ...... ~ MIN ..... lim
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, , , •" , • , " " ,w, " 'W, ,W ,'w, ,~
-
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....... ~temlonn.
_......, ..,.. in ........ ~ ..." nte IOJ' ..... 1M ntI manipulalion in 1M S~l'; do haw Ih; in tn.: predicWd , adaptive d irction (Fi>;u rt.> 22) 1M3). In ",m~ way. tho; ft,mal~ warb l~rs us lnlormation gathered aroulterrito'Y quality to manipulate meiosi'. Femal", on good krriton{'S .lrl' abl,' to bia' gam l'll' p"'" dncti"" toward a,1. I,omal..,. ha" .. """""tially perfect control Owr the se~ oillieir p"-',o;eny ['1551In some socia.l hymenopl",alchaviur uf all tne otne, m"ml>c", of her group 1229).Or p"'maps u"d." """'" circum,l.",c",. "",h as hillh ri, k " f pata.'ilie inft.,;tatior'_ f,,,,,,,1t,,; that <J1a", "'Pnxluumblcbt't' 10'"1''' wert' manipulaled to ,",'al., ",k'ni... with high an d k,w g 23) [6%1. Or perhaps d"mi""nt f so. they might make the helpers' inclusive fitn
24 Who r@produr;@, ;n ~I"'r wa,p coton ~ 1 In PoIi".. coni
[962].
o
0 .2 iloUlJUCUlK f' bngIdd..,J ""' kin 1Thl1ce tot alt,...;ting on lhei' own, L·nn. ltw g.>ined~' t~"'P''''.lon,: ",'I'd not ht-I';rt'al in ,....J..,. It,,.. a oul-ot> lI;"-'''r AI~ rn-.,;!octJon!; Imnl ",,",,,,,",",n tftto,,") .... ,~ ht...., "'41"" If .ond ..,.,.,.. ,"t"ftl'ttr.!('S 1\1"111. ltw abilit\' of ltw tftto,,-..v 10 .ocrounl for mosl .aspects of !lot b\ ..-pro.i.-.m...... ca~ lnrwlr.. a"!'" unn"l.olftllo ttw quo.,.." " not ~'I't comrlr-totl" undrr'>lt"od. n", ""'"' ~ .... tho;- ....,.;lr-c_ of...-.tain .....-yj ir-.'t< IFIjI;Uft'251, Thl> an.t1Om)' and ~'k,.. "f t t - ca;.W II'lt-'fRbo>r; >how ..._ Sf""CIlIlUatiaol for "'-It......... nne.- Th"". honfo\ M worJ,.,>n ....,'.... b.arb.-d ,"n~ dc-.'KJ'IftlIo catch in tt,., .kin of ",-.M>r.", "",,",iJudi ...• (a,,,.. an' kn"wn a, ..usoci.1 '1",·i,..., I'u""ial in",...1>; "."glll [M.win'. t'y,·, .. nd hI. Ihdto tho> indin'CI hlnPSS ~Wf"'I"''''' "Ir,,'dy llulii ",..J. [M.-
Iw,'"
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~In_ eUst. INCh de>oo)no
25 l ..-W w.-n , - JWrile aotfl.
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44 6
( hap'''' 14
26 Suicidal _ .lfote by a wor~". lift. W""". 1Ion~ bee pl"dipl,~d system of sex dwrmination in this group I4&lJ. The potentially \'~ry dose g~rttic sim ilarity bctw,...n sister bees, anI., and was!" an_ beo...... ~ I.i ~ lNl'" ""f'l"""'~. cIo>otI\. ......"""',indi· ncoct .. kim, - For 1fW sis for .....soc;.li!\' t.... I.I>I,· p,..,.Ji(tinns. Firsl. if a f,·malt. "'rs p"". Sr brolho>rs on aVCfal\" (, _ 0.25). Bob Tn""rs and !lnp" 1-1"", """'I;Ililro that tht.-se bn>tlwr---,;i,h>r inequahtit'S in r should lead to oonflic1 betwC'S male ",producti" nesttIwr ~ NI......w1 in !n"mt'h '*- ~ rt'l.1t...J""". " ...."'" rrwmbe.. oi >OCi.oJ group" """'-'Id .10", bt' .. with c",I.. /",mato"n.onod ..' If.oord in.>TY ""It........,hcinll bo.·tw,·".... 8lh inbl'duction u n """II in ,.•'ry hi"h Cnl:5 of ... 1.01,..I m''''11 /"mily m..m be-rs. In lhost' 'f'C'Cio... of " phi,h in whirl> m"I""',," "Tn"l""" ..".·, ,,.d ly, 100 .."" mple, d..""IlI.,.. ",·t c"",,on lH"", '" Ill,· r ..~Iu~ lur ,i.slef'< i, 1,0. A nu ml>t', '" ~"" , ,,,, I ~rlljd. ha ..e con\" "I):.