THE NEW PANORAMA OF ANIMAL EVOLUTION Proceedings XVIII International Congress of Zoology

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THE NEW PANORAMA OF ANIMAL EVOLUTION

Proceedings XVIII International Congress of Zoology XVIIIème Congrès International de Zoologie

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THE NEW PANORAMA OF

ANIMAL EVOLUTION Proceedings XVIII International Congress of Zoology XVIIIème Congrès International de Zoologie Organized by the Hellenic Zoological Society Athens, Greece 28.8.–2.9.2000 Edited by A. Legakis, S. Sfenthourakis, R. Polymeni & M. Thessalou-Legaki

ISBN 954-642-164-2

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Opening Remarks

THE NEW PANORAMA OF ANIMAL EVOLUTION Proceedings XVIII International Congress of Zoology XVIIIème Congrés International de Zoologie Edited by A. Legakis, S. Sfenthourakis, R. Polymeni & M. Thessalou-Legaki

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The new panorama of animal evolution

This book is published with the support of UNESCO

Opening Remarks

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THE NEW PANORAMA OF ANIMAL EVOLUTION Proceedings XVIII International Congress of Zoology XVIIIème Congrés International de Zoologie Organized by the Hellenic Zoological Society and held at the National and Kapodistrian University of Athens, Greece, from the 28th of August to the 2nd of September 2000

Edited by A. Legakis, S. Sfenthourakis, R. Polymeni & M. Thessalou-Legaki

Sofia-Moscow 2003

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ORGANIZING COMMITTEE Francis Dov Por – Chairman (Israel) Rosa Polymeni – Secretary (Greece) Anastasios Legakis – Treasurer (Greece) Spyros Sfenthourakis (Greece) Maria Thessalou-Legaki (Greece) Chariton Chintiroglou (Greece) Maria Lazaridou (Greece) Drosos Koutsoumbas (Greece) Basil Chondropoulos (Greece) Stella Fraguedakis-Tsolis (Greece) INTERNATIONAL INITIATIVE COMMITTEE Francis Dov Por (Israel) Bruno Battaglia (Italy) Daniel R. Brooks (Canada) Edwin L. Cooper (USA) Vassili Kiortsis (Greece) Claude Levi (France) Paulo Nogueira Neto (Brasil) Stuart G. Poss (USA) Song Daxiang (China) Maher Houssain Khalifa (Egypt) PROCEEDINGS EDITORIAL COMMITTEE Anastasios Legakis (Greece) Spyros Sfenthourakis (Greece) Rosa Polymeni (Greece) Maria Thessalou-Legaki (Greece)

First published 2003 ISBN 954-642-164-2 © PENSOFT Publishers All rights reserved. No part of this publication may be reproduced, stored in a retrieval system or transmitted in any form by any means, electronic, mechanical, photocopying, recording or otherwise, without the prior written permission of the copyright owner. Pensoft Publishers, Acad. G. Bonchev Str., Bl.6, 1113 Sofia, Bulgaria Fax: +359-2-70-45-08, e-mail: [email protected], www.pensoft.net Printed in Bulgaria, February 2003

Opening Remarks

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Contents Preface of the Editorial Committee .................................................................................... xi Chairman’s opening remarks .............................................................................................. xii Secretary’s opening remarks ............................................................................................... xv Invited lectures PIANKA E.R. A General Review of Zoological Trends During the 20th Century ......... 3 WILEY E.O. On Species and Speciation .............................................................................. 15 BUCKERIDGE J.St.J.S. Aristotle: Descriptor Animalium Princeps! ............................... 19 POR F.D. The Persistent Progression: a New View on Animal Evolution ..................... 27 The new paleontological panorama BERGSTRÖM J. Introduction: The new paleontological panorama ............................... 43 AHLBERG P.E. Fossils, developmental patterning and the origin of tetrapods .......... 45 CURRIE P.J. Feathered dinosaurs and the origin of birds ................................................ 55 FORTELIUS M. Evolution of Dental Capability in Western Eurasian Large Mammal Plant-Eaters 22-2 Million Years Ago: A Case for Environmental Forcing Mediated by Biotic Processes ................................................................................................................... 61 WALOSZEK D. Cambrian ‘Orsten’-type preserved Arthropods and the Phylogeny of Crustacea ............................................................................................................................. 69 BERGSTRÖM J. & HOU Xianguang. Cambrian arthropods: a lesson in convergent evolution .................................................................................................................................... 89 Molecular macroevolution MÜLLER W.E.G., MÜLLER I.M. The urmetazoa: Molecular biological studies with living fossils - Porifera ........................................................................................................... 99 The integrative approach in zoological evolution NYLIN S. Evolutionary dynamics of host plant range in the butterfly tribe Nymphalini (Insecta, Lepidoptera, Nymphalidae) ........................................................................... 107 Comparative Immunology of the animal kingdom COOPER E.L. Comparative Immunology of the Animal Kingdom ............................. 117 STOTZ H.U., AUGUSTIN R., KHALTURIN K., KUZNETSOV S., RINKEVICH B., SCHRÖDER J. & BOSCH T.C.G. Novel approaches for the analysis of immune reactions in Tunicate and Cnidarian model organisms ..................................................... 127

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KAUSCHKE E. & MOHRIG W. Does Functional Similarity of Certain Innate Immune Mechanisms of Invertebrates and Vertebrates Point to their Phylogenetic Relation? ............................................................................................................................................. 133 DE EGUILEOR M., GRIMALDI A., TETTAMANTI G., VALVASSORI R. & COOPER E.L. State of the art for the immune system in leeches ...................................................... 139 SALZET M., TASIEMSKI A., LEFEBVRE C. & COOPER E. Comparison of Molecular Neuroimmune Processes Between Leeches and Human .......................................... 147 PESTARINO M. Bidirectional communication between the immune and neuroendocrine systems: an evolutionary perspective ................................................................. 159 PARRINELLO N., CAMMARATA M., ARIZZA V., VAZZANA M. & COOPER E.L. How do cells of the invertebrate immune systems kill other cells? .................................. 167 ROCH P., MITTA G., VANDENBULCKE F., SALZET M., AUMELAS A., YANG Y.-S., CHAVNIEU A. & CALAS B. Originality of the Mytilus (Bivalve Mollusc) antibacterial peptides: structurally related to Insects but involved as in Mammals ............... 177 Evolution as reflected in embryonic development SHANKLAND M. Evolution of body axis segmentation in the bilaterian radiation ...... ............................................................................................................................................. 187 The role of parasitism in animal evolution MØLLER A.P. Behavioural, genetic and evolutionary interactions between cuckoos and their hosts .......................................................................................................................... 199 POULIN R. Phenotypic Manipulation and Parasite-Mediated Host Evolution ........ 205 MORAND S. Parasites and the evolution of host life history traits ............................. 213 CÔTÉ I.M. Parasites and the evolution of cleaning symbioses among fish ................ 219 COMBES C. Host behaviour: the first line of defense .................................................... 227 HUGOT J.P. TreeMap: an algorithm to maximize the number of codivergences when reconstructing the history of an associate and its host .............................................. 235 The Protozoa-Metazoa boundary SHIELDS G. & FOISSNER W. Diverse perspectives on the Protozoan – Metazoan transition ................................................................................................................................... 243 RIEGER R. The phenotypic transition from uni- to multicellular animals ................. 247 BRASIER M. From Famine to Feast: a context for the protozoan-metazoan transition .. ............................................................................................................................................. 259 DEWEL, R.A., DEWEL W.C. & MCKINNEY F.K. Origin and Diversification of the Metazoa: Superorganisms among the Ediacarans ............................................................... 269 HACKSTEIN J. The protozoan-metazoan boundary: a molecular biologist’s view ........ ............................................................................................................................................. 277

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BENGTSON S. Tracing metazoan roots in the fossil record .......................................... 289 Archaeozoology. Human-animal interactions as a tool for present and future WILKENS B. & DELUSSU F. Wild and domestic mammals in holocenic Sardinia ......... ............................................................................................................................................. 303 MARCINIAK A. People and animals in the early Neolithic in Central Europe. New approach to animal bones assemblages from farming settlements ......................... 309 Benchmark events and key figures in 20th century Zoology WINSTON J.E. Libbie Hyman and Invertebrate Zoology in the 20th Century ........... 321 BURKHARDT R.W. Konrad Lorenz, Niko Tinbergen, and the founding of ethology as a scientific discipline .......................................................................................................... 329 JAX K. From scientific natural history to ecosystem research: changing roles of the animal in the history of animal ecology ............................................................................. 337 DELSOL M., NOIROT C., GENERMONT J. & D’HONDT J.-L. Hommage à Pierre-Paul Grassé ................................................................................................................................. 345 SMOCOVITIS V.B. The Invisible Subject: Zoology and the Evolutionary Synthesis . 351 SCHRAM F.R. Our evolving understanding of biodiversity through history and its impact on the recognition of higher taxa of Metazoa ..................................................... 359 SCHMITT M. Willi Hennig and the Rise of Cladistics ................................................... 369 Diversity, endemism and conservation priorities in Madagascar LOURENÇO W.R. Diversity, Endemism and Conservation Priorities in Madagascar ... ............................................................................................................................................. 383 LOURENÇO W.R. The remarkable levels of diversity and endemicity in the scorpion fauna of Madagascar ....................................................................................................... 385 GANZHORN J.U., GOODMAN S.M., RAMANAMANJATO J.-B., RAKOTONDRAVONY D. & RAKOTOSAMIMANANA B. Biogeographic relations and life history characteristics of vertebrate communities in littoral forests of Madagascar .......... 393 ANDREONE F. The amphibians and reptiles of Madagascar: diversity, threats and conservation perspectives ..................................................................................................... 403 THALMANN U. An integrative approach to the study of diversity and regional endemism in lemurs (Primates, Mammalia) and their conservation ............................... 409 Comparative biology of sperm storage in vertebrates HAMLETT W.C., GREVEN H. & SCHINDLER J. Sperm Storage in the Class Chondrichthyes & Class Osteichthyes ............................................................................................ 421 SEVER D.M., RANIA L.C. & BRIZZI R. Sperm Storage in the Class Amphibia ........ 431

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SEVER D.M. & HAMLETT W.C. Sperm Storage in the Class Reptilia ........................ 439 BAKST M.R. Oviducal Sperm Storage in Turkeys (Meleagris Gallopavo): The Infundibulum as a secondary Sperm Storage Site, or is it? ......................................................... 447 SUAREZ S.S. Sperm Storage in the Class Mammalia .................................................... 451 Integrative approaches to phylogenetic relationships of arthropods SCHMIDT-RHAESA A. Integrative approaches to phylogenetic relationships of arthropods: Introduction to the Symposium .......................................................................... 461 KRISTENSEN R.M. Comparative Morphology: Do the ultrastructural investigations of Loricifera and Tardigrada support the clade Ecdysozoa? ......................................... 467 BUDD G.E. Arthropods as ecdysozoans: the fossil evidence ........................................ 479 SCHOLTZ G. Is the taxon Articulata obsolete? Arguments in favour of a close relationship between annelids and arthropods ........................................................................ 489 GAREY J.R. Ecdysozoa: the evidence for a close relationship between arthropods and nematodes ......................................................................................................................... 503 Zoological implications of the discovery of geothermally-driven communities GAILL F., ZBINDEN M. & PRADILLON F. Adaptations of hydrothermal vent organisms to their environment ............................................................................................... 513 The role of symbiosis in physiology and evolution NARDON P. & HEDDI A. The Role of Symbiosis in Physiology and Evolution ....... 521 BOURTZIS K. Wolbachia: Symbionts as Reproductive Parasites ................................... 523 HEDDI A. The weevil’s symbiocosm and its four intracellular genomes ................... 527 ISHIKAWA H. Characteristic features of the genome of an aphid endosymbiotic bacterium, Buchnera .................................................................................................................. 535 JEON K.W. Integration of bacterial endosymbionts in amoebae .................................. 541 Diversification and evolutionary Ecology MARTENS J. & PÄCKERT M. Disclosure of songbird diversity in the Palearctic/Oriental transition zone ............................................................................................................ 551 Ways for improving modern zoological education BUCKERIDGE J.St.J.S. Zoological Education in New Zealand: a 21st Century perspective ...................................................................................................................................... 561 AZARIAH J. A New Engine For a Holistic Zoology Education in the 21st Century ..... 569 POR F. D. The Crisis In Teaching Of Zoology: The Israeli Experience ......................... 575

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BUCKERIDGE J.St.J.S. Ways for improving modern zoological education: overview of the session ......................................................................................................................... 581 Coordinated development and use of collections databases POSS G. Coordinated Development and Use of Collections Databases ..................... 585 FORTUNATO H. Evolutionary Paleontology and Informatics: The Neogene Marine Biota of Tropical America (NMITA) Database ....................................................................... 591 LEGAKIS A. & EMBLOW C.S. The Register Of Collections Of European Marine Species: An Overview ............................................................................................................ 603 FROESE R. & REYES R.Jr. Use Them Or Lose Them: The Need to Make Collection Databases Publicly Available .................................................................................................. 611 WILEY E.O. & PETERSON A.T. Distributed Information Systems and Predictive Biogeography: Putting Natural History Collections to Work in the 21st Century ........... 619 The taxonomic impediment, in search of a remedy action POR F.D. Remedies for the Taxonomic Impediment in Zoology .................................. 627 CRESSWELL I.D. & BRIDGEWATER P.B. The Global Taxonomy Initiative (GTI) and the International Congress on Zoology – a perspective on the role of the Convention on Biological Diversity and UNESCO ............................................................................... 631 FAUCHALD K. Taxonomic impediment in the study of marine invertebrates ......... 637 POR F.D. A “Taxonomic Affidavit”. Why it is needed? .................................................. 643 The new International Code of Zoological Nomenclature and related issues MINELLI A. Zoological nomenclature after the publication of the Fourth Edition of the Code ................................................................................................................................... 649 HOWCROFT J.M.& THORNE M.J. Zoological Record – a bibliographic service and taxonomic resource ............................................................................................................... 659 GREUTER W. Biological nomenclature in the electronic era: chances, challenges, risks ............................................................................................................................................. 665 RIDE W.D.L. The International Code of Zoological Nomenclature, 4th Edition - What Next? .................................................................................................................................. 673 WYRWOLL T.W. Still Desiderata: Scientific Names for Domestic Animals and Their Feral Derivatives .............................................................................................................. 683 Special presentations TIAGO C.G. & HADEL V.F. Neotropical Biodiversity Conservation and Sustainable Use in São Paulo State (Brazil) - BIOTA/FAPESP - The Biodiversity Virtual Institute ...... ............................................................................................................................................. 701

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BUCKERIDGE J.St.J.S. & GORDON D. Species 2000 New Zealand: Outcomes of the February Symposium ............................................................................................................ 705 ´ PRÓSZY NSKI J. Large computer monographs in zoology - possibilities and perspective. Demonstration of a test case - “Salticidae (Araneae) of the World” ............... 711 BÃNÃRESCU P.M. New data on “satellite” fish species and their evolutionary significance ................................................................................................................................... 715 List of Participants .............................................................................................................. 725 Index ....................................................................................................................................... 737