~j ,''''ll"mk" lIy ~nd bt'ha , 'i"",lly w ilh lho.· ~,> tl - f", min~ thri"" [ ~, ]{Ill'll. 'Jh,;o".. "phid, .,1,,, he in WOlls m..d,' by ~ I""nd n.., km. I.·, .",.1 Iht-y ..I"., M W ..old,,·, C.. 1nU,l.d .......; ond....·,t .I". In .it,It.""" "I tht-i, ,i. """. In ~'p"rirnt"lll!o cond"dilht< had".,.... .. >idiert ,............ ,thou!~. Thr .. >id plk ......... ..., bn\i'>, as lil.dy 10bt' ,,It.Ickd to.' 'l'J'hid!; ... othrT in>«1 pn'd.oItho. ~> ... inJin'ct ""pp"rt In"" tt... finJ'''l'lllwt mn..le >4olln"" on "",n> """wI"I""'--;,.,;.utLS ho........' M. as VllU ""'y "",..II. A 'I......... ..... ill> ....\ ,·, .. 1n",les pn>dll1 .......... hifo\h .."" fficid . hort. ,rabbirog beaks protec' 1~lr more delicate {right).whkh ~,~ po' ''''' i.1 '" repro.duc! when IN'Ufe, Tho ,pee,", w"'" drown at diffe,""t "'. ... by Chri";n. Thaid [10991.
coicJnyma'' '
""'to
I pos· ""'" the haplodiploid melhOO of ..., delermination. 111 evf1')' bil as eu social as honey"""" and papt" wasp". d''Spit''lh~ fact lhal both ma l,," and females a .... d iploid (see Figure 25, right) ,
Tile holulion of Socl.llleh.vlo.
4 51
] 0 "mamma! wifll ca"lK- _ ......on.lYe Iorve _ • _..01 .....,.....,.,....In_ _ _upone
or. few bl_... __ JIIIou>gr""" to, lla'll ... td MencSu
A fi....1 ~ ....mpw Cmsl-stud,t>d 0/ Ih•.".. i. Ih,' bi; ""-l",,king kt>d m"I.... ~t. a hnl", h.li.Inth an unrrilt'od indh id.... of the. ('fIo,fully. then ...>nd,'I'..."...... thai ........ in at lIwi.... tal .it,' It, ho,·lp '>lhoor rt'1~h ..... art' lik~ly 10 st'run.- ""ftiI the "'-1.,"",i.11 ~ft'slylt> in mammals. In ~aL il is ... asler to ofter a lo>ntalive e'plan"lion lor why a sf""cics hils e"olved a parlicular Irall than for why a spt",i,,, ha, ""I c"oked a particula' If.,,!. For e""mplc, "·.,,archcrs ha,'c accounted wn"incingly f'lT the s<x;iallif repruduch,'. success of lhe I>Ipt'r whil. at lhe sam. lim. ,aising the "'Producti... o"lput of aMII>, t r - helpe'" may bo slffile. The«e indi .. iduals I>oosl th";r indusi,·. fi"""" by aiding dCISonelicia')' i. high, "".oci.lily Can evoke .,'.n when the deg of ",Ialedn""" i, not g",at, pr,,,"ldro th.>111>s i, .uch th.>tMlpel'; can improve the production of ",lali""" ma,kedly, and tonnine whether this helpful behavior is rti,,,,?
2. L.t'> say thai in c.lcul.ting tlw inclu.iw litno&> of • maJe in a roalition of lion>, you "",a.ured hi, difl'C! I i _ by multiplying by O,5tho nwnw of off"l'ring p."ducro by the malo, and Ihm added as his indifl'C! fi_tho rutal number "I all off"l'ring pruduced by the ntho. mf'ffiben; of hi, roalition timo>s tho ""'"" ,of lhost> off,pring to II>
4. In """ .....1ant >peele;. two or m",.,. unn>lated fem"Je. may jin frft .Lve [~l. How can it PO)' l jin such .n .... -.;i.tit.." Whal predictK1J1 can you aboul the surviv.1 •• OJhavior, If thr bohaviorof tilduct of natll'al selection, Il-lhd b!u tirlfl in the> und,''''tanding 0/ >0 determininf; whethe, .-vlutiortdry hypotho.'s..,s ~bout humil/\ bl'havior ,an be d.'vi,,-'d and I....tt'd d ..'Spik th~ ,uliural variation;n human beh,"';n' (Figure 1l. We un take the fin;! st"P by analyzing the J'O""ibk adapti"e b.,is ill my generous donation of blood to a blood bank lhe othe-r d.y.
The Adaptationist Approach to Human Behavior
1 Men In
m~ny
pa t1.of New Guinea
haYluud donatiun is immune to .....". luhv"ary anal)"'is anti i> in,,,,ad a kind of "p ure" all1'Ui.s", p''''-lisibl" filncau.se Richard Aio-',and,'t was intTigu,od by the chan""g.. 0/ ....plaining blood donation from an ""'olutionary !",l'Sf"-'CIl\''', h.. kept at il. rerhaps, Mid Ale"""d,'l', lhe donor is "'raid. not by tl,.. "",ipi..nt of hi, blut>d.l>ut by !ht' don",', """'J'day ",-''''pani",,-,. ",l-., mav bt· Imp"-"'''''' by, and wish "' «l()p;,t-neficial aliianu.'S, The Indl....,l ....,iprocity hypolhr'Si.loT blood d,,,,,,,tiOll, ,••,,0,,1ing 10 whjffi th,· d"nur gain.. filn~" In>m oth"" who " ... his g, ..>h>d. lJobbi t~,w and Jc..:llleint." n'ptlt1 that ,tud""" at the Un;"ersity of Michigan a,.,.significantly m",.,. likdy to donal.. 10 lundrai.sing dri,·,>d driv", [7261A serond pR'diction i. that f"",pk! will b..> ....." fd;JthN:o It.... ltnJi..... /11'171. (lbo,·""'~ly . lho.· Lo~1 word on indi"""l """Ipmci~· ha~ no! y.. t t>.....< ..'ri lWO. ~t, ...-.,,'..... """",,,I ......... rcl> indion of 5«~". hunwn ......i<Jtoiok'fly io ~ undn- tho. ....... iabf'U of hulT\olO brIv\"ioraI~ . ...-uluhr\&'" p"'~v . and rl-olul>!5.. 113]. Although tho. ron""' ......y t-larKd)' fadtd. somt' f"l is' ,ot ~ aboul tlM'rl'O' lulionu>' .ppnlokh 10 human bf'h.o\"'" still rlf'ftl1O boo tionio;t arrro.odt 10 """""I t>dwvitlt. Tht tatheor of socio-biol,'II\' i" U\" C.... r1,-s o"",·il\. with.on .,..i"t r....m Gf'org~ C. William s, who_ 't'"n k .-th"tarion «>III N«lural StJt.-t i<m app"'rt'd ,Iy a d....ad .. befn... Wil",,,,'. bI.... k [12.'WI. K""aU lhal il W,l~ Wi ll ~lIns wl\ ind'-"C! his f~ U" w biol-
0."""'......
460
CI,apter 15 gi'ts ,,11hha,'i""t. A' nur Im".wlt>dg.. " f the roJ" of gt."l1 of Ct'1"Iain human chilracterislics withoulany inf"nnahon on the g.......lic or devel· uplTleiobiology have poinll'd out Ihat, althoul'\h hum.ns d",i", many things, the wish 10 maxiIniz,' our inclusi"e hint"'" is nol whal muhval'" our behavior [9B6]. II you had askl'd Pic....." why htoca"-,,, w.. POSSt'SS physiological merain mod""" thai c{lfltn,lhl olhe'r g,'Il{,'r"Uy ad..ptive ..l>ilitics, Soncthcrn," 'lOciol>ioIogisl mighl 'hlliry to p",d"", .. I""tabl~ hyptllh""is 0" ""w iICct'Ftanct' of celibmgic..l hypol""",-" ..bout the celibale prieslhood were inrorn..-t. eff..,-ti,·" ""''' "'o"ld lell u, st', and we "'ould pn-.l>"hly le.m some interesting thing. along til'eit>pm.'nl of ('lyand",u" p',I;·lO'''ous, and monog.,mous ""i,'li,'S; "ultu"... in ",hich fe"",l"" make impt.'rt.",t p f'olll off under unf.1\-orabIr <Xnh""",,, ""'Y dn..... 1n oIip.. ~ ifili) .... , . . . . . . "",",'s nest. or In boo...", " hrIpof oIllhr . - in """ n.u.aI IdN Ih.ttIhr brftding p.oit I!'orn' ' - p.o_ 1o ..1>orn W is ~. """'-d 1/ r.lhtT ..... ~ Ihrir irdlS>", rm-. St_....~· boO. f;isfi hil,'", ~ tNllhr ll\M\~' and ""rifd ron,"norwl..,..~Ih.ol und..rlio:-
-"""""1""" "'''=.