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Preface of the Editorial Committee This volume contains the proceedings of the 18th International Congress of Zoology organized by the Hellenic Zoological Society and held at the National and Kapodistrian University of Athens, Greece from the 28th of August till the 2nd of September 2000. The congress is a continuation of the series of International Congresses of Zoology that were started in Paris in 1889. During the 5 days of the congress, 233 participants from 36 countries around the world attended 102 oral presentations that were divided into 3 opening lectures, 8 general symposia, 8 special symposia, 4 general discussions, 1 special mini symposium and 6 special presentations. 127 posters were also exhibited on the site of the congress. The proceedings editorial committee was established by the General Assembly of the congress, which also decided to hold the next International Congress of Zoology in Peking, China in 2004, expressing the willingness of the participants to continue this institution. This congress will be organized by the China Zoological Society and the Institute of Zoology of the Chinese Academy of Sciences. The General Assembly also established the International Congress of Zoology Committee, which will overlook the next congress and will also decide on the statutes of the International Congresses. This committee includes Dr. W. Bock (USA), Dr. J. Buckeridge (New Zealand), Dr. E. Cooper (USA), Dr. Daxiang Song (China), Dr. R. Polymeni (Greece) and Dr. M. Schmitt (Germany), with Dr. S. Poss (USA) as secretary. In this volume, we are happy to present you a number of very important contributions that can be considered as milestones for the study of Zoology in the beginning of the 21st century. The publication of this volume would not be possible without the generous assistance of UNESCO, which we warmly thank. We would also like to thank the colleagues who accepted the task of reviewing and providing valuable comments on the submitted papers, and also all the contributors to this volume. The Editorial Committee

© xiiPENSOFT ThePublishers new panorama of animal evolution Sofia - Moscow

A. Legakis, S. Sfenthourakis, R. Polymeni & M. Thessalou-Legaki (eds.) The New Panorama of Animal Evolution Proc. 18th Int. Congr. Zoology, pp. xii-xiv, 2003

Opening Remarks Francis Dov Por, Chairman, Organizing Committee

Dear friend zoologists, It is with deep satisfaction and with a sentiment of humility that we are starting, in this olympic year, the International Congresses of Zoology of the New Era, in Athens where Aristotle, the father of Zoology taught. Zoology, the revolutionary science of Darwin, was among the very first disciplines to build an international organization. The Congresses started in 1889 on the initiative of the Société Zoologique de France on the occasion of the International Exposition in Paris. For decades to come, Milne-Edwards, Perrier, Caullery and Grassé were the Presidents of the Permanent Commission of the Congresses. Raphael Blanchard was the soul of the Congresses for more than 30 years. We are glad to have after 110 years, the representatives of the Société Zoologique de France here with us. Chers Mr. Daguzan, vice-président de la Société Zoologique, Mr. D’Hondt, son Secrétaire Générale et Mr. Dupuis, doyen des participants aux congrés, nous sommes heureux de vous voir aujourd’hui parmi nous. In all the years that followed, the Congresses were held at regular intervals till 1963 under the direction of a “Comité Permanent”. For many years, French was the official language of the congresses. Great names were in the chair of these meetings and keynote lectures were presented by such names like von Virchow, Agassiz, Metschnikov, Grassé, Romer, Julian Huxley and others, It has been a long and meritorious history of which I shall mention only the beginnings and the final moments. Right from the beginning, in Paris, on the initiative of Raphael Blanchard, the Congresses dealt with problems of Zoological Nomenclature. In due time the International Committee of Zoological Nomenclature started to work in the framework of the congresses, routinely submitting its reports to the Congress Assemblies. The attendance increased from congress to congress. From a few tens in Paris and in Moscow – where there were almost only Russian zoologists from all parts of the then Russian Empire - to 700 in Budapest in 1927. The London Congress set a target of 1000, but there were 1400 members and 400 associates. Finally in Washington the number reached 2500. Clearly, there was a problem with the big numbers. In parallel, the number of sessions and sections increased, to keep abreast with the growing specialization. In London in 1958 there were 8-9 daily parallel sections of communications. In Washington an attempt was made to organize symposia instead.

Opening Remarks

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There were no less than 29 such symposia. The problem of unifying subjects became even more important than the numbers of participants. In London, the Darwin-Wallace Centenary of that year provided for a unifying framework. The congress in Washington in 1963 chose as its symbol the Phoenix bird and the goal was “a phoenix-like rebirth of breadth of vision in the study of animal life”, in the words of its president Alfred Romer. Or according to the General Secretary Gairdner Moment, the Phoenix was a symbol of the ”organism reborn from its homogenized macromolecules”. The Phoenix did not rise. What happened? The Washington Congress decided that the Board of the Division of Zoology of the newly founded IUBS, would assume in the future the role of the Comité Permanent and would be responsible for the maintaining and the continuity of Zoological Congresses. This did not work. There was an invitation from New Delhi, which was withdrawn for lack of funds. The new International Congresses of Systematic and Evolutionary Biology ICSEB, took over what in the view of many has been the role of the Zoological Congresses. The International Committee of Zoological Nomenclature became an independent organism in IUBS. A gallant effort was made in 1972 by Vaissière and the French colleagues to convene a XVIIth Congress in Monte Carlo. Attendance was poor and the proceedings never left the xerox stage. A long hiatus started. The care for the “vanishing species” was central in Washington. Instead, what followed, was the vanishing of Zoology from the international academic scene. Names were even changed in order to avoid the word “Zoology”! This unbearable situation appeared in its full light after the 1992 Rio de Janeiro Conference and the ensuing Convention on Biodiversity. Now, after nearly three decades since Monte Carlo, the computer revolution entirely changed the situation. With rapid communication and interchange, a reunification of the splinter specialties of Zoology became easily possible. The concept of an integrative zoology, synthesizing data and results ranging from molecular biology to behavior, gained wide acceptance. Cybernetics became the means which could raise again the Phoenix of unified zoology on “wwwings”! This Congress sprung into life entirely through the world-wide web. What started from my letter exchange with Rosa Polymeni found within a few months a world wide positive response. On our web page and with the care of Stuart Poss, the congress turned rapidly into a vibrant virtual, electronic reality. My thanks to both of you, dear friends. The Congress in Moscow in 1893 obtained a financial support of 7,000 gold roubles personally from Emperor Alexander II and the Czarevitsch Nikolas. Seventy years later the Congress in Washington had a budget of 256,000 $ (old dollars!) of which 200,000 came from the US Government through the NSF and of which 100,000 alone were spent in travel grants! Athens started from nothing. I wish to give my full appreciation and thanks to the Hellenic Zoological Society, our host, which had the courage to sign the blank check of the XVIIIth Congress. We received back the sponsorship of IUBS and this has been a major moral buster. For this, our thanks are due especially to Marwalee Wake and Talal Younes. We have received a grant from UNESCO/MAB, thanks to Peter Bridgewater,

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for the publications of the Congress. National Zoological Societies have also contributed from their meager means. But the present Congress owes its existence almost exclusively to the voluntary enthusiasm of its participants and their registration fees. We are especially thankful to the 20 organizers of the symposia and discussions and to the over 100 invited speakers who did not receive resources from us. Special thanks are due to Sandro Minelli and to Philip Tubbs who brought the meeting of the International Committee on Zoological Nomenclature back to the venue of the Congress of Zoology. The symposium program of this Congress strove to present a cross-zoological picture of the many levels of zoological inquiry, both horizontal and vertical. We shall have a very good selection of such symposia. I am only sorry that ethology is not sufficiently represented. The four General Discussions on stringent issues of zoological science and education policy are an innovation which has to prove its justification for the future. The world community of zoologists has to regain its say in international science politics. Due to the special panoramic structure of the Congress, specific aspects of faunal conservation, important as they are, could not be sufficiently represented. Hopefully this will be done in the future. Attendance here in Athens is far from the incommunicable thousands in the last congresses. Perhaps too far. But if we will succeed to create a precedent and a framework which will conveniently re-unite on line Phoenix-like, all the zoologists and make them interact, both virtually and in future reunions, this Athens Congress will really be a new start. During this week we shall have plenty of opportunities in the lecture halls and outside, to discuss the ways in which Zoology should be put back again on the academic world map. The world of culture has changed much since the Washington congress. It needs an active zoological thinking in order to redefine our relation to the living world in face of the dangers of destruction and in order to respond to the onslaught of creationism and to the ethical mysticism of the “deep green” philosophy. All this we shall try to synthesise in the General Assembly which will take place on Friday. Unlike the sleepy Business Meetings of regularly functioning organisms, this meeting should represent the quintessence of our efforts here. Please attend! Let us work together for the successful proceedings of this Congress and reach a fruitful closing session. Long live Zoology, the rich and integrated science of animal evolution and of the human roots! Thank you all for coming.

© PENSOFT Publishers Sofia - Moscow

A. Legakis, S. Sfenthourakis, R. Polymeni & M. Thessalou-Legaki (eds.) Opening Remarks The New Panorama of Animal Evolution Proc. 18th Int. Congr. Zoology, pp. xv-xvi, 2003

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Opening Remarks Rosa Polymeni, Secretary, Organizing Committee

Distinguished Minister of Agriculture, Distinguished Rector of the University of Athens, Dear colleagues, In 1963, Prof. Romer, the president of the last official ICZ in Washington stressed the disintegration of Zoology stating that “today each biologist has a much better knowledge of some fraction of the picture. But few of us can or do make any attempt to fit the pieces together. The animal has dissolved into fragments; and so has the Science of Zoology”. Four and a half years ago we were wondering if this opening ceremony would ever happen. It is exactly then, that I received a letter from Prof. Por –a very serious letter as he characterized it - proposing to help him for the realization of the 18th (New) International Congress of Zoology. The purposes of this idea are to resist against the extreme specialization which very often develops into a blind alley, to bring forward again the rich unifying aspects of Zoology, and to reverse the crisis in the professional Zoological education. These facts which the last 20 years I had the sad opportunity to feel and realize in my own professional domain, pushed me to answer the fatal “Yes”. At the very beginning we tried to bring back in action the International Zoological Society. And it worked out! The very hopeful fact is that the new generations of Zoologists responded too. But, believe me, it has not been easy. Very soon the Hellenic Zoological Society entered the game officially. My colleagues in Athens, especially Dr. Spyros Sfenthourakis, who worked on a 24 hour basis, and also Prof. Tasos Legakis and Prof. Maria Legaki, worked very hard to keep the Congress going. The financial matters have been the real nightmare of the Congress. We started from the absolute zero. Thanks to Professor Por’s continuous injections of optimism we were able to overcome our normal pessimism and reach our goals. We have received support from many Zoological Societies and Organizations, especially from the French Zoological Society, who founded the institution of the International Congresses of Zoology. This fact invigorated us to keep on and conclude our efforts. Chers collègues, de la Société Zoologique de France, nous sommes très heureux de vous avoir parmis nous. Nous souhaitons de pouvoir reétablir ensemble et continuer l’institution des Congrès Internationaux de Zoologie.

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I would like to express my thanks to all the conveners and invited speakers who came to support the Congress by their own means, as well as the to the representatives of UNESCO, the International Committee of the Zoological Nomenclature and the International Union of Biological Sciences. Special thanks to our Section of Zoology Marine Biology and to the University of Athens, under the aegis of which we accomplished the realization of the Congress. The list would very long in order to mention all the moral and, more infrequent, financial support that we have received. Despite our good intentions, some mistakes, omissions or delays may have occurred. We take full responsibility for these and we ask for your understanding. I wish this congress will prove fruitful and will support effectively the discipline of Zoology. Thank you

A General Review of Zoological Trends During the 20th Century

Invited Lectures

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A. Legakis, S. Sfenthourakis, R. Polymeni & M. Thessalou-Legaki (eds.)

A General Review of Zoological Trends The During the 20th of Century 3 New Panorama Animal Evolution Proc. 18th Int. Congr. Zoology, pp. 3-13, 2003

A General Review of Zoological Trends During the 20th Century E. R. Pianka Integrative Biology C0930, University of Texas at Austin, Patterson Labs, 24th at Speedway Austin, TX 78712-1064 U.S.A. E-mail: [email protected]

Abstract Enormous progress has been made in zoology during the 20th century, largely due to a multitude of clever new technological advances: electron microscopes, oscilloscopes, radioisotopes, radiotelemetry, digital and satellite imagery, PCR and DNA sequencing, global positioning systems (GPS), rapid and affordable travel, unimaginable computing prowess, faxes and email. All this new technology has allowed zoologists to study things previously impossible. The century began with the rediscovery of Mendelian genetics, followed by the discovery of DNA structure, the genetic code itself, instinct and animal behavior, speciation, hybrids, parthenoforms, a new previously unknown Kingdom of chemosynthetic organisms, restriction enzymes, cloning, genetic engineering, genetic control of development, and understanding of metabolic pathways. One of the strongest recurrent themes in biology this century has been to consider all sorts of phenomena within the context of natural selection. Phylogenetic systematics has revitalized many areas of biology, forcing and facilitating an evolutionary approach. Evolution provides the conceptual backbone of zoology. Zoologists study phenomena that range across vastly different spatial and temporal scales, from molecules to cells to organisms to populations to communities and entire ecosystems. Like other scientists, most zoologists have rushed to embrace the reductionistic approach. Too often, workers at different levels look somewhat askance at the next higher level of approach. The reason for this hesitancy to accept the next higher level may be that one must slur over interesting detail at one’s own level in order to practice biology at the next level up. Each level of approach offers distinct advantages but suffers from its own problems. Molecular biologists cannot “see” the objects of their studies, but they can do experiments in Eppendorf tubes in small spaces in a matter of hours. An experiment is planned before lunch, executed that afternoon and results are analyzed that evening or the next day. Rapid progress can be made with such a compressed timetable. Other sorts of biology require more space and greater patience. Funding for zoological research is strongly skewed towards molecular biology. We should all attempt to couple our approach to higher levels and we should be more tolerant of others working at higher levels of approach.

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Funding should be spread more equitably across disciplines. We have made impressive strides in understanding phenomena at most levels of approach in biology, but the approach at the community-ecosystem level lags far behind others. Much more thought needs to be devoted towards attempts to connect community properties with those of individuals in populations. Examples of how community-level properties could emerge from attributes of individuals are given.