_
n
i
~
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_
I......"'''J'IionI ro,..'......
t
,
2 So" .... , _ " ' I t _ _
H ....._ _
I~...'tit' ·IF:':lI IH.Ipor.,
tlw.- ''l'''''''
tklpo _
I
Loy.
OM"'- ...... [11.1p« .....
ro'''''' opIioo
C""",,",. _lilt 6e<Woru .... . . -
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by IN")' _ _ frn~ b.. _ . ,_I0 _01 [3661.
~""""'.~!i...
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£........... ai,
464
ChapIN 15 "uI beh.>\'ior do lo r uS wh.lllht' young n·mal., ~rel'~ wndilio.",l str"k1\Y dOl'S for ht"r. ""mely. tho."}. p"lVid~ II> with ali",ilrJ. not OPt on the arbitrary cuhu'" hypot[..,si, while supporting an indi""t fitnes.s hypothesis for this lonn 01 hUl""n allnlism. l'\ev"rtheless, a minorily of ad"pt"rs in Oc·..."'ia do tak~ in the children 0/ strangers. their gm to .",plain fmm a ",,,,inbiological pcrspectiv~? No . Si lk sugg''''ts that ,m.1I lamilies in s"m~ agricullural cultu"" mil\ht bt'nrad,>pliild
..-.d ,
.......... fi_. ,*"",. """ m.oinWnrd
in human J',..........tfrd h, I,d... lot ~.ohooll*"""Oto.... ~ protilu," for li:'-""""" otf>pring. Anoll..- ~,.,If"m m;" hyJ"'lho--;' lhM ado.'J"b m.·thinK th.t .Im""t .,.., . ,>tw""n malt'S and I"mal...s CT\.·,lt., sd""tion p"""on: on both ""X'-"', leadinf: to the rot'c'olulion of the';r n"f"-'ChH' "1'nld",'li,l' tactics, You c.mnol undcrstand what mal,-," of a 'p !Ilt'i. hint">.... Sill(\' human males ha"" !he pote'11tial to pro"idc matcrial N'11dit, 1 c~pcct •.,j to have ....·olc·ed cnunlt'''''''''''ure;; to reduce the' ';,k. Thus. an ""olu!i"nary c'il'w of human ryroducti"" 1>ppUt.. _ .
l AJ -'- ~ "' IIw _ ""' _
01_ P"P"" a good iro«lmr or _
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"""'_looly oK~ 10 ~ p.>11nt>tll ",lJy. and so do ",omen fRlm an>uno.t tilt' ",,,rid 1111.11_M" """ ..".. "',........... .adn'1'l .. inlt fo, p.>rtne1'S in rww'f""f'""" ..... fa. """" likdy than ""'" 10 'I""t'ity 'h.>t'ho..,...re Ieo:_ d.u ha wei oil ..... not dI>pend.....t ,... . ponrwr ·, should ~ mud< ""~on ....... Nm'"It!"of ~ ,............ Itl-l'l. 1m) Anolht'r ..., ' to t>- tho;- ~ of 1N,,-n.I~frmak-s ~ to ..... """""",,I ads I ... IcuIa tho;- . m.ari.et " ........ 01 mm of dilkrent .. ges, which ... n br dt..... by d"'llling dW' number ci indi,-iduab "",...-wng ... porticuiaor.ge dao8 f"'rtnt'r in Ihrir ad,-...n""""",,,,~· tho;- numbrr of indl\'iduals in lh.1t .1\" d '1>0..... .ad....rn'duCliw suCO'SS, lhen We might ' '''p"clthos,,' P"-''''''-'rl('"' In be Jifferenl when womc", 0"-' o\'ulahnl': as oppc.... .,j wht'll they a"" inferlile . Copulating oulside Ihc' fe,tik p haSt' "I the m~,,-,trual cyd~ rotltribUIkiand Dunb¥ [8911.