Introduction First, I’d like to thank the organizing committee for inviting me to present this opening address to the 18th International Congress of Zoology. I suspect that my Greek friends Petros Lymberakis, Moysis Mylonas, and Efstratios Valakos, were instrumental in my being chosen and I’d like to thank them as well. I did not choose this title — it was “assigned” to me by the organizers. How could anyone review a subject as broad as zoology over an entire century? It’s the kind of challenging thing one would expect somebody like Ernst Mayr to do. I guess if you live long enough, you get a chance at something like this. Obviously, I won’t be able to mention many things zoologists have discovered during the past one hundred years. Please, do forgive me if I fail to mention your own favorite area of research! I’ve been a zoologist for only 35 to 40 years and I’ve seen rather massive changes and new developments during just these four decades. For example, when I entered graduate school in 1960, numerical taxonomy was just being invented. It quickly replaced “old fashioned classical systematics,” and then, just as quickly, phenetics was swept away by phylogenetics, which has endured and become entrenched during the last several decades. Zoology has become Obsolete I fear that I must begin with some bad news for all zoologists. Zoology is rapidly becoming obsolete! Let me illustrate this with the example of my own ill-fated department at the University of Texas. It seems as if people get restless towards the end of centuries and they like to reorganize things to become more “modern.” From 1892 to 1899, the University of Texas had a “School of Biology” which included botanists, geologists, and zoologists. As the end of the century drew near, in 1899, the University reorganized and created three new “departments” of botany, geology, and zoology. These departments thrived and became recognized as among the best in the world. But last year, in 1999, the powers that be at my University got restless and decided to reorganize biology once again. [After all, it was the end of another century!] The once proud Department of Zoology where I spent the last 32 productive years was abolished on the eve of its 100th birthday! Our Departments of Botany and Microbiology were also eliminated. We went back a century to the old 1899 plan and created a new “School of Biological Sciences.” Departments were out now, replaced with four “Sections.” Their major motivation must have been to emphasize molecular biology since two of the four new sections are:


and

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Molecular Cell and Developmental Biology Molecular Genetics and Microbiology

Another strangely narrow small section is Neurobiology. All three of these sections adopt a reductionistic approach. In the fourth section, mine, we embrace an explicit anti-reductionistic approach. We call it Integrative Biology Our group includes botanists and zoologists who work on ecology, evolution and organismal biology. We understand the need to integrate across levels of organization and taxonomic groups. We engage in interdisciplinary research (for example, I’m an ecologist and I have a small DNA laboratory). We hope that zoological research will flourish in our section. These four sections are expected to serve as focal points for research, but all activities including faculty hiring and promotion, undergraduate and graduate programs, teaching and advising, are now coordinated through the overarching School of Biological Sciences, which has its own Director and staff. The School is a sort of “super” department for the biological sciences. What do you suppose they’ll do when 2099 rolls around?? If, indeed, humans haven’t gone extinct by then! Techniques and Technological Breakthroughs When you think about the past century, the first things that pop into mind are new techniques and technological breakthroughs. Electron micrographs allow us to see and study phenomena at a microscopic level. Satellite imagery has given us “macrographs” that allow us to see and study very large phenomena like El Niño. Satellite imagery has been available long enough now (since 1972) that chronosequences can be used to follow cyclical phenomena such as fire succession in grasslands. Oscilloscopes are a relatively old invention that greatly enhanced the ability of physiologists to study neural phenomena. Isotopes allow us to follow the movements of molecules through an organism or an ecosystem and to follow a given cell or cell lineage through development as well as many other things like carbon 14 dating. Modern molecular biotechnological tools, such as restriction enzymes and gene splicing, now enable geneticists to transfer particular genes from one organism to another using vectors such as plasmids and various viruses. Human insulin and growth hormone are now routinely produced in chemostats of E. coli bacteria that have had human genes spliced into their genomes. Transgenic cows produce milk containing medically useful proteins such as human blood clotting factors (useful for hemophiliacs!) Genetically altered transgenic bacteria have been used as living vaccines that confer resistance to particular diseases such as typhoid. Such recombinant DNA technology has also enabled us to produce useful new life forms such as pollutant-eating bacteria that can help us to clean up what’s left of our environment. Pest resistance and nitrogen-fixing genes are

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being spliced into crop plants with the hope of vastly increasing yields. Any day now, some enterprising genetic engineer will transplant elephant growth genes into cattle to make bigger and better cows! You want a bigger chicken: I’ll transplant some ostrich genes into chickens! We are audaciously bypassing natural selection and creating whatever phenotypes we think best. A large percentage of US crops (corn, soybeans, cotton, tomatoes, etc) are genetically engineered and are now being grown commercially. More transgenic organisms will eventually be designed for release into nature. Genetically engineered organisms could have adverse effects on other species in natural ecosystems. We already have enough natural pests and certainly don’t want to make any new ones! Unfortunately, we still know far too little to engineer ecological systems intelligently. Obviously genetic engineers should work hand in hand with ecological engineers (a nearly non-existent breed)! Radiotelemetry has advanced to the point that very small transmitters can be attached to small animals and used to follow their movements. Large animals like sea turtles and whales now carry devices that transmit their locations to satellites which download the data at prescribed times and positions. You can now be anywhere and follow a whale’s migration from the arctic to the Antarctic. In many ways, this is the best time ever to be a zoologist. We have easy access to anywhere in the world via rapid and affordable travel. We can go almost anywhere anytime and there are still bits and pieces of wilderness left scattered around the globe. Global positioning systems (GPS), invented for military purposes, now allow us to get relatively exact co-ordinates for any spot on earth quickly and with ease. Modern biological technological tools such as the polymerase chain reaction (PCR) allow us to amplify tiny amounts of DNA, which can now be sequenced relatively easily and inexpensively. DNA sequences can be used to establish degrees of relatedness among animals and to recover robust phylogenies, which can be used to infer probable evolutionary pathways. I have been using computers and the Internet ever since their inception. I learned FORTRAN in grad school during the early 1960’s and I wrote my own programs to do statistical analyses on one of the first vacuum tube IBMs (it took up a entire large room and could not even match one of today’s low-end desktop personal computers). The speed with which personal computers have been improved is awesome. Just a few years ago, I treasured floppy disks. Now I almost never use them, only 100 meg zip disks. When my hard drive failed, I upgraded from 4 gigs to 38 gigs for only $289. Recently we got a 400 megahertz G4 which processes 128 byte bits rather than 32 byte bits. Being twice as fast and processing 4 times as much information at each step makes this computer eight times faster than last year’s. Such computing prowess was unimaginable a mere decade ago. People reading this 10 years from now will undoubtedly laugh at how modest my fancy new computer was! Today you can collaborate with people around the world with ease using faxes and email. While your colleague on the other side of earth is sleeping, you work, emailing it to him at the end of your day. Then, he or she plugs away at it while you sleep. Together, you can work around the clock!


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Major Developments Now let’s consider some other major developments in zoology during the last century. Of course, the century began with the rediscovery of Mendelian genetics and genetics has been a focal point all though the 1900’s. Herman Mueller discovered that x-rays cause mutations. Mid century came the discovery of the structure of DNA, then the genetic code itself, the machinery of genetics, transcription, translation, etc. Instinct and animal behavior came to the fore, as did speciation, hybridization and parthenogenesis. The late W. D. Hamilton (and others) developed the idea of kin selection and inclusive fitness. Studies of sexual selection abounded (Andersson 1994). A new kingdom of chemosynthetic organisms was discovered. Metabolic processes such as the Kreb’s cycle were understood for the first time. These still need to be placed in an evolutionary perspective ... how do metabolic pathways evolve? Why are they sometimes dismantled? The vast majority of mammals can synthesize ascorbic acid but humans cannot and must supplement their diets with Vitamin C. Many aspects of the genetic control of development, including developmental plasticity and canalization, have been elucidated, but much more remains to be learned. Phylogenetic systematics has revitalized many areas of biology and has both forced and facilitated an evolutionary approach. Evolution is Our Conceptual Backbone One of the strongest recurrent themes in biology this century has been to consider all sorts of phenomena within the context of Darwinian natural selection. Dobzhansky (1971) said that “nothing in biology makes sense except in the light of evolution.” Evolution provides the conceptual backbone of all zoology. Natural Selection: the ultimate inventor Natural selection is surely the ultimate inventor: a short list of some of its many patents includes flight, fusiform shapes, celestial navigation, echolocation, insulation, infrared sensors, hypodermic needles, plus a wide variety of pharmeceuticals including analgesics, antibiotics, diuretics, emetics, laxatives, and tranquilizers. As another example of natural selection, consider gecko feet. These lizards can run up a pane of glass and even run upside down across a ceiling. Scanning electron micrographs show literally millions of elaborate very fine hairlike setae, each bearing tiny hooks and hundreds of spatulae which allow these lizards to gain purchase on almost any surface including very smooth ones (Hiller 1976). A single individual gecko can have as many as a billion spatulae! Several mechanisms of adhesion have been proposed, including suction, glue, electrostatic attraction, and friction. Gecko feet still stick in a vacuum, eliminating suction. Gecko feet have no glands, making glue most unlikely. Experiments using x-rays to ionize air have eliminated the possibility of electrostatic attraction. A smooth pane of glass offers very little in the way of friction, although friction would certainly be quite important when climbing on any rough surface.

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In a very interesting recent study published in Nature (Autumn et al. 2000) of gecko setae, scientists removed a single seta from a large Tokay gecko and under a microscope glued it with epoxy to an extremely fine wire. Each seta ends in hundreds of spatulae, which press up and conform to the substrate. Direct forces of setal attachment were measured with an extremely tiny (about 100 x 100 micrometers) high-tech microelectromechanical sensor (a two dimensional “dual-axis piezoresistive cantilever fabricated on a single-crystalline silicon wafer”). Earlier work that had rejected two previously proposed mechanisms of adhesion, suction and friction (Hiller 1968), had demonstrated that intermolecular forces, or van der Waal’s forces, provided the adhesion. Van der Waals forces are basically like gravitational forces, but acting between molecules. Autumn et al’s amazing high-tech study provided indirect support for such intermolecular forces. Van der Waal’s forces require exceedingly intimate contact between a gecko’s spatulae and the surface and they are extremely weak at distances greater than atomic distance gaps. These authors estimate that if a gecko’s entire billion spatulae were simultaneously engaged with substrate molecules, the force holding a gecko to the substrate would be over 500 pounds per square inch! With such powerful forces, one might expect geckos to be plastered against their substrates unable to move. During a powerful cyclone on Mauritius (Vinson & Vinson 1969), Phelsuma day geckos were actually beaten to death by the furious flapping of leaves they were on — but these dead geckos nevertheless remained firmly attached to the leaves! How do geckos manage to break such strong bonds? How do they control their powerful feet and toes? Autumn et al. (2000) liken the complex behavior of toe uncurling during attachment to blowing up an inflating party favor, whereas toe peeling during detachment is analogous to removing a piece of tape from a surface. During running, geckos peel the tips of their toes away from a smooth surface. Toe peeling may have two effects. First, it could put an individual seta in an orientation or at a critical angle that aids in its release. Second, toe peeling concentrates the detachment force on only a small subset of all attached setae at any instant (Autumn et al. 2000). Indeed, one of the great remaining mysteries is why don’t such clinging toe pads pick up all sorts of debris? These authors comment that manufacture of such small, closely packed arrays mimicking gecko setae is currently beyond the limits of human technology. Nevertheless, the natural technology of gecko foot-hairs could provide biological inspiration for future design of remarkably effective re-usable dry adhesives. Perhaps one day, people wearing gecko skin gloves will climb cliffs and buildings! If so, natural selection will hold the patent! Biological Hierarchies: Time and Space Scales Zoology has a complex hierarchical organization. Zoologists study phenomena that range across vastly different spatial and temporal scales, from molecules to cells to organisms to populations to communities and entire ecosystems (Fig. 1). Across this broad range of scale, factors vary by many orders of magnitude. Emergent properties arise at each level. For example, glycolysis is a property shared by some metabolic pathways but it is not a property of a molecule. Dominance or recessiveness are properties


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Fig. 1. Diagrammatic representation of the time-space scaling of various biological phenomena. Community and ecosystem phenomena occur over longer time spans and more vast areas than suborganismal- and organismal-level processes and entities. Most subdisciplines of biology take a narrow reductionistic approach. A broader integrative approach across all these levels of organization must be adopted.

shared by some genes but not of nucleotides. Sexual behavior is a property shared by some organisms but not of a gene. Sex ratio and population density are properties of groups of organisms but not of single animals. Food web connectance is a property of a community but not a property of a population. Dan Brooks (1988) gave a nice example: (1) individuals move and disperse during their lifetimes, (2) over the lifetimes of multiple individuals, immigration and emigration take place between and among populations, giving rise to metapopulation structure, (3) over still longer time and space scales, geographical ranges shift in response to changing climates and geotectonic movements, ultimately leading to geographical patterns of diversity. Molecular biology is small and fast. You can do multiple experiments in a few rooms using tiny Eppendorf tubes. In some cases, a researcher can plan an experiment while driving to work, execute the experiment early in the AM, go to lunch, and analyze the results later that afternoon. The next day a paper can be written and submitted to Nature. Simple causality reigns in molecules. In contrast, community ecology requires lots of space and time. It may take decades to acquire results. Community ecology is not for the impatient or feint of heart. Multiple causality is the rule and constitutes an effective roadblock. People are impatient — they want results, recognition and fame NOW, not later. Many scientists adopt a reductionistic approach: take something apart into its component pieces and then try to put it back together again. The molecules are in motion,

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but knowing their positions and paths, can you extrapolate to explain phenomena at higher levels? An alternative integrative approach attempts to understand an entire complex entity across levels of organization, although some scientists express disdain for such a perspective. Both the reductionistic and integrative approaches can offer insights, often of very different sorts, into how a biological entity operates. As we race to embrace molecular biology, many have been neglecting higher levels of approach. Indeed, it is worse than simple benign neglect. People working at each level actually express disdain for those struggling to work at higher levels. Molecular biologists think cell biology is sloppy because it necessarily slurs over interesting detail. Cell biologists find physiology crude. Organismal biologists wonder how population biologists can gloss over so much important biology of organisms. Population biologists scoff at community ecologists. Such narrow-minded snobbery towards higher levels of approach is inadvisable and unacceptable. It has resulted in funding being diverted more and more towards molecular biology and away from other disciplines like ecology. Worse, traditional areas of zoology like comparative anatomy and physiology are no longer deemed important and therefore are not attracting new graduate students. “Ology” courses, such as protozoology, entomology, ichthyology, herpetology, etc. have disappeared from curricula everywhere. When everyone has become a molecular biologist, who is going to be able to tell molecular biologists what they are studying. Who will describe new species? Understanding molecular interactions seldom provides great insights into evolutionary forces molding adaptations. This is perilous because all levels of approach are necessary to truly understand any biological phenomenon. We need to integrate from molecules to communities. Proximate versus Ultimate Factors Consider the question “Why do migratory birds fly south in the autumn?” A physiologist tells us that a bird compares photoperiod against its internal biological clock. Decreasing day length stimulates hormonal changes, which in turn alter bird behavior with an increase in restlessness. Eventually this “Wanderlust” gets the upper hand and the birds head south. In contrast, an evolutionist would most likely explain that, by virtue of reduced winter mortality, those birds that flew south lived longer and therefore left more offspring than their non-migratory ancestors. Over a long period of time, natural selection resulted in intricate patterns of migratory behavior, including the evolution of celestial navigation, by means of differential reproductive success. The physiologist’s answer concerns the mechanism by which avian migratory behavior is influenced by immediate environmental factors, whereas the evolutionist’s response is couched in terms of what might be called the strategy by which individual birds have left the most offspring in response to long-term consistent patterns of environmental change (i.e., spring bloom, high winter mortality). The difference between them is in outlook, between thinking in an “ecological” time scale (now time) or in an “evolutionary” time scale (geological time). At the physiologist’s level of approach to science the first answer is complete, as is the evolutionist’s answer at her or his own level. Ernst Mayr (1961) termed these the “how?” and “why?” approaches to biology.