'1If!i,
The Evolution of Human Behavio,
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F"," a~ mate preft>r""ce. change duri"ll the men" ' ual cycle. Women w!lo are no! "" birth c"",,'" pill. are more likely to find the 00"" of ih'y uI nl:'-'" in tOOr t"l"5f""'S" to m",,'s fees, the reaction "I V>'d~' 00"''' also' <wngl" OH.,. the m~nstru.ll cycle. Du ring the "" ulat"'y phd.", " I th e cycle, ",,,men prele r the oJ "" of men ",ith symmetrical bod;"", a point eslablished by measuring !he body symmetry " f a ...m1'1.., ,>I ""'" and tho"'a,kinl: "'"m~n to "val",, ~ the ,d.lh"e .1ltraeliv"""", of the ,"-""",IS d;n¢ng ttl ",hite T...hirts tha I the mnl had worn while sleeping (FiKUTC B) 14161, an..... again, il body symmetry is a pn'f"'rt}' of healthy""'" ", ith " gtl<Jd ~en,.,." (>c\" p. HltI), then women's p ....f "rcnccs may CauSt' U""m 10 see k oul "'x",,1 pal'tnt-r>l "f hil';h I'; ,,,,,·tic quality durinl'; the "'''Y lime ",ho", they .1rc mOSI likl}' to become pn-gn.ont. jI,j ,lling prcfl'Tl.'JlCr, Are ",omen af "'" hight"SIIl f"mily inc"m" is no' positively ",Iakd 10 the numbt'r of child"", produced (Fi!!;u,"" 10). lnde society in the 1Sth fnd 16th ce om,iM "" oll""ing Numbo, Mean number of nwn of ofhPfing
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Number 01 men
Mean number 01 oIhpring
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pointt.-d nul tlwl l..... di ",ORnI'd bt>!,..". .., "t'""jochw success may bo.' tho.' prodlJ(1 o( (ert.>i" {'1,,,luh,,,,,,rily no".'1 "'Mun'S nr m"d.'m 5OCilI
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...... In"''''" , "'f"\UIIl-m'" """- '" ~ fi .and I'on>mo;.t. ""'..a<Xl'!tIJ" tht-~of fntiIO' "'onwn. and tu.. fim. . Iht-rrit "an ""'" with
Itw numlot.'f'-.I ft.nmtj ............... i!h who:.... '-" ""p.. I.0 .,. ..nd tht- fn..qut-ncy ...i!h " 'hoch .I,..... "'_n.. poin' is th.ol ""......, .. nd R' n"'",,f""dt'd to "",,... Ih.· ""' ,nl,''''''' In I.o.l}:.. n.. mlot"... "I I"rlil~ cop.. l.. tory p..nnt>"" Iot.· uu..• lho.· h _ PO~'.,ffs for roln;.. m~ ditfo.,. f" r lho.· I..." ...·u.... h '~lJlu'.r)' f"y.........~ ........ ~ .... pnu;........t th.ll ""'" ""'->uld, I,", .." ..... • ~, , " • k"',.... Ih",.h"Jd It". "",.....1 ""Ii,'il~ th.on t'Spt'Cidlly if lhO')' ",," ..,u,,· aHu"ti,·~ ['J 1,",l..s" in ... hjl;u,,' 51. ludjl;in" Imm Ih.. i,
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d."""_ .. fa mily in - . . in .....hal m...... in W,,,t.-m cui· tun' «>",id,', physi,ally aUractive, we find that pA'fo>m!d ft..mal~ tr.ill. indud~ fuJI lips, 'mall "'''"'''. a waist r:lTCUml..n'ft'" thai i' substantially smarr..r lh.tn hip circum!.."''''... (the hourgla.s figu,,-,j [l0f.6], and an inl"nnediaw w..iR!t1 ralher than ,.trcmp thi"""", or obesity 1114111. Th·N prior k> moo...m birth ronlrol and u.., pul>Ii1 onI)' is maw ..............""' ..r. mud> _(t.'mll"OOrl than dw Jo.rtW.. ,Ving known this person for ""riod . ranwng from 1 hour 105 yea .... ttw difkn~ bt,tw"", m'.... and wom~n w~", .11....' dramatir (figun' 12B)," Aflt'T knowing a potential mate for ju,t I hour, ""'" a .... slightly di.,.indind to consider having ""'", but u.... disindi""lion ;,. not st"Iflg. For most women. "'" after just 1 hour i.s a "irtual impossil>ility" [l!!1ll· fu' klWl". st.lndard.s pi ma"",. al lea'l w",-." il com", to casual S
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ThfllUgh(lUt human hislory, lhe wiv... ul 'Tlimy m.... hav~ had 1 (O<mlt.-nd with. tIw possibility nyt Ihrial gOband to "'-'ss, and vire """"' One result 0/ this hlnt>ss conflict b,ual jmloo'y should d iff..r betvo.'"",,, Ih....'x .... 'lewrding 10 " ...,lu!i(mary psychologisl" t>,' wh..... husband """''''' an addilional m,lt" (in a polygynus ,,>r in fa"or of a "'.... partner usually loso>s ",-'me or aU of h"r acCl>SS ttl ho,r husband'. w..alth, and Ihus th" m"allS to .upport h,>n;!f and f'.t" child"'n. The",fo"" a woman's "",,,,,I jealou.y. "'" tm- argumenl g" "s, o/l"uld be focused on tIw ros,i!>l" I"" of an atlt... ti\'~ pmvid.... and he lpmal" that occu ... wht... a man 1>wnmally ca", fM offspring iathered by that oIhr than th~ lo.s of and ~moli"",,1 commitm"nt [285]. If this vi""" i' ~orl\'Ct. th,,,, if m"" and ""om~n we", asked to imaginl"ps a d",p frit'Odsh ip wi th anolh..r individual and On notion that 'uch culm"". actually ~,iSl app"ars to hac'" bern a (wistful') misinlt""""" Ialion on the p..rt 01 out,id" obsc>f\-'ers . In all cultures studied to date, adul"'')' committed by a woman. or ,,,,.,... suspicio" or il. is consid"red an oif"""" against her husb,'nd and ofh>o pn:cipitates violenc.. [28Jj . A cuckoldl'and may legally murd'" his .....if" or h~r lover in many socieli... [2H5] 11>0> possibili!)' that a woman may copulate .....ilh more than one man has also app"-O'fltly shaped ct'Il.iin aspt'cls "f male anahl£IlY and phy.iology, which """m d''S i",,'-d I" help m"" engage in sf"'rm com"",ilion fJ074 ). Human testes, for ....,mple, .......igh mon>lh.ln thClSt!>t-r mal.. during the ",me ,,,,,,lat,,1)' po>ri is away from hi.. f'o'rtnt'r fur much of tht.> limo;, lht- pn'lhahilily of spo-nn competition ioc ",ases (Pif'''''' 15), favoring an added inY....!"",nl in spenn 15\11. IWhin a.lu.·r and Mark Ilelli, colk..-!t"d data fn'm ""'p,,r.lliv~ co"ples who 5"1'· p liro ..j""u]aleo; captured in "undom, for 'p."m
ornln.. """"Id ,oboob.,~,.......rtin Oa.Iy ~ ltwol mm who tw,,~ bon> .w.y from lhlr r-rtnrs """y twv~ hood \CUII 'n '....« II"n' "'Im "tht-r W<Jft'W'J\, wl\rll thO' mUr psyd>t- migh t inlnpn"t f"lImlJ.lI Of'P'Jrtunit>e;, r"" .......-po" mpuLo_, h ..... Ioolmg.M l.ltgE' nurnl>t-n 04 ....,...." rrugh l do Iht tn 10 ,"" """""""{Bottom) ~ . molt I _I.., Iotc... _ I _ I 10 b,- """'*'910 ..... grflPlng ...., , ~.-ing ""' _ . _ !'-1n....,"'9 "" ~~
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Photoqo'."". b,-,.... 1\1I110t1\l those individual. to copulaI hint»/; 01 SOIlldurt1, , 1acti"I~ indudm,; ...........m.tin. As we ha .. ~ n,>tt. R...,,,,,,,,tit-rthat an individual's impact 00 til "",,xt i:""'-""ation's 1\'-"'" pool is d_nnlned roll! by the number." babies y will suni..... 1tl "'1"''' d""", then parenll; that nedun- 'l< end their in\'t'Slmiir da u ~n-n; identically ",hffi it IJ. mate. Thr atl1OlJ ntg i""" to a getIelk oIfsprir>g ilving with a ~. male wa. u>eel a•• " .... dard ogain" whoch ,he Ol~ tlon ation. we« ""'" lUred. Alter Ande-toon et ai,(301,