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They have also been called the “functional” and “evolutionary” explanations and the “proximate” and “ultimate” factors influencing an event (Baker 1938). The first involves short-term cues whereas the second is a long-term strategy for passing on genes. Neither is more correct; a really thorough answer to any question must include both, although often only the first can be examined by direct experiment. Nor are those two ways of looking at biological phenomena mutually exclusive; behavioral, physiological and ecological events can always be profitably considered from within an evolutionary framework and vice versa. To understand avian migration, one needs to know about both immediate mechanisms and evolutionary forces. We should all attempt to couple our approach to higher levels and we should be more tolerant of others working at higher levels of approach. Funding needs to be spread more evenly across all levels of approach rather than most of it being devoted to molecular biology. Community Ecology Community structure concerns all the various ways in which members of communities relate to and interact with one another, as well as any community-level properties that emerge from these interactions. Just as populations have properties that transcend those of the individuals comprising them, communities have both structure and properties that are not possessed by their component populations. You can think of a community as a complex network of interacting populations. Ecologists are not very interested in captive animals. Their subjects are wild organisms in natural settings, with a normal environment in which that particular creature has evolved and to which it has become adapted. Rolston (1985) made a useful analogy: he likened life on earth to a book written in a language that humans can barely read. Each page in this book of life represents a species, describing not only its phylogenetic relationships, but also its interactions with its physical and biotic environments, as well as its relationships with its competitors, parasites, predators, and prey. Each chapter represents a biome with pages describing all of its component species. Zoologists are just now acquiring the skills necessary to read and decipher this book, but the poor book is tattered and torn, pages are missing (extinct species such as passenger pigeons), and entire chapters have been ripped out (e.g., the tall grass prairies of midwestern North America). There is considerable urgency to study wild organisms in pristine natural habitats now. We must save as much of this vanishing book of life as possible. We must also read it before it is gone forever. Community ecology has to attract population ecologists who are well versed in natural selection. It has become the province of systems ecologists and ecosystem engineers: more born-again population ecologists should become community ecologists. Community ecology is doubtlessly one of the most difficult kinds of biology, but it has obvious utility as we approach oversaturation of this planet. Moreover, data must be gathered now because so many systems are vanishing. Community ecology is also very promising. Major new discoveries, potentially things as important as DNA and natural selection, remain undiscovered because biologists have shied away from this discipline. Community ecologists are still in the process of developing their vocabulary. Identification of appropriate aggregate variables or macrodescriptors (Orians 1980) is

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essential, but constitutes a double-edged sword; macrodescriptors allow progress but simultaneously constrain the directions that can be pursued. To be most useful, macrodescriptors must simplify population-level processes while retaining their essence without fatal oversimplification. Examples include trophic structure, connectance, rates of energy fixation and flow, ecological efficiency, diversity, stability, distributions of relative importance among species, guild structure, successional stages, and so on. At this early stage in community ecology, we should not become overly locked in by words and concepts until we are confident that we are going in the most fruitful directions. Moreover, a diversity of approaches seems desirable. Even the trophic level concept should not be inviolate. A major pitfall for community ecologists is that communities are not designed directly by natural selection (as are individual organisms). We must keep clearly in mind that natural selection operates by differential reproductive success of individual organisms. It is tempting, but dangerously misleading, to view ecosystems as “superorganisms” that have been “designed” for efficient and orderly function. Antagonistic and asymmetric interactions at the level of individuals and populations (such as competition, predation, parasitism and even mutualisms) must frequently impair certain aspects of ecosystem performance while enhancing other properties. Much more thought needs to be devoted towards attempts to connect community properties with those of individuals in populations (Pianka 1992). Terrestrial succession offers a possible example of how community-level properties could emerge from those of individuals. For an individual plant, a fast rate of photosynthesis and hence a rapid growth rate and high rate of reproduction are presumably incompatible with shade tolerance, and hence competitive ability in a light-limited situation. In contrast, shade tolerance and an ability to compete require slower rates of photosynthesis, growth and reproduction as well as relatively larger offspring. Such physiological trade-offs at the level of individuals could very well dictate many of the sequential patterns of species replacement (i.e., colonizing species to climax species) that characterize terrestrial succession. Another example concerns ecological energetics. Only about 10% to 15% of the energy at any given trophic level is available to the next higher trophic level (an “ecological efficiency” of 0.10 to 0.15). This low efficiency has become a sort of rule for how natural communities behave. Genetic engineers tinkering with plant genes hope to increase ecological efficiency by making transgenic crop plants. Why are natural communities so inefficient? Natural selection operating on individual predators favors more efficient predators — this in turn increases efficiency of flow of energy up through the trophic levels but reduces a system’s stability. In homogeneous simple predator-prey systems, efficient predators harvest their prey to overexploitation, driving it extinct and then starving to death themselves. Selection operating on individual prey always favors escape ability, which reduces energy flow and enhances stability, exactly the reverse effects as those operating on predators. Heterogeneous complex habitats offer hiding places where prey can take refuge from predators, thus reducing energy flow and enhancing stability. In the coevolutionary arms’ race between a predator and its prey, the prey must remain a step ahead of their predators, or they are overharvested to extinction. As a corollary, community-level properties of ecological


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efficiency and community stability may in fact be inversely related precisely because natural selection operates at the level of individual predators and prey. Thus, the apparent constancy and low level of ecological efficiency observed in natural ecosystems could be a result of the “compromise” that must be reached between coevolving prey and their predators. Humans seem to feel that we do not have to obey ecological rules — we think that we are somehow above nature. Soon we may find out that we are not! Acknowledgments I am grateful to the organizers for inviting me to give this address. I thank Michael Pianka, Monica Swartz, David Hillis, and Antone Jacobson for reading earlier drafts and for suggesting improvements. Aaron Bauer gave me the Vinson and Vinson reference. References ANDERSSON M. 1994. Sexual Selection. Princeton University Press. AUTUMN K., LIANG Y.A., HSIEH S.T., ZESCH W., CHAN W.P., KENNY T.W., FEARING R. & R. J. FULL 2000. Adhesive force of a single gecko foot-hair. Nature 405: 681-685. BAKER J. R. 1938. The Evolution of Breeding Systems. In, Evolution, essays presented to E. S. Goodrich. Oxford University Press, London. BROOKS D.R. 1988. Scaling effects in historical biogeography: A new view of space, time, and form. Syst. Zool. 38: 237-244. DOBZHANSKY T. 1973. Nothing in biology makes sense except in the light of evolution. Amer. Biol. Teacher 35: 125-129. HAMILTON W.D. 1964. The genetical evolution of social behavior (two parts). J. Theoret. Biol. 7: 1-52. HILLER U. 1968. Untersuchungen zum Feinbau zur Funktion der Haftborsten von Reptilien. Z. Morph. Tiere 62: 307-362. HILLER U. 1976. Comparative studies on the functional morphology of two gekkonid lizards. J. Bombay Nat. Hist. Soc. 73: 278-282. MAYR E. 1961. Cause and effect in biology. Science 134: 1501-1506. ORIANS G.H. 1980. Micro and macro in ecological theory. BioScience 30: 79. PIANKA E.R. 1992. The State of the Art in Community Ecology. In Adler K. (ed.), Herpetology. Current Research on the Biology of Amphibians and Reptiles. Proceedings of the First World Congress of Herpetology at Canterbury. Contributions to Herpetology, Number 9, pp. 141-162. ROLSTON H. 1985. Duties to endangered species. BioScience 35: 718-726. VINSON J. & J.-M. VINSON. 1969. The saurian fauna of the Mascarene Islands. Mauritius Inst. Bull. 6: 203-320.

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A. Legakis, S. Sfenthourakis, R. Polymeni & M. Thessalou-Legaki (eds.) On Species and Speciation The New Panorama of Animal Evolution Proc. 18th Int. Congr. Zoology, pp. 15-18, 2003

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On Species and Speciation E. O. Wiley Department of Ecology & Evolutionary Biology, Natural History Museum and Biodiversity Research Center The University of Kansas, Lawrence, KS 66045 USA

Abstract Discovering the mode and tempo of speciation requires detailed knowledge of the relationships and distributions patterns among species in clades where extinction and dispersal have not affected the original speciation pattern. It also requires adoption of a species concept that provides an ontology appropriate to the processes thought to be at work. Modern phylogenetic and biogeographic methods, coupled with a lineage concept of species, have allowed systematists to corroborate Wallace’s hypothesis that the predominant biogeographic pattern between sister species is a pattern of allopatry, suggesting that vicariance is the predominant mode of speciation.

Wallace (1855) concluded that the most likely place one would find the closest relative of a particular species was in an adjacent region and not in the sympatry. This observation was used by later workers to develop what we know recognize as Model I allopatric speciation (e.g., Jordan 1905, literature summaries by Bush 1975 and Wiley 1981). However, determining the frequency of this mode of speciation compared to other possible modes was not possible until the development of modern phylogenetic techniques for reconstructing the evolutionary relationships among species and the identification of monophyletic groups of species (Hennig 1966). The combination of a robust phylogenetic tree and a detailed knowledge of the distributions of species within a monophyletic group permit both qualitative and analytical studies of the relative frequency of modes of speciation (Wiley 1981, Lynch 1989). Wiley (1981) outlined the patterns of phylogeny and biogeography one might expect if a particular clade of group of clades speciated. For example, patterns of phylogeny and biogeography repeated between groups of unrelated clades suggests vicariant, Mode I, speciation, while unresolved polytomies between closest relatives suggest peripheral isolation and persistence of the central ancestral species. Wiley and Mayden (1985) investigated a number of patterns of North American freshwater and coastal marine fishes and found an over whelming pattern of allopatry between sister species. Similar patterns are found in many groups of North American freshwater fishes (e.g. Mayden 1988, Wood & Mayden 1993, Grady & LeGrande 1992). Similar patterns also have been

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demonstrated in several vertebrate groups, as summarized by Lynch (1989: frogs, fishes, and birds) and Chesser and Zink (1994: birds). The predominance of allopatry between sister species even extends to the deep ocean where Myia and Nashida (1996) have shown that the majority of sister species of the mesopelagic fishes of the genus Cyclothone are largely to entirely allopatric in their distributional patterns. Determining the tempo and mode of speciation is not easy. The first requirement is a robust phylogenetic hypothesis at the species level. The second requirement is a detailed knowledge of the distribution of populations in each species. The third requirement is that extinction or a change in habitat is not giving a false picture of the original pattern of speciation. That is, if extinction is common and the extinct relative is not included in the analysis, one might very well conclude that sympatry was common among recent sister relatives when, in fact, actual sister species were allopartic when both were extant. Conversely, movement of sister species into non-contiguous refugia might give the impression of allopatry, even if the species had speciated via some sympatric speciation mechanism. So, such analyses are by no means straightforward. There is another complicating factor, the manner in which systematists conceive of species as entities (species taxa). Among those who conceive of species as existing in nature (realists as opposed to nominalists), the very perception of the pattern of speciation can differ because two investigators have adopted different species concepts. Consider, for example, the patterns of variation and distribution of a small clade of topminnows, the Fundulus nottii group (Wiley & Hall 1975, Wiley 1977). Agassiz (1854) originally described five species. Mayr (1963) considered the clade as a single polytypic species and he considered the recognition of five species as an example of typological thinking. Wiley (1977) recognized five species. (I do not know if these are the same five species originally described by Agassiz as the types were lost of misplaced.) Obviously, the difference between Mayr’s and Wiley’s interpretations lies in the adoption of different species concepts. Adding to the possible confusion is the ontological status of the species themselves. Hennig (1966), Ghiselin (1966, 1974), Hull (1976) and others have asserted that species taxa are individual entities and neither sets nor natural kinds. Although the claim that species taxa are individuals rather than kinds or sets may be “radical,” the properties of species taxa seem to fit this concept. Species taxa, unlike natural kinds, have particular origins and extinctions. They are not timeless, but time bound. Species taxa, unlike sets, can change their parts over time. Under this concept, an individual organism is not a member of a species taxon, but rather, it is a part of a species taxon. And, groups of species taxa make up the parts of a monophyletic groups rather than being members of a monophyletic group. Further, species and other taxa do not function within scientific theories in a manner similar to natural kinds (Wiley 1989). If species are, logically, individuals, then what of species concepts? There are a plethora of such concepts (see review by Mayden & Wood 1995). Some, often described as “operational”, are designed to help investigators discover species but fail to capture the relationship between macroevolutionary theory and the relationship of individual species to that theory. They usually describe properties thought to be characteristic of species, such as sufficient morphological distinctiveness or possession of an apomorphy. Examples include the morphological species concept and various version of the

On Species and Speciation

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phylogenetic species concept. Obviously, if particular species are individuals and not kinds, then such species concepts, which treat species as kinds or sets, cannot serve as general concepts regardless of their utility to particular systematists. In other words, while it is true that many species are morphologically distinct, or have one or more apomorphies, it is also true that such characterizations do no actually define a natural kind “species” that exists in some logical relationships with the underlying theories of descent with modification and speciation. Species are not apomorphies nor are they smallest or largest clusters (sets) of organisms or populations. However, I do not wish to imply that such concepts are useless. They may very well allow us to discover new species that will be shown by later investigation to have more interesting biological characteristics. Others attempt to derive the kind species directly from a process theory. This is the usual way natural kinds are defined in science. One cites biological characteristics such as isolated breeding system (e.g., Biological Species Concept; Dobzhansky 1937, Mayr 1942) or continuity of lineages through time (e.g., Evolutionary Species Concept: Simpson 1961, Wiley 1978) that are judged to delimit members who play a significant role in natural processes (anagenesis, speciation, etc,). Fundulus nottii is a member of the kind “evolutionary species” because it is hypothesized to have properties that define the kind “evolutionary species.” That is, it forms a lineage though time that has descended from an ancestral lineage via a speciation event. Such concepts can be judged based on whether they capture a more or less complete picture of species as they are found in nature. For example, the Biological Species Concept is not wrong just because we recognize many species that have entirely allopartic distributions. It is simply incomplete. A lineage concept seems to be much more general. Macroevolutionary processes produce descent trees composed of ancestral and descendant lineages. Species are those lineages (Hennig 1966). Acknowledgements Thanks to my Greek hosts for a wonderful meeting and the organizers for inviting me. Thanks also to Keith Coleman, David Hull, and Rick Mayden for many hours of conversation on the “species question.” References BUSH G.L. 1975. Modes of animal speciation. Annual Review of Ecology and Systematics 6: 339364. CHESSER R.T. & R.M. ZINK 1994. Modes of speciation in birds: a test of Lynch’s (1989) method. Evolution 48: 490-497. CRACRAFT J. 1983. Species concepts and speciation analysis. Current Ornithology I:159-187. DOBZHANSKY T. 1937. Genetics and the Origin of Species. Columbia University Press, New York, NY. GHISELIN M.T. 1966. On psychologism on the logic of taxonomic controversies. Systematic Zoology 15: 207-215. GHISELIN M.T. 1974. A radical solution to the species problem. Systematic Zoology 23: 536-544.

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GRADY J.M. & W.H. LeGRANDE 1992. Phylogenetic relationships, modes of speciation, and historical biogeography of the madtom catfishes, genus Noturus Rafinesque (Siluriformes: Ictaluridae). In Mayden R.L. (ed.), Systematics, Historical Ecology, and North American Freshwater Fishes. Stanford University Press, Stanford, CA, pp. 747-777. HENNIG W. 1966. Phylogenetic Systematics, Urbana, Illinois, University of Illinois Press, Urbana, IL. HULL D.L. 1976. Are species really individuals? Systematic Zoology 25: 174-191. JORDAN D.S. 1905. On the origin of species through isolation. Science 22: 545-562. LYNCH J.D. 1989. The gauge of speciation: on the frequencies of modes of speciation. In Otte D. & J.A. Endler (eds.), Speciation and its Consequences. Sinauer Associates, Sunderland, MA, pp. 527-553. MAYDEN R.L. 1988. Vicariant biogeography, parsimony, and evolution in North American freshwater fishes. Systematic Zoology 37: 331-357. MAYDEN R.L. & R.M. WOOD 1995. Systematics, species concepts, and the ESU in biodiversity and conservation biology. In Nielson J. (ed.), Evolution and the Aquatic Ecosystem: Defining Unique Units in Population Conservation. American Fisheries Society, Bethesda, MD, pp. 58113. MAYR E. 1942. Systematics and the Origin of Species. Columbia University Press, New York, NY. MAYR E. 1963. Animal Species and Evolution. Harvard University Press, Cambridge, MA. MYIA M. & M. NASHIDA 1996. Molecular phylogenetic perspective on the evolution of the deep-sea genus Cyclothone (Stomiiformes: Gonostomatidae). Ichthyological Research 43(4): 375398. WALLACE A.R. 1855. On the law which has regulated the introduction of new species. Annals and Magazine of Natural History 16(2): 184-196. WILEY E.O. 1977. The phylogeny and systematics of the Fundulus nottii species group (Teleostei: Cyprinodontidae). Occasional Papers Museum of Natural History, University of Kansas. 67: 1-31. WILEY E.O. 1978. The evolutionary species concept reconsidered. Systematic Zoology 27: 17-26. WILEY E.O. 1981. Phylogenetics. The Theory and Practice of Phylogenetic Systematics. Wiley-Interscience, New York, NY. WILEY E.O. 1989. Kinds, individuals, and theories. In Ruse M. (ed.), What the Philosophy of Biology? Kluwer Academic Publ., Dordrecht, The Netherlands, pp. 289-300. WILEY E.O. & D.D. HALL. 1975. Fundulus blariae, a new species of the Fundulus nottii complex. American Museum Novitates 2577: 1-14. WOOD R.M., & R.L. MAYDEN. 1993. Systematics of the Etheostoma jordani species group (Teleostei: Percidae), with descriptions of three new species. Bulletin of the Alabama Museum of Natural History 16: 29-44.