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t>nd~·. family (Fi)\u n' 2.11; in "'M gn",p". f"mily "f , ho.. bnd~...nd' dau""",," oH to malT)' ",ith. 'f"'ci.>I dooation- Iht- d"",'1"-to he r .......... hu.t>and " r his jamil~'_ U I>tidt_lth 01" dowr f'I\."" t>o ..'...... puM\' arbitrary tr~;tio......_tho- ;II(lj. <WntoI J""ldOCt!o of cuJlUrai Utl< then w.. would J""' J"ft'dict ~ bndfoo'Mlth or oo..TV """'-'Id tor tho0.""""'" adIuraI pnr1l(it ..-..kiwidg"mv umMJ l'uly~y"y Genca uS in just 31"-""-""'1 of tht.... "->O..Iio,,. Brid,'w~allh p"ym.,,,ts ,,,e found p"'hcuJ.,riy fm.:ju,·ntly in poly!,:}'ftOu, cullu"-'S. occurring in mu,,· Ih.:in Ill) p.,remt of Ihr"" suci'-"i 2), Wht'n .om~ ""'.... monopolize ",,'eral fmal, j12~1- n...... son' can pnxluce "",ny more grandchildn'fl for the dccl'a>d pa""'l than a dau~I"', who", ",pnxluctiv,· SlICC'"", Can ,'Xcwd titduc.. and nurt""" John Harl"ng found Ih.. pH,,]i,·ted ",rrd.tion hetw,,,'n tho> practice oj poly!,:yny in a sodety and lhe ,tcCur"'r": .. of inh,·,il.nc~ nJll'S Ih.,t I,"'or son5 ("-,,, T.bl" 2) 14'15). Guy Cowli"h". .nd Kulh Mac~ ronlirm,'d Ilt.lt IhL~ p"ltem was ",al afk..controlling ro, the nr.",ind.".",d..""", 01Cllllt'n:s---Ih1 is. aft,'r d,'ahng wilh the .tdtislical prot>l~m 01 how to 1"",1info"""li"n In"" ..."'..rol Cllltu....'S lho,t m,'y IM"e inherit"" similar practi= as a ["('Sull of sharinl\ a "-",,nl mmm"n Cllllut. lh mono!':amy 1248J. Even in supl"""'ily mon"!,:3m"", Wr..h'm >do 11.>,-,- 'lilly ....."8odo dau,¢llt't has .. lo\.",.j """""" ot marrying. mt"mM of • higl>l'r talu~ Irit>. """'" J" group';>nd ..' in ~h..,1 ...~'. A•• mult of !he S"".... -... ut ~ for diluKh....,. Ihon I"r "'_, !he ,,, num....... of offi,pring of • Mu~ doushll.-r .......r1). 4. ..no..·~ d 1\'1:1 h _ "'onI)' .ah>uI J ThD,rwqu.ohty bv"", I.m, l.... n· '"''"' d.uShlt"~ I.... n ......, . n "",In....., I.... t IS . ct",·n"d It>rough p DW'-"'>!rneftt '" YOWl(tKIn. Ihon in young ~.,.. nu" C'a!oO' """""". iII.-thr f"""t IN! human bo>N>..... .. .ad.opt>\ ety fIe>.ilW. ~ .rt>itrarih·OO' h ' • ...-wbIr. ",............ P'~ ~ .infini . . conb'rll fW""tol ~ Io_.onl u.-.-.. ~ o.g. tt......, ","""",j ,. - pennil pocfIll!I ... I.n ~",.,... on;'\J~.and d.augl:>trro ~ utho:n. ..-hiIr """""r..tting u.. 1trNlmrrIl u nd ..... ~t'/l others- ~ pf.... c"'-n k"nd~ ro ............. p"' 1.11 h~ unJ ..... 10.",..1roodi",,",,- The ,1,"'",..:",~""" thr ....uWt.... -fd\'tlling MukogpJo.and tho_ """n,' """-ting OJ/lu"'" in .. Itich ""'" n......" ·.. rn-hormlidlln'>ltlTlt'llt .on' ........1)' ~ genm in a variabk> social em~rorun",,1. Among the M ukogodo and mosl olher Irihal groups. ml." pay a price 10 acquire a hride, Why do a f~w e" nITa ')' rultu"", ,",,,,,linn paym; thi>1help their daughter 'buy" the ri..,bl ki" d of rna" l!his rl11Jy wife and her ,hildren, T" the "xl",,1 tha t w"alth and high slalu, tr "nsl,'te inlo Tl"roducti"e .l1CCt'SS, a woman's parent' may gain hy competing wilh the par.mls of iht>r familil"S for an "alpha " hu.sbond, even if Ihi' ""lui"" thallht'y offur a mdt~ria l indu(\'m""t I I~ right mal~ or 10 hi. family, Sit'""" Gaulin and Jame. Boster found that d ow ry payn'''''I' occur in sub,t,mliillly 1..... lhan 0.5 pe"'''''1 of tl.., nonslratified socielil"S, when'as q pe",enl of Ih ,· slra tified ,otieli..... and 60 f';«werits thai will be used 10 wn"",n. r~tru,r lhan allevia te, th social and military eri""" lhat characlcrize modem life. But whatever our wishl"S, lhe lacl that we a.... a" ""olved dnimal speci"" is not goi"lllo cba nge. a"d "" w~ might"" well und~l'Stand the signific~nce of this facl. if only 10 giv'e ou"",lv... in~ight into whall'ogO me..,,1 when he dedared, "We have met lht' """my and it is us."
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Summary 1. Hu""'" beings a.... an e"ol,'oo ani"",1 .peei.,.. Hum.." sociobiology, a field "I 'tudy that includ... evolulionary psychology and evolutiona ry dnthn>poJ_ OIly. employs naturdl ",I''th""""~,,. desi~ t" explain, not ju,lify, Ouf bo.>hav;or. T...'ing tht'SC hypotheses can 1«'11' us understand why we ha"c psyd",lngical mccMni,m, tM I "">Ii,'at... us to behave in certain way•. 3, Unhk arbitrary cult u", throry, which pn'P''''''' that hu man beMvior is lhe arb itrary p",dut! of cultural traditions cun' traint'd only by Iii limits 0/ our imaginalio", sociobiological th.,,,ry vicws human beha"ior as lhe p",ducl 0/ ""nd ' lional.trategi"" invol\'in g limitoo oplions that tl'nd to incn>aw, ratht" tM" d.",,,,a,,,. the fitr>l"SS 0/ indi,·idual•.
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lJ tj"'~ .l iHHH IflfJt~ummm m~mUf iFUll,H f !"::~ Wit !il ,". " ~, !:~'. "'j:'-',"r §'~~,r.il 'J!~"~~Jg~t-
}-, " ~g. 1,,5 inWd men h.>vethe ..me probability of fertihzing dJ\ '-'AA pt'f ropuJation with their w ives as rapist>< do when fvr\:;ng coS'u ldtion on a victim [391 . In the past the prob.lhility thaI dJ\ offspring oj a married man would .un-;ve 10 "'I',,>dlX't' was almc,,1 'lId 0",,,,, Jon.... [SOlJ]. Most 0/ the cr-ic rape'" on the t"\',"utionory d""l~ 0/ human bo.-M,, ior can [.., found, dklllg with upd>"".nd rnli<ju ..... in H"man Nat""'_ edited by Laura Iletzig oroJ. Modem accounts of an "",~"'i"",,ry dppn",,-n tn hwnan be-fl.,,;"'- include books by Rkhard Alexander [18, 19J, Martin Daly dnd Md'!!O Wdson [282, 2ll-IJ, and Rol>o.'1I Wright [12(7). wh".....ccounl of t"\'"luti""a')' psychol"ID' is ex""mely ",ad.ble, The ""olut;"n ,>/ hUITldn ".,,,"11 bmo.'igy r...,. b "';mil.o. ~ P'ft'"U ,
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hma~ prrfrtmcr hyporhnis An "'pLonati<W> /0' th.f"nnalion of k-b ba>ed on kmale ~ fur ITI.II · mil with 1TI.Ik'5 ttribu"... can be rorn~tN w ith lI..- of the od>oef ml ..'. of .. Jt1"UpF#mIityin~r An il"i'.W lilod r"'n.~, ..,,hring ~ NI work on briwlf oi th."'f""dUC!l'''' II. ",b... of tIw SOcCU'
IdeClI fr ee distribution The dislributi,m of nonlt'mIMial individ""l, in spa,e wh.'n th('y are fn't' to make deei,io"s thai n1a ~imi~e thl'ir individual lil",-,,"s. lIIegitimClte recr iver An indi"idualtha t u""" informali,m gain...-l from th.. signals of another 10adv.""e its own hln.- al a c"slto the ,ignal..,.. IllegitimClte signale r An indi"idu"lth,,1 prodU
Monogomy A m.,ting 'ysh'm in whidl one ma l" m,ltl'S with "nc femal,' in a b"...odin); ",a",,,,, In f"ma le ""fo,e.oJ m"ngamy, m"I,-.,..re unabl" to mat" wilh more Ih.ln '''''' f"n,ale """auS lo.",,",, Of1lh., gains in mat"rial benfils Ihat eh,."y individuals """in.
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Mutuolilm A mulually bqu"ntly ""rformed if il is ,,·ward.od.
Operational se. ,atio Th" ,..tio of Il'Ccpliw males to ""-"'pti.... lcm,'l"" d"rin~. "i ...·" f'l'riod. Optimal foraging theory An ",pla""tion for lh f,....-d· ing d."i.ion, m,,,k by animals b!i and fcmal...,; thai prefer Ih~m, Se1(ual selection A form of ""tural selection lhal : role feYer$ol n.... OCCUrre""" of compt1ition among femal .... lor aCClt- in p''''.... " ..... rt.in CUt-"> or s,tuation._
Evolutionarily stoblor st,ott'9y That"'" 0/ ru"-'" of beha~'ior that wl>t-n.d,'Pl