A. Legakis, S. Sfenthourakis, R. Polymeni & M. Thessalou-Legaki (eds.) Aristotle: DescriptorThe Animalium Princeps! New Panorama of Animal Evolution Proc. 18th Int. Congr. Zoology, pp. 19-25, 2003

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Aristotle: Descriptor Animalium Princeps! J. St. J. S. Buckeridge Earth & Oceanic Sciences Research Centre, Auckland University of Technology, P.O. Box 92006, Auckland, New Zealand. E-mail: [email protected]

Abstract Aristotle’s “formative world” was dominated by Platonic dogma, in which reality was perceived as an entirely transcendent and immaterial realm of ideal entities. Aristotle’s challenge of this was total and enduring: He replaced Plato’s ideals with concrete reality, empirical veracity and a world of independent substances defined by qualities. A lifelong fascination and wonderment of nature, combined with his “New World view” paradigm, led to Aristotle’s establishment of the foundations of modern zoology. Throughout his life, he was consumed with the “need to know”. This lead to his developing the elements of a zoological classification, which, although paying some regard to physical differences between organisms, is more a consideration of animal behaviour. Aristotle’s prime aim was not to develop a tidy systematic taxonomy; rather, he constructed a system through which he could ascertain the causes of observed phenomena. A pre-occupation with causes lead Aristotle to base his classification of animals upon reproduction, with the highest level of organisms, the internally viviparous, closest to perfection. Although this aspect of his work is less palatable to modern zoologists, we should view Aristotle’s extraordinary advances in heredity and animal reproduction in light of the intellectual and technical resources available to him. It is appropriate then, to conclude that Aristotle was “Descriptor Animalium Princeps” - the founder of modern zoology, and arguably the greatest biologist of all time. Today’s re-evaluation of phylogeny, on the basis of DNA, necessitates an even greater paradigm shift than that from Aristotle’s causal classification to one of systematic taxonomy. However, we must not forget the extraordinary variety of nature. And this, in twentyfirst century terms, is perhaps Aristotle’s great legacy: an imperative to adopt a sustainable stewardship of nature, so that future generations can, with wonderment, enjoy the beauty and richness of the earth’s biodiversity.

Introduction Aristotle was born in 384 B.C. at Stageira, a small Greek settlement in Chalkidiki. The state of Chalkidiki lay at the north-east end of the Aegean Sea, adjacent to Macedonia,

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into which it was absorbed in 348 B.C. (Hammond 1986). The Greek States, each of which previously had jealously guarded its individual autonomy, were soon about to become part of an empire that would extend from the western Mediterranean to India. It was a time of expansion – military, politically and intellectually. Aristotle was to play a significant part in this, for in 343 B.C., Philip of Macedon appointed him to tutor his young son, Alexander, (the future Alexander the Great). The personal relationship between Aristotle and Alexander is uncertain, especially in later years, although Hammond (loc. cit.), contends that Aristotle was responsible for the instilling of a love for Greek culture, daring speculation and amazing versatility in Alexander during his formative years. According to Novikov (1998), the friendly relationship between Alexander and Aristotle was eventually destroyed by “court conspiracies”. None-theless, Alexander and Philip acknowledged their great debt to Aristotle by richly rewarding him, and rebuilding the ruined settlement of Stageira. Of particular significance for the advancement of early science was Alexander’s endowment of a great library for Aristotle. Further, during his eastern campaigns, he permitted the collection of a large amount of materials and data for Aristotle and his students. Philip’s choice of tutor to his son clearly confirms Aristotle’s pre-eminence as one of the great thinkers and teachers of his time. But Aristotle was not an intellectual island; rather, his education was part of a pedagogic continuum that can at least be extended back to Socrates. Although Aristotle’s father was a learned man and could have been expected to influence his son’s education (he was court physician to Amyntas II, father of Philip), he died when Aristotle was still a child. The most significant teacher then, was Plato, a student of Socrates. In 368 B.C., a seventeen-year-old Aristotle entered Plato’s Academy in Athens. He was to remain a member of the Academy for 20 years, until the death of Plato in 348 BC, at which time he went to live in a small Greek state in Asia Minor near the island of Lesvos. According to Singer (1959), the following five years were pivotal in the formulation of Aristotle’s ideas of zoology, as he had both sufficient time for study and an ideal natural environment in which to undertake it. In 336 BC, following the assassination of Philip and the accession of his pupil Alexander to the throne of Macedon, Aristotle returned to Athens, and established his own school, the Lyceum. Here, in a garden setting, near a temple to Apollo (Lykeios = light-bearing, an epithet of Apollo), a peripatetic Aristotle was to teach and research philosophy for a further fourteen years. He left his beloved Lyceum, and Athens in 322 BC, shortly after the death of Alexander, and died in the following year, aged 63 years. There are two distinct foci within Aristotle’s scientific works: one toward an understanding of the physical universe, the other toward biology. Interestingly it was the former that, until the sixteenth century, formed the basis of man’s understanding of the cosmos; whilst the latter, for two millennia, was largely ignored. Today, Aristotle’s geo-centric model of the cosmos is rarely discussed, except as an historical curiosity, whilst there is increasing interest in his biological works, which still demonstrate a keen appreciation of natural systems. Although Aristotle’s legacy to science is extraordinarily broad, it is to biology, especially zoology, that he contributed most. His curiosity and wonderment of the natural world endures, and is emulated by those of us who have inherited his passion and perspective of the natural sciences:

Aristotle: Descriptor Animalium Princeps!

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“Εν πασι τοιζ ϕυσιχοιζ ενεστι τι θαυµαστον” In all the things of Nature, there is something marvellous. [Parts of Animals, 645a: 16.]

After Aristotle’s death, his library and works were collected and concealed in a cellar in Asia Minor. They remained there until the first century BC, when they were reassembled and edited by Andronicus of Rhodes. Our current knowledge of Aristotle is based upon Andronicus’ edition. Aristotle’s Intellectual Inheritance The Classical Greek Intellectual Environment: Although Aristotle lacked the physical accoutrements that one could anticipate in a modern zoological laboratory, his intellectual environment was none-the-less impressive, as contemporary Greek thought was very much focussed by a desire to understand the forms and functions of nature. There were distractions, such as the Pluralists (e.g. Empedocles, c. 493-433 BC), who saw matter as comprising four “elements”: fire, air, water and earth, and the Eleatics (e.g. Parmenides c. 475 BC), who perceived reality as “single and changeless”. Interestingly, it does not appear that philosophies such as these particularly hindered Aristotle’s understanding of zoological science. A very compelling intellectual environment existed however, for Aristotle during his “formative years” – a time when he was tutored by Plato. For Plato, and his teacher, Socrates, were very much opposed to research into nature. Rather, the focus of their study was the behaviour of man, particularly the determination of the nature of an individual’s actions, which upon death, would ensure that the soul returned to heaven. The methodology employed by both Socrates and Plato was the dialectic, a process in which analytical discussion through criticism is used to pursue knowledge. This, rather than any pre-occupation with nature, is the legacy of Socrates and Plato to Aristotle, as the dialectic established a platform for the development of science. Rationalism and Empiricism: Plato’s basic philosophical perception was that the ultimate reality lay in the world of intelligence, i.e. in “ideas”. He perceived great inspiration in mathematics, especially in the field of geometry, where the certainty of geometry was likened to timeless perfection. Plato’s pre-occupation with mathematics was anathema to Aristotle, who contended that perfect forms were of no use as models for living organisms, or the processes operating within them. Aristotle asks the following, which succinctly states the limitations of mathematics in understanding the natural world: … indeed one might ask this question, ... why a boy may become a mathematician, but not a wise man or a natural scientist. It is because the objects of mathematics exist by abstraction, while the first principles of these other subjects come from experience. [Nichomachean Ethics 9. 1142a: 16-19]

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Experience, based upon observations of natural phenomena, followed by deliberation of any interpretations, was the way that Aristotle saw as best leading to an understanding of nature. Aristotle’s perspective was that ideas could not exist separate from their physical embodiment. Rather, all things possess a striving to attain their telos, or true nature. The mechanism through which the Greeks believed teleology was achieved was through a mystical vitalism. Interestingly, although modern science dismisses the vitalism concept, there is still no broadly accepted theory as to the nature or essence of “living”. Plato was a rationalist, in the sense that reason, derived from the dialectic, is the foundation of certainty in knowledge. Although Aristotle inherited aspects of this, he was able to lay the foundations of empirical science: where understanding is based upon observation, in which reality is defined within the world of perceptible concrete objects, and where the real world is one of independent substances, each characterised by qualities. Thus Aristotle’s emphasis was on form and function, through which he attempted to define the fundamental nature of an object. Our modern concept of empiricism is firmly founded in both observation and experimentation. It is perhaps a little surprising then, that Aristotle himself did not develop the art of experimentation. None-the-less, he did provide the framework for it, as Strato, one of his successors, and head of the Lyceum in Athens, became the first to establish an experimental technique (Checkland 1993). Tutor and student: There are indeed great differences in the philosophies of Plato and his student, Aristotle. It is a testament to the compassion and vision of Plato that this was achievable, and a testament to the tenacity and originality of Aristotle, that an intellectual transformation that was to last two millennia, was achieved in one lifetime. One of the most informative images of the relationship between them can be gained from the painting, Stanza della Segnatura : La Scuola d’Atene, by Raphael, painted between 1509-1511. In the fresco, Plato stands pointing heavenward (i.e. to the One), while Aristotle gesticulates downward, with his fingers splayed, he is thus focussed upon the earth – the diversity of life and the demands that the material world makes upon us. Aristotle and Nature Aristotle’s primary objective was to understand the “nature of nature”. His perception of nature was an almost imperceptible, but continuous growth and development towards perfection (in form). In order to achieve this understanding he recognised two fundamental postulates: that nature is changing, and that nature can be classified. His approach was thus systematic, and it is this that places him as first zoologist in the modern genre. Pangenesis: Aristotle was responsible for a singular leap in the understanding of how organisms replicate. Philosophers such as Hippocrates, who had formulated the theory of pangenenis, were of the opinion that the means by which heredity functioned was located within all parts of the body (hence pangenis). In this sense, Hippocrates and his adherents believed that form was derived from the existing organism. Aristotle demolishes pangenesis elegantly, with the example of a two-legged child born of a onelegged warrior. He was adamant that the process of inheritance involved a “potentiality


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to develop”, and that every substance possesses a form, and is possessed by a form. In this, he is remarkably close to how we currently view heredity. Systematics: Aristotle considered that it was not possible to develop a systematic classification on the basis of physical differences, as many characters do not appear to be exclusive to one group. e.g. the possession of a placenta, a characteristic of mammals, is not restricted to the mammals. Aristotle describes a selachian (now known as the “placental dogfish”, Mustelus laevis), that was both vivaparous and had what he perceived to be a placenta. Importantly, he did not place this fish with the mammals, as other characteristics, especially behaviour of the fish, clearly placed it amongst the sharks. This example is significant in that it illustrates the importance Aristotle placed on observation. Singer (1959) points out that most naturalists dismissed the possibility of a “placental dogfish”, and that it was not until the nineteenth century that the German biologist Johannes Müller proved that Aristotle had been correct. None-the-less, Aristotle did group animals, although not in a formal systematic way. By grouping animals that possessed characters that were commonly found in combination, he believed that he would be able to ascertain the causes of observed phenomena. This pre-occupation with causes led him to group animals on the basis of their methods of reproduction, with the highest level of organisms, the vivapara, closest to perfection. Evolution: Aristotle was not in the strict sense an “evolutionist”, although some (e.g. Singer, 1959), believed he may have become one if he had lived another decade. What Aristotle did achieve in determining the relationships between organisms is remarkable, and serves as a first step in defining an evolutionary framework. He concluded that living things could be arranged in a Scala Naturae (i.e. a “ladder of nature”), of ascending worth and complexity, in which grades within the hierarchy are not rigorously separated (Fig. 1). It is important to note however, that the Scala Naturae is not “taxonomic”, nor Man Mammals Cetaceans Reptiles & Fish Cephalopods Crustaceans Insects Molluscs Medusoids Zoophytes Ascidians Sponges

Inanimate Matter Fig. 1. The “Scala Naturae”, demonstrating how nature proceeds gradually and imperceptibly from things lifeless to animal life. Based on the books of Aristotle. (After Singer 1941, Barnes 1982).

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was it intended to be. Rather, the groups were divided on the basis of “movements”. As one drops down the scala, there is a progressive weakening of movements, and a commensurate reduction in the nature of the soul. Man was perceived as the closest to “perfection”, as he possessed the highest form of soul (i.e. a rational soul). Inanimate matter by contrast, could not move of its own accord, and of course it possessed no soul. Zoology as a “working science”: The greatest impediment to understanding nature would be a lack of a formal nomenclature to describe the features, behaviour and organisms under study. Aristotle’s nomenclature was well developed, sufficiently so to permit reconstruction of many of his diagrams (the originals no longer exist), e.g. the mammalian generative and urinary systems described in History of Animals, have been reproduced in Singer (1959). Aristotle’s descriptions confirm that he had a very good appreciation of form and function, and this is demonstrated over a wide range of taxa, including cephalopods, teleosts, sharks and cetaceans. Indeed, in Parts of Animals, he uses the term “genus” and “species” (genos and eidos), in a similar manner to that of the present. It is appropriate then, to give credit to Aristotle for development of two key areas of science: scientific illustration and a sophisticated scientific nomenclature. Without these, zoology could not be a “working science”. Epilogue The current pre-occupation and “narrow” focus of many modern zoologists is clearly at the molecular level. This necessitates an emphasis on the geometric disposition of certain protein and carbohydrate groups, rather than a quest to understand relationships through form and function. Perhaps we are in danger, through reductio ad absurdum, of failing to understand the real picture. We should be mindful of Aristotle who concluded [Nichomachean Ethics 9. 1142a], that mastery of natural science is best achieved though wisdom (and experience), rather than by abstraction, (through which he perceived the path to mathematical competence to be achievable). Acknowledgements I thank Emeritus Professor John Morton, Castor Bay, Auckland, for encouragement and thoughtful advice during the preparation of the manuscript. Financial support to attend the XVIII (New) Congress of Zoology was provided by a grant from the Deputy Vice Chancellor’s Discretionary Fund, Auckland University of Technology, New Zealand. References Note: Apart from quotes from Nichomachean Ethics, which are cited as such, references to Aristotle’s works have been taken from selected translations provided in Ackrill, and McKeon. These two texts are listed below, but the works are cited in the text using the well-established numbering system for Aristotle’s work.


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ARISTOTLE 1985. Nichomachean Ethics. Transl. T. Irwin. Hackett Publishing, Indianapolis, 441 pp. ARISTOTLE 1987. A New Aristotle Reader. Ed. by J.L. Ackrill. Princeton University Press, New Jersey, 580 pp. BARNES J. 1982. Aristotle. Oxford University Press, Oxford, 101 pp. CHECKLAND P.B. 1993. Systems Thinking, Systems Practice. John Wiley and Sons, Chichester, 330 pp. HAMMOND N.G.L. 1986. A History of Greece to 332 B.C. 3rd Edition. Oxford University Press, Oxford, 691 pp. McKEON R. 1992 (ed.). Introduction to Aristotle. Modern Library Edition, Random House, New York, 712 pp. NOVIKOV I.D. 1998. The River of Time. Transl. from Russian by V. Kisin. Cambridge University Press, Cambridge, 275 pp. SINGER C. 1941. A Short History of Science to the Nineteenth Century. Dover Publications, Mineola, New York, 399 pp. SINGER C. 1959. A History of Biology to About the Year 1900. A General Introduction to the Study of Living Things. 3rd Revised Edition. Abelard-Schuman, London, 580 pp.

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A. Legakis, S. Sfenthourakis, R. Polymeni & M. Thessalou-Legaki (eds.) Aristotle: DescriptorThe Animalium Princeps! New Panorama of Animal Evolution Proc. 18th Int. Congr. Zoology, pp. 27-39, 2003

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The Persistent Progression: a New View on Animal Evolution F.D. Por Hebrew University of Jerusalem, 91904 Jerusalem, Israel. E-mail: [email protected]

Abstract Animal evolution is seen today through the dilemma of two reigning views. The first sees animal evolution as a shallow sequence of contingent accidents and catastrophic extinctions. The second, accepting a progressive trend in this evolution, sees a hidden vitalistic or deistic force at work. I propose a third way, which accepts progressivism, but considers it to be a historical consequence of directional dissipative thermodynamic processes which are acting on the globe. The animals have a crucial role in stimulating the gradual expansion of the biosphere and the increasingly efficient recycling within it. The different animal phyla, irreversibly marked by their morpho-physiological signatures are the selective and selected players in this process. The terrestrial environment, once colonised, provided for maximum biomass and highest animal efficiency and complexity. The thermoregulating vertebrates and among them the human species selected out as the recent culmination of this evolution.

Introduction Zoologists looking at the animal world parented the idea of Evolution seen as a structural unfolding of life in time. Aristotle, the father of zoology was also the first evolutionist, as he wrote ‘Nature proceeds from the inanimate to the animal in small steps... a continuity (συνεχεια)”. At the “Darwin Centenary” XVth International Congress of Zoology in London (1958), Julian Huxley said in his keynote lecture that evolution is a progressive ‘natural process of irreversible change, which generates novelty, variety and increase of organisation’ (Huxley 1959). By a strange historical twist, half a century later, the scions of Neo-Darwinism of which Huxley was one of the founders, consistently oppose the idea of progressive evolution in the animal kingdom. All animal species and even all beings are ‘equally evolved’ (Margulis 1998) since the only objective value criterion is selective success. As a consequence of the reigning reductionism, all beings are ‘organisms’ on an equal footing, from bacteria to elephants, and they represent only different strategies to succeed in the struggle for existence. Modern biology seems to ignore the need for a theory of Zoology

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that tries to explain the evolutionary sequence from unicellular to multi-cellular animal organisms, followed by the appearance of animals with complex structure and complicated behaviour and lately by the appearance of the human species. Deprived of any qualitative dimension, evolution as seen by many today, is nothing more than shallow transformism. Evolution is presented by the reigning view as a sequence of sudden (‘punctuated’) aleatory modifications, the products of which are reshuffled again and again by equally unforeseeable and sudden mass-extinction events, primarily of extra-terrestrial causation. This doctrine of saltations and of contingent catastrophes is opposed to Darwinian uniformitarianism and actualism. It is a neo-catastrophism masterly popularised in the many writings of S.J. Gould (1995 and passim). The zoological community has been strangely silent in face of these ideological positions that have invaded all the media of popularisation. Today, as the relationship between humans and the rest of the biosphere is of wide interest and extreme acuity, it has to be openly debated whether humanity is an accidental, ephemeral, and even deleterious side-product of evolution, soon to disappear, or on the contrary, a natural, logical and irreversible result of it. Unfortunately also, a concept of transformism caused by contingency alone, makes a singularly poor argument against the recent aggressive rise of creationism. Fitful and stray transformism is philosophically primitive, perhaps on equal footing with creationism. An alternative theory of animal evolution, which has been published in extenso (Por 1994), is succinctly presented here. Animal evolution is seen as a predictable, persistent process that is progressively channelled. In this view the humans represent a natural consequence of organic evolution. The conflict between the two views of extremely relevant philosophical and operative significance ought to be solved in the field of zoology alone. The result should be a unifying theory of zoology, consistent with a general theory of cosmic and global evolution, without having to take recourse to idealistic and vitalistic concepts. Evolutionary irreversibility and channelling The biosphere is an open, dissipative thermodynamic system in the sense of Prigogine. It operates with the external source of solar energy, and with the thermal sink is the surrounding space. Like other such systems and within the given constraints, the biosphere evolved away from an original high entropy state of structural simplicity. Progressive animal evolution is a consequent stage in this evolution, which previously led already to the organisation of living matter, and in sequence to the raise of the eukaryotic cell. With each step, more energy expending structures evolved and the information content in each new system increased. The emergence of the complex animal organisms led to an increase of the energy greed per unit by several orders of magnitude. Being part of a global progressive thermodynamic dissipative process, progressive animal evolution can be called, with some reserve, a ‘telematic’ process in the sense of Mayr’s (1974) terminology. The whole process has been channelled by natural selection already from the biochemical level. Left-handed amino acids were selected and the four-nucleotide bases

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of the genetic code were chosen among the many of them. Some time in the late Proterozoic, the photosynthesising RuBISCo enzyme of the green plants became globally predominant. Although fairly inefficient, it has been never surpassed. Likewise the basic energy storage and exchange phospho-nucleotide molecule ATP was selected. Its energycarrying capacity is the official tender of the living world. This singled-out twosome of the energy fixing and of the energy-storing molecules, constitutes the constraining mould which delimited all further biological evolution. At each organic level, evolution proceeds in a roughly similar way. New mutations undergo testing in the selective natural environments. The selected solution, often the best available at that time, becomes irreversibly fixed, limits the contingent liberty of future mutations and hence canalises the consequent evolutionary process. This is a somewhat expanded rendering of the well-known Dollo’s Law. Like in a game of chess, each evolutionary step is a move which cannot be taken back and which inevitably influences the whole sequence of the game. The Biosphere and Global Evolution During its existence, the biosphere was exposed to an increase of more than 30% in solar irradiation, as our central star advanced in its own predetermined stellar evolution. Had the biosphere not been able to buffer this increase, the result would have been a thermal death in an overheated atmosphere, perhaps similar to our sister planet Venus. By the end of the Proterozoic the active tectonism of continental accretion was nearly completed and on the mature globe a new phase of plate-tectonic shifting of the existing continents started instead. Around and on the stable established continents, biological evolution could gain continuity and momentum. This has been probably impossible in the times of the ‘peristable’ Archean micro-continents. Biological evolution has been a follow-up of a necessary tectonic evolution. At the end of the Varangerian, after a last phase of global volcanic paroxysm, the atmospheric CO2 concentration stood probably at some 350 times the present value. In the following the dominant process started to be the gradual extraction of CO2 through fixation of reduced carbon by the expanding volume of global organic biomass. This ‘ice house’ process has been probably essential in balancing the impact of the further increase in radiation and maintained global temperatures for the last 600 million years within limits compatible with multicellular life. The atmosphere maintained a ‘complex equilibrium (between) the production of Oxygen from CO2 by plants and regeneration of CO2 by respiration of animals’ (Brown & Mussett 1981). This is the basic ‘Gaian’ feedback process of Lovelock. Since the limits of biochemical efficiency are irreversibly set, the progressive accumulation of live biomass and of other forms of biologically reduced carbon could proceed only along two avenues of liberty. Firstly, the vegetation expanded to the whole global surface. Secondly, the processes of recycling and renewal of biological fixation by the plants was accelerated, refined and globalised. In both these processes the activity of animal organisms has been essential. As a result the global energy capturing green cover grew in extension and the total volume of the energy flow increased.

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The Age of the Animals Among the kingdoms of the living organisms, Kingdom Animalia contains and contained by far the largest number of species. This seems to be paradoxical, since the biosphere existed for most of its history without the presence of animal organisms and functioned only through the simple linear cycle of prokaryotic producers and prokaryotic decomposers. The animal organisms, which appeared in the last billion years, added an apparent complication to the cycle, by interposing different levels of consumers and various links in the food chain. To some, the exuberant flourishing of the animal world is an unnecessary ‘little blimp’ on the body of the laborious producers and decomposers and the biosphere could have gone along quiet well without them (Gould 1996). However, in fact, reprocessing of the organic product through a complicated food web of hungry consumers is much more efficient than the old linear cycle. Unlike bacteria and fungi, which mainly feed on dead organic matter, the animals are killing, engulfing and digesting their food organisms alive and without delay. Moreover, they are generally highly motile organisms, which detect and approach their prey, actively spanning distances unheard of by plants, fungi and bacteria. Some aquatic animals developed advanced techniques to trap suspended food particles. The complicated multi-level food webs ensure that little of the organic production is being lost unrecycled. The big diversity of the animal organisms corresponds to as many channels of recycling specific food items, everywhere in space and during all the time. Feeding on live prey includes all the food objects, from bacteria to plants and of course to other animals. I called animal activity in all its varied facets ‘harpactic activity’ (from the Greek ‘Harpagein’). Darwinian fight for survival and natural selection gained a dramatic and rich content with the rise of the animals. A colony of unicells cannot allow itself to become senescent; it has to maintain a logarithmic growth in order to replace predatory loss. Rapid growth in order to replace the losses and increased body mass of the prey organisms became widespread means of defence. Suddenly, the biological world became replete also with physical and chemical defence devices, rapidly improving in response to the improving performance of the predatory animals. A seemingly endless chain of positive feedback effects resulted in what Vermeij (1987) aptly called ‘escalation’. Over time, action and reaction became more and more rapid and complex and reached the present breathtaking speeds. Gradually also, the behavioural means became more important in this race. The importance of the animals as promoters of bacterial decomposition cannot be estimated enough. On the large extents of the oceanic bottoms they facilitated decomposition, by digging after the dead organic mater in the marine sediments and liberating carbon dioxide. In the continental soils animal reworking results also in massive CO2 restitution to the atmosphere. A runaway depletion of carbon in the atmosphere is being probably balanced by harpactic activity. Due to harpactic activity metabolic rates increased in the organisms over time (Maiorana & Van Vallen 1990) and there has been an increase in per capita energy use, a stepwise economic expansion of the multicellular animals (Vermeij 1987).


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Expansion as an escape Harpactic activity has been most probably the main stimulus for the expansion of the biosphere. One of the most frequent ways to avoid predatory pressure has always been the escape to novel and more extreme environments, out of the reach of the predators. Temporary escape from predation compensated for the extra metabolic cost required by the unfamiliar environment. But the animal consumers always follow after some delay and the same cycle of predation and defence and of escape starts again. One can rightly suspect that without the incentive of escaping predation, there would have been no expansions of the biosphere from the marginal belts of the coastal shallows to a recent almost complete global covering. With the appearance of the animals in the Phanerozoic, diversity, mode and tempo of biotic evolution entered in a qualitatively new phase. The brackish waters, the first to be colonised by the expanding marine biota have probably always been the most productive environments. The continents themselves rapidly turned to be extremely productive. Today they produce 3 times more organic matter than the seas, although they represent proportionally much less than half of the oceanic cover of the globe. As plant production flourished, animals found ample food resources in the estuaries and on land for their complicate and costly functions and structures. In their turn, they facilitate renewed production. Progressive Animality Lotka (1922) wrote: ‘Evolution proceeds in such direction as to make the total energy flux through the system a maximum compatible with the constraints’. It is the animals that turned the modern biosphere into an interwoven global system of energy fluxes. The higher an animal consumer is situated in the food chain or food pyramid, the more mobile, the more sensorial alert it is, the more space it covers in search of its prey Some oceanic fish migrate from shore to shore. Migrating birds visit seasonally, ecosystems situated at the antipodes. The essence of animality in the biospheric context is aggressive consumption of live organisms, sensory capacity to detect the food resources, mechanical means to approach the prey and liberty to move among different environments in search for food. Improvement in these capacities is the yardstick of progressive animal evolution. The trend to progressively improve ‘animality’ is however far from universal in the animal kingdom. It is not a broad front in which all the animal types participate. The critics of progressivism often imply universality of progress, a zoological ‘orthogenesis’, for the sole purpose of knocking it down. Neither is progress in the animal kingdom, as also often assumed, a relay race in which each phylum hands the torch to the following one, a modern replay of the classical Aristotelian scale of life. Many branches of the animal world diverged into specialised side alleys, for instance progressively improving adaptation to sedentary or to parasitic life styles. To use another athletic comparison, progress in the animal world resembles more a cross-country marathon race in which a whole crowd starts out and gradually, as most of the participants remain behind or leave the race, the leaders run in a single thin and distanced file.

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Phyletic Selection The runners in the race are the phyla and the classes of the animal kingdom. Every phylum or class is defined by a set of irreversibly fixed physiological and morphological properties. These represent the ‘Bauplan’ of each of these major taxonomic units. The 35 animal phyla exist since at least the early Cambrian. Classes within them have been defined later. Each and every animal species bears the limitations and freedoms of the phylum or class to which it belongs. Therefore the individual success or failure of the totality of the component species is summing-up as the success or the failure of the phylum. As a result, natural selections acts also at the level of the phyla, provided of course, that the phylum as we define it, is a monophyletic natural unit. Every echinoderm is invariably penta-radial. No flatworm ever developed a skeleton and all are limited to gliding movement. All the nematodes are structurally obliged to move on a wet substrate and therefore cannot live in the plankton. Five phyla and several classes, with all their multitude of species are irreversibly condemned to sedentary life. So are the countless species of the parasitic phyla and classes. It results that natural selection does not play its hand with jolly jokers or wildcat cards, but only with a limited set of cards, which belong to a certain suite and colour. In the Cambrian shallow sea environments, all the 35 phyla were represented by a relatively low number of species each. As life branched-out into the different environments and evolutionary history proceeded, many of the phyla remained confined to the oceanic waters and several of them saw their diversity reduced to a handful of species. On the contrary, three phyla, namely the Mollusca, Arthropoda and Chordata, with their classes, expanded over all the environments of metazoan life and showed a disproportionate increase in species numbers. On their account, also parasites, Platyhelminthes, Nematoda and several classes of ‘Protozoa’ (see below) have achieved hyper-diversity. The top-heavy emergence of these few privileged hyper-diverse phyla is one of the most significant results of the Phanerozoic animal evolution. These phyla were selected out of the many because of the elements of adaptive freedom of their Bauplans. Natural selection acts day-by day at the level of the species. Phyletic selection acts cumulatively over long periods of time and especially in the critical time-periods, called ‘global extinctions’ by the neocatastrophists, when legions of species of a phylum are being felled. The Osmotic Hurdle Expansion into brackish-estuarine and fresh inland waters required adaptation to low, fluctuating and unpredictable salinities. To achieve this, the animals had to secure the osmotic hoemostasis of their internal liquid milieu. Many phyla and classes of marine animals, such as the corals, the echinoderms, the brachiopods, the cephalopods and the sea squirts are stenohaline, fundamentally unable to osmoregulate. Most of the animal phyla remained in fact confined to the seas. Only the good osmoregulators, different phyla of worms, the crustaceans and arachnids, the shells and the snails and most of the fish classes could produce species able colonise the estuaries and in the following also the fresh waters. The high biological productivity of the land-locked waters amply


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compensates for the considerable metabolic costs of osmoregulation. The stenohaline marine phyla confined to the oceans live on the contrary, in an oligotrophic, nutrient poor environment, albeit much less energy-demanding. The capacity to osmoregulate has been a long-term asset also in the marine environment, since seawater has a stable high salinity and a buffered temperature, at least on the secular scale. But during critical periods of the tectonic history of the globe, oceanic salinity and temperatures fluctuated sharply and even dissolved oxygen could be at times deficient. Though extra-terrestrial factors, such as massive meteorite falls possibly joined in, the crisis periods were nothing but rare instances of congruence of extreme fluctuations in several earthly, tellurian environmental factors at once. With the exception of the below-mentioned demise of the dinosaurs, the catastrophes of the neo-catastrophists have been all reported as impacting the marine biota. Phyla unable to osmoregulate were severely castigated and many of their classes extinguished. The frequent near-extinctions suffered for example by the echinoderms and by the cephalopods, were due to the fact that all of their species are strictly stenohaline. The coral reef taxa both stenohaline and stenothermic were also gravely touched and it sometimes took millions of years before they could recover. Euryhaline phyla could always survive fluctuations of marine salinity and temperature in refugia of semi-secluded marginal environments. As a matter of fact the dominant euryhaline phyla emerged hardened from each global crisis. Unlike Russian roulettes in which the rule of natural selection was suddenly suspended and replaced by the rule of sheer chance (see for instance Eldredge 1999), the crisis times have been the major events of phyletic selection in the oceans. Into the Open Air Only mobile and osmoregulating animals could emerge onto the dry land. Moreover, only animals that could not keep their body fluids protected against evaporative loss, animals that developed homeohydric capacity, could leave the protection of the wet soils. A watertight body cover and a water-saving excretion were needed for this. Out in the open, also a skeleton was essential to oppose gravity, to withstand the blowing winds and to serve as a lever for efficient movement. Only the class of the gastropods, the arthropods and the vertebrates could colonise open land. However, the snails use their external conch only as a protection against exsiccation, and not as a lever for their musculature. When moving, they have to extend and creep flatworm-like, loosing big amounts of water. It is understandable that the gastropods remained by and large marginal players in the terrestrial ecosystems. Two phyla, the arthropods and the vertebrates remained in the race, capable of using all the rich vegetal biomass that developed on land since the Carboniferous. They could take also unlimited use of the free plentiful oxygen for the full respiratory use of the ingested food. Unlike their aquatic ancestors who had often to face oligotrophic conditions and lack of dissolved oxygen for their respiratory metabolism, the land animals had all the food resources needed in order to develop extremes of energy dissipative complexity. The most dramatic and extreme chapters in animal evolution, both in terms of complexity as well as functional and behavioural achievements could have happened only on land.

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A Constrained Host It seems paradoxical to assert that despite their hyper-diversity of many millions of species presently living; the arthropods have had their own dramatic limitations in the progressive evolutionary race and in phyletic selection. Their armour-like exoskeleton has to be shed periodically and in their inter-moult periods the soft-skinned arthropods are exposed to predation and to water loss. Small body size was required for better hiding in these critical periods. Among the three great arthropod classes, the crustaceans never fully adapted to terrestrial life, because of functional shortcomings of their own. The arachnids and the insects developed good aerial respiration, a watertight epicuticle and water-saving purine-based excretion. However the arachnids remained morphologically restrained to predatory life. The tracheal system for air breathing, which the insects developed to maximum efficiency, is not a centralised respiratory system. Above a certain critical body mass, oxygen supply is impossible for the muscles, which exclusively need full aerobic conditions. The diffuse tracheal system ‘replaced’ also a proper circulatory system and functional decentralisation characterises the insect body functions. A further premium for small size was set with the appearance of the agile raptorial reptiles in the Permian. As a consequence, the advanced insects specialise in miniaturisation. Owing to some not fully elucidated constraints, insects colonised the high seas only in a few exceptional cases. Vertebrate Primacy The vertebrates were thus left in the cross-country marathon of progressive evolution towards the highest complexity and animal efficiency. They probably displayed right from the beginning a morpho-physiological type with the minimal set of constraints, with maximal liberty to adapt to the requirements of the biotic and abiotic media. The success of the vertebrates could have been foreseen right from the beginning, among others because of the possession of the multiple HOX gene sets. Gould (1989) speculated that the presence in the Cambrian Burgess shale of only one isolated chordate, Pikaia, is a proof that the future success of the vertebrates was pure contingency. Lately, chordate remnants were found much more in abundance in the older Chenjian site and the widespread Cambrian fossil conodont animals have been also identified recently as chordates. In the Silurian the jawed fishes, some of them gigantic, already dominated the seas. In a continuous sequence, uninterrupted by the extinction events, their descendants, the bony fishes and other vertebrates are today the masters of the aquatic world. Subservience It is often and rightly being asked, why the vertebrates are ‘chauvinistically’ singledout, when there are so many more species in other phyla, notably among the arthropods and the nematodes. The large hosts of these animals are mostly subservient to the higher terrestrial vegetation and to the vertebrates. With increasing success, higher complexity


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and more refined homeostatic functions, the vertebrates turned into hosts and were exploited by many species of organic beings, starting with the bacteria. The fact that there are today many more bacteria and other simple organisms than at the start of the Phanerozoic is not a proof that evolution is not progressive (Gould 1996). Quite on the contrary, the recent huge diversity of these organisms depends on the existence of the advanced plants and animals. Without the opportunities created by the newfangled complex host organisms, the biosphere would still be dominated by a few conservative species of prokaryotes, as it has been during pre-Phanerozoic times (Schopf 1995). Among the Platyhelminthes, the Nematoda, and many classes of ‘Protozoa’, there are many more subservient parasitic species than free-living species. All of these depend on the more complex animal and vegetal organisms. Very much of the insect hyperdiversity is due to the relationship with the flowering plants. Several insect orders and many families are parasites and commensals of terrestrial vertebrates: blood-suckers, feather and hair eaters, nest parasites, dung eaters and even tear-lickers. Tens of thousands of mite and tick species are also subservients of vertebrates and higher plants. The geometric multiplication of the subservient phyla and classes on the expense of the relatively few highly organised top-organisms is another important evolutionary trend of the Phanerozoic times. It is worth mentioning that, baring a few picturesque exceptions, there are no parasites among the vertebrates. Hot Blood The sub-aerial environments, unlike the aquatic ones, are always prone to extreme temperature changes and fluctuations. The efficiency of the biochemical processes increases with body heat and low temperatures induce lethargy. Therefore homeothermy, at the highest possible temperature has been an important terrestrial adaptation. The homeothermic animals evolved to live a thermal brinkmanship at the highest tolerable temperatures, avoiding heat death, which starts soon above 400C. Many insects bask in the sun before taking to the wings. Bumblebees even conserve their muscle-generated body heat below an insulating fur-like body cover. But small size prevents insects from maintaining high temperatures for a prolonged time. Ectothermy, the technique of heating-up by basking in the sun was extensively used by the big reptiles of the Jurassic-Cretaceous times. This has been an exceptional and long period of about 70 million years with pole-to-pole high temperatures and very little seasonal fluctuations. Impressive body sizes were reached by the dinosaurs during this period, enabling them to maintain inertially the accumulated solar heat in their massive bodies over night and during the year-long summers. Fairly high and constant temperatures in the guts of the Mesozoic reptiles and later of the mammals promoted the establishment there of large colonies of cellulose-splitting bacteria and protists. This symbiotic relationship enabled the vertebrates to consume large quantities of vegetal cellulose, which they could not digest alone before. The stage was set for large-scale terrestrial herbivory. The joint processing of the terrestrial vegetal biomass by the vertebrate + bacteria couple opened an unlimited energy supply for the more and more energy-avid vertebrate organisms.

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Whereas the Mesozoic dinosaurs were diurnal sun-basking giants, in the nocturnal and shaded arboreal environments the forefathers of the birds and of the mammals developed active, endothermic thermoregulation. Towards the end of the Cretaceous, as world temperatures fell and the dry savannah forests were replaced by wet rainforests, spanning to the poles, the ‘dinosaur-strategy’ became anachronistic. In the cool and wet forests of the Paleocene, huge reptiles could neither move nor keep warm. They were on their way out even without the helping hand of a catastrophic meteorite impact. During the downward trend of world climate, which continues from the Eocene till now, only small ‘cold-blooded’ reptiles could survive on land, leading a life of alternative activity and of torpor. The turn of the endothermic vertebrates came. Birds and mammals rely on the heat produced by a variety of body functions, its conservation by an insulating plumage or pelt and, if needed, active means of avoiding overheating. Internal heat production needs massive feed since about 90% of their food intake dissipates as heat production. Endotherms are the most energy wasting and complex organisms ever to be produced. In compensation they are continuously foraging, often day and night and generally irrespective of climate changes. Jointly with their gut micro-organisms, they are the most efficient recyclers of vegetal biomass, and massive CO2 producers. The Behavioural Attribute To the dismay of the reductionists, only animals behave. Behaviour is a fundamental animal property and an advance in behavioural performance and complexity is perhaps the main indicator of animal progress. In most of the animal world, patterns of behaviour are innate, genetically transmitted functions of the central nervous system. Learning, memorising and horizontal experience transmissions, superposed on the innate behaviour, are the indices of the most advanced animals. The smallness of the insect brain and the consequent small number of neurons in their central nervous system limited the insects on the level of behavioural automatons. Each species represents one behavioural pattern. Perhaps herein lies another reason for their hyper-diversity. The insects escaped this limitation only in their complicated ‘multibrain’ societies. That learning and memorising is not an accidental attribute of the higher vertebrates, but exists in the potentiality of behavioural evolution itself, is shown by the fact that such capacities appeared independently also among the Cephalopoda, at the other end of the animal panorama. They are rightly considered to be the apex of invertebrate evolution. The cephalopods have very voluminous brains, extremely developed eyes, ‘manipulating’ tentacles, and their learning, discriminating and memorising capacities are competing with those of a mammal. They carry, however, the irreversibly limiting deficiency of their respiratory pigment, the haemocyanin. They could not avoid this basic shortcoming even though their circulatory system is anatomically more perfected than that of any vertebrate. Furthermore, the squids and octopuses are all stenohaline and limited to the relatively poor oceanic food supplies. Understandably all are also aggressive and nimble predators, perhaps the only real competitors the fish ever had.


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But their wound-up metabolism extracts its price: without any internal food reserves the cephalopods live one year or maximum two (except Nautilus, the living fossil). The wisest octopus cannot accumulate much experience and does not pass it on to its progeny. The Fettered Birds Back again to the vertebrates by the fiat of phyletic selection, we have to see in endothermy the major factor that promoted the functions of the brain in the birds and in the mammals. An internal medium of stable and optimal temperature enables the brain to accumulate memorised individual experience. The brains expand progressively in relation to the body size and this expansion, even taken with a grain of salt, is a good general measure for progressive vertebrate evolution. Memory build-up and exchange of experience within the group, weaning of the progeny became a new type of information transmission, superposed on the genetic one. Nothing likely can happen among the small cold-blooded reptiles, which as suggestively expressed, forget during the stupor of the cool nights what they experienced over day, not to speak of the long seasons of hibernation. Perhaps the dinosaurs, able to preserve their resilient sunlit body heat, were wiser. The birds and the mammals, representing two separate lines of reptile descendants, have achieved independently endothermy, by somewhat different but equifinal ways. This speaks again against the alleged orthogenesis of progressive evolution. On the contrary it proves that the same circumstances encourage parallel adaptations, wherever and whenever possible. Once again phyletic selection acted, and this time fated to turn the birds into an evolutionary dead end, even if a glorious one. Extreme adaptation to flight severely limited the birds. Flight limits their size to around 15 kg and all their anatomical structure is surrendered to the aerodynamic needs. Small heads, lack of dentition, reduced pneumatic skeleton, lack of manipulating fore limbs, all this are flightinduced. Although the metabolic energy production in the birds is higher than in the mammals, the lack of homeothermy of the nestlings is also a limiting aspect. The need of highenergy food limits birds to insectivorous, frugi- and granivorous or to outright nectar feeding. Besides perhaps the geese, no bird lives on heavy loads of slow-digesting leafy food. The average positioning of the birds in the terrestrial food chains is between that of the small insects and that of the large mammals. Both birds and mammals achieved high capacity of learning, again each through a different and morphological evolution of their brains. The bird forebrain developed a ‘neostriatum’ as site of the advanced co-ordinated behaviour. Unlike the mammalian neocortex, it is growing inwards and is space-limited. According to Allman (1999), the birds have only one stereotypic visual map and limited possibilities to change their stereotypic behaviour. Still they are champions in sound imitation. Human Primacy It is evident that from among the mammals it was the Primates, a very old Paleocene order that had the best preconditions to produce the first rational animal. Gould tries to

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make us believe that in the unlikely event of a reshuffling of the cards of animal evolution, the results would be completely unforeseen products. To the contrary, I believe that under similar gross environmental circumstances, the result can be again only a terrestrial endothermic vertebrate, perhaps even primate looking. The use of fire has been most important in human evolution. Of the most overwhelming importance has been the human cooking pot, which hydrolyses cellulose and prepares for human consumption the most refractory or poisonous vegetal materials. A unique and perfectly omnivorous animal machine was born. Humans became the only natural cosmopolite metazoan species ever to appear, when a baby was recently born even on the Antarctic continent. All the available sources of energy of the globe, biological and physical, are being gradually captured in the service of the human consumption. The soon 10 billion strong human population, represents the most complex and energy dissipating monospecific biomass ever produced. For better and for worse all the species of the globe fell under the subservient human bondage. The humans have selected out several tens of animal and several hundreds of plant species and turned them into new biological entities, cultigens, a kind of pseudospecies able to survive and flourish only under human care. Many of these are of a rare beauty, which competes with that of the ‘wild’ species. Continuing an old evolutionary story, unaccounted numbers of species from bacteria to mammals became subservient profiteers of the successful human population and of its anthropic environments. Out of them tens of thousands of species accompanied willy-nilly the humans and reached a cosmopolite distribution. With the emergence of the humans, the biosphere reached a new stage in its evolution, comparable to the other big steps, like the emergence of the eukaryotes or of the metazoans. True to their animal ascendancy, the humans have now almost completed the integration of the biosphere into a unique global supermarket. On a globe wide open to human agency, the whole evolutionary process has come to a near standstill. What is being called wildlife survives today only due to the varied degrees of human goodwill. Some natural speciation will still continue among the undesired camp followers, but the large sweep of evolution is over. This is a novel evolutionary stage, as irreversible as any other has been (Por 1996). Humanity is bound to produce, like each previous new stage, a breakthrough in the energy capture and transformation on the globe, both by transgenic increase in the primary production and by the liberation of new energy sources like hydrogen burning and ‘clean’ atomic fusion. To Gould (1996) the humans might be a small twig, a mere Christmas bauble on the tree of life. But in real time this twig came to overshadow the whole tree. The humans, the first and probably only rational species produced by evolution, will survive and dominate the globe until it will start to be engulfed by the red giant-turned sun. By than we shall have had already colonised space. References ALLMAN J.M. 1999. Evolving Brains. Scientific American Library, New York BROWN G.C.& A.E. MUSSETT 1981. The Inaccessible Earth. Unwin Hyman.


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ELDREDGE N. 1999. The Pattern of Evolution. Freeman and Co. New York GOULD S.J. 1989. Wonderful Life. The Burgess Shale and the Nature of History. Norton. GOULD S.J. 1995. Tempo and Mode in the Macroevolutionary Reconstruction of Darwinism. In Fitch W.M. & Ayala F.J. (eds), Tempo and Mode in Evolution. Genetics and Paleontology 50 Years after Simpson. National Academy Press, pp. 125-144. GOULD S.J. 1996. Full House. The Spread of Excellency from Plato to Darwin. Harmony Books. HUXLEY J. 1959. The Emergence of Darwinism. Inaugural Lecture. In Hewer H.R. & Riley N.D. (eds.), Proceedings of the XVth International Congress of Zoology. William Cowles, London. LOTKA A.J. 1922. Contribution to the energetics of evolution. Proceedings National Academy of Sciences 8:147-152. MAIORANA V.C. & L. VAN VALEN 1990. Energy and Community Evolution. In Dudley E.C. (ed.), The Unity of Evolutionary Biology. Dioscorides Press, pp. 655-665. MARGULIS L. 1998. The Symbiotic Planet. A New Look at Evolution. Phoenix Books. MAYR E. 1974. Teleological and Teleonomic: a new analysis. Boston Studies in the Philosopy of Sciences 14: 91-117. POR F.D. 1994. Animal Achievement. A Unifying Theory of Zoology. Balaban Publishers, Rehovot. POR F.D. 1996. Diversity, subservience and the future of evolution. Israel Journal of Zoology 24(2): 455-463. SCHOPF J.W. 1995. Disparate rates, differing fates. Tempo and mode of evolution changed from the Precambrian to the Phanerozoic. In Fitch W.M. & Ayala F.J. (eds.), Tempo and Mode of Evolution. Genetics and Paleontology 50 Years after Simpson. National Academy Press, pp. 41-61. VERMEIJ G.J. 1987. Evolution and Escalation. An Ecological History of Life. Princeton University Press.

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The New Paleontological Panorama

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Introduction: The new paleontological panorama 43 The New Panorama of Animal Evolution Proc. 18th Int. Congr. Zoology, pp. 43-44, 2003

Introduction: The new paleontological panorama J. Bergström Swedish Museum of Natural History, Stockholm, Sweden

Although not very clear from our daily newspapers, there is more to palaentology than finding even bigger or more horrible dinosaurs. The last decades have provided us with an unprecedented number of new lagerstätten, that is, occurrences of well-preserved fossils that can give exceptional glimpses of the morphology and construction of old forms of life. Fossil animals usually are represented only by biomineralized shells and skeletons, but in the variety of different kinds of lagerstätten also soft tissues can be found. The understanding of the fossilization processes is a science in its own. Quite a large proportion of the lagerstätten is from the Cambrian. This has the surprising result that some marine groups known from today but are virtually unknown from fossils through much of the last 500 million years can be retrieved from rocks some 500-540 million years old. Not only can we recognize them, but some of them yield surprising detail on the µm scale. We have now to realize that we can get information that would hardly be possible to get from the field of comparative morphology in zoology, or from genetics. An example is the new understanding of the arthropod coxa. It was thought to be the most proximal segment of the leg in all arthropods – but “orsten” material demonstrates how the coxa came into being first only in the crustacean lineage through the growth of a ring-shaped sclerite from a new endite where there was before only soft skin. A somewhat similar revolution occurred in vertebrates during the transition from fish to amphibian. Although the evolution from fin to leg is a classical textbook example of gradual evolution, even the most amphibian-like osteolepiform fish had fin rays where the first amphibian had fully developed digits. Evidence from developmental genetics shows that HoxD genes cause a 2-phase growth pattern in tetrapods, but only a single phase in fishes. Thus a genetic “invention” seems to have created the digits by “doubling” the bone formation procedure, and the digits are a completely new structure without any forerunner. Data squeeze this event into a 5 million year interval, which would be very short if only gradual evolution were involved, but time in excess for a genetic “invention”. It is not long ago that we learned that birds most probably evolved directly from dinosaurs. The oldest birds used to be a handful of specimens from Solnhofen in Germany. Recently, nicely preserved bird specimens in the oldest Cretaceous of China have been found in the order of a thousand. The Chinese deposits are also yielding small carnivorous

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dinosaurs with the skin covered by feathers. Thus, birds apparently inherited feathers from their ancestors and made a new use of them. In dinosaurs, feathers should have been for insulation and display. Ultimately, one paper provides an example of the more broad-scaled faunal analyses that can be done as data are accumulating. This gives us new possibilities to understand how communities were composed and how they evolved. The example is taken from mammal faunas in Eurasia during pre-glacial times, thus in times with great changes in climate and vegetation. These are glimpses from the papers in the palaeontology session. They demonstrate that a great evolution has taken part not only in animals, but also in our capability to extract and deal with their remains.



Fossils, Developmental Patterning And The Of Tetrapods 45 TheOrigin New Panorama of Animal Evolution Proc. 18th Int. Congr. Zoology, pp. 45-54, 2003

Fossils, developmental patterning and the origin of tetrapods P. E. Ahlberg Department of Palaeontology, The Natural History Museum, Cromwell Road, London SW7 5BD, U.K. E-mail: [email protected]

Abstract Our understanding of the origin of tetrapods has improved greatly in recent years, due to new fossil discoveries and improved phylogenetic analyses. The move from water to land occurred gradually within the upper part of the tetrapod stem group, during a 15-20 million year time interval from the late Middle Devonian to the Early Carboniferous. The first stage, represented by Panderichthys, involved transformation of the body and head to a “crocodile-like” shape; this may reflect a move into very shallow water. This was followed by the rapid evolution of defining tetrapod characters such as limbs and sacrum. However, the earliest limbed vertebrates, represented by Acanthostega and Ichthyostega, still retained many aquatic adaptations including a tail fin and fish-like lateral line canals. Real terrestriality probably only evolved at the base of the tetrapod crown group in the Early Carboniferous. Developmental genetics shows that the production of digits is dependent on a late distal phase of Hox expression in the limbs, which seems to be unique to tetrapods. This expression phase, which probably originated in the stem group between the Panderichthys and Acanthostega + Ichthyostega nodes, may have been prompted by the duplication of a promoter for Bone Morphogenesis Protein receptor IB.

Introduction The origin of tetrapods or land vertebrates, which occurred during the Late Devonian period between about 370 and 355 million years ago, was one of the most important events in vertebrate history (Ahlberg & Milner 1994). It generated a new “kind” of animal, with a morphology and lifestyle radically different from those of its ancestors, and sparked an evolutionary radiation that has continued to the present day and now comprises more than 24000 living species of amphibians, reptiles, birds and mammals. It is also what can be termed a “major morphological transition”, that is an evolutionary transformation of such magnitude that it is difficult to establish detailed homologies between the ancestral and derived conditions, explain how the derived condition was generated, understand the selection pressures involved, or infer the morphology and

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mode of life of unknown intermediate forms. As such it represents an important class of evolutionary problem, which also includes the origin of the different animal phyla - as demonstrated for example by the contributions in this volume on the origin of the Arthropoda. Until recently the origin of tetrapods was not well understood, but new fossil discoveries (Coates & Clack 1990, 1991, Coates 1996, Clack 1994, 1998, Ahlberg 1991, 1995, 1998, Ahlberg et al. 1994, 2000) and revisions of existing material (Ahlberg & Clack 1998) coupled with detailed cladistic analyses (Coates 1996, Ahlberg & Clack 1998, Ahlberg & Johanson 1998) have created a much clearer picture of the transformation. It is now possible to map the sequence of character change from fish to tetrapod, to describe certain intermediate morphological states, and to define approximate time frames for these changes. At the same time, the science of developmental genetics has advanced to a point where it allows tentative hypotheses to be framed about the genetic basis for some of the morphological innovations. A sketch synthesis of these approaches, applied to the origin of limbs, is presented below as an illustration of the potential of “evolutionary developmental phylogenetics”. The phylogenetic context The “origin of tetrapods”, in the morphological and ecological sense, was an event within the tetrapod stem group. As such it conflicts with much of current taxonomic usage (De Queiroz & Gauthier 1990, Patterson 1994), which would pin the term “Tetrapoda” either to the tetrapod crown group or total group. A brief explanation of these terms may therefore be helpful (Fig. 1). The tetrapod crown group comprises the living tetrapod groups - Lissamphibia (containing frogs, salamanders and caecilians) and Amniota (containing reptiles,

Fig. 1: Schematic cladogram of a Recent group and its Recent sister group, illustrating the concepts of crown group, stem group and total group. Note that all these concepts are defined in relation to Recent taxa and that the stem group consists, by definition, entirely of extinct forms.

Fossils, Developmental Patterning And The Origin Of Tetrapods

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mammals and birds) - and the fossil members of these lineages. Fossil evidence indicates that the crown group originated during the Early Carboniferous (Ahlberg & Milner 1994). The closest living relatives of the tetrapods are probably the lungfishes, Dipnoi (Cloutier & Ahlberg 1996), so the tetrapod total group comprises all animals that are more closely related to living tetrapods than to lungfishes. The lungfish and tetrapod lineages appear to have separated by the Early Devonian, as the earliest known lungfishes are of this age (Denison 1968, Campbell & Barwick 1984). Numerous members of the tetrapod stem group (the total group minus the crown group; see Fig. 1) are known from the Devonian and Carboniferous. Basal stem group members have paired fins, were apparently wholly aquatic, and would subjectively be described as “fishes”, whereas derived forms have limbs, were probably at least partly terrestrial, and would be described as “tetrapods”. This is a situation comparable with that of birds (Currie, this volume), where the upper part of the bird stem group contains Archaeopteryx and other obvious “primitive birds”, whereas the base of the stem group contains some very un-birdlike dinosaurs such as Diplodocus. When I discuss the “origin of tetrapods” in this paper I refer to the morphological and ecological transition within the stem group. As the stem group by definition consists exclusively of fossil forms, the detailed phylogeny is based on morphological data and the chronology on stratigraphic evidence rather than molecular divergence dates. The morphological transformation The morphological transformation from the base of the tetrapod stem group to the base of the crown group can be summarised as follows (Fig. 2): Losses: Median fins and tail fin, dermal fin rays (lepidotrichia) of paired fins, bony gill cover, internal gills in adult, bones connecting top of shoulder girdle to back of head. Gains: Digits on paired appendages, sacrum (connection between pelvis and vertebral column), zygapophyses (articulations between neural arches in vertebral column). Modifications of existing structures: Braincase reconstructed so that intracranial joint between orbitotemporal and otic regions disappears, hyomandibula modified into stapes, skull modified into “crocodile-like” morphology with dorsal eyes and long snout, lateral line canals less deeply incised into dermal bones, rib cage greatly expanded, scapulocoracoid (endoskeletal part of shoulder girdle) and pelvis greatly enlarged, hind limb enlarged, tail lengthened. These transformations did not of course occur all at once. Looking at the stem group in more detail (Fig. 3), we can discern the following stages: Rhizodonts and osteolepiforms: These fishes form the basal part of the stem group (Johanson & Ahlberg 1998, Ahlberg & Johanson 1998). They have certain tetrapod characteristics, such as an internal nostril or choana (Jarvik 1980), which are not present in other fish groups, but show no obvious adaptations toward life on land. Eusthenopteron (Fig. 2A) is a representative osteolepiform. Panderichthys: This genus, from the late Middle Devonian of Latvia (Fig. 4A), has a crocodile-like skull shape and has lost the median fins but not the tail fin (Vorobyeva & Schultze 1991). The intracranial joint has been immobilised by fusion of the skull roof,

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Fig. 2: Two members of the tetrapod stem group, Eusthenopteron (an “osteolepiform fish”) and Ichthyostega (an “early tetrapod”), illustrating the main morphological changes of the fish-tetrapod transition. Structures labelled in A disappear during the transition; those labelled in B are morphological novelties of tetrapods. Further changes from B to the tetrapod crown group include the loss of the lepidotrichial tail fin and the reduction of the foot from 7 to 5 digits. (The hand of Ichthyostega is unknown.) A modified from Jarvik (1980); B from Coates & Clack 1995.

Fig. 3: Schematic representation of the tetrapod stem group. Note that the “osteolepiforms” are a paraphyletic group. Eusthenopteron is one of the most derived osteolepiforms.


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Fig. 4: A, Panderichthys, the most derived “fish” in the tetrapod stem group, showing tetrapod-like body form coupled with paired fins of osteolepiform type (pectoral fin shown in detail). Lateral view. B, Acanthostega, a Devonian “tetrapod” from the stem group, showing a similar body form but with 8-digit limbs (forelimb shown in detail). Dorsolateral view. Note that Acanthostega has a larger tail fin and smaller rib cage than Ichthyostega. A from Ahlberg & Milner (1994) and Vorobyeva (1992); B from Coates (1996).

but persists internally; the braincase and hyomandibula are still unmodified (Ahlberg et al. 1996). The ribs are moderately enlarged (Vorobyeva & Schultze 1991). Panderichthys retains paired fins, a bony gill cover, and a connection between the shoulder girdle and the back of the skull. It has a short tail, a pelvis that is apparently not connected to the backbone (pers. obs.), and no zygapophyses (Vorobyeva & Schultze 1991). Acanthostega and Ichthyostega: These forms, from the latest Devonian of Greenland, are the earliest limbed vertebrates known from complete skeletons (Fig. 2B, 4B). However, fragmentary earlier genera such as Elginerpeton from the middle Late Devonian of Scotland (Ahlberg 1995, 1998) seem to be essentially similar. These animals have all the tetrapod characters of Panderichthys, and in addition have a tetrapod braincase without an intracranial joint, a stapes rather than a hyomandibula, no bony gill cover, limbs with seven or eight digits, greatly enlarged scapulocoracoid and pelvis, contact between pelvis and vertebral column, no bone contact between shoulder girdle and skull, moderately (Acanthostega) or greatly (Ichthyostega) expanded ribcage, a long tail, and poorly developed zygapophyses (Coates & Clack 1990, 1995, Coates 1996, Clack 1994, 1998). However, they retain some fish-like characters such as a lepidotrichial tail fin and deeply incised lateral line canals which open to the surface through series of discrete pores. Acanthostega retained internal gills as an adult (Coates & Clack 1991).

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Early Carboniferous tetrapods: A number of Early Carboniferous tetrapods such as Greererpeton (Smithson 1982, Godfrey 1989) and Whatcheeria (Lombard & Bolt 1995) fall into the top of the stem group or the very base of the crown group. They have all the tetrapod characteristics of Acanthostega and Ichthyostega, and in addition have shallow lateral line grooves, limbs with four or five digits, a further enlarged scapulocoracoid, well developed zygapophyses, and no tail fin. They probably lacked internal gills as adults. As can be seen from this summary, the lower part of the tetrapod stem group shows no obvious trend towards terrestrial life and only modest morphological change. The first step in the transition is the evolution (in the common ancestor of Panderichthys and tetrapods) of a tetrapod-like head and body form. This is followed by an episode of major character change between the Panderichthys node and the Acanthostega + Ichthyostega node, where the paired fins turn into limbs (initially with seven or eight digits) and much of the internal skeleton is redesigned; this corresponds to the conventionally recognised “origin of tetrapods”. Finally, in the uppermost part of the stem group, the tail fin is lost, the number of digits is reduced, and the lateral line canals become more superficial - probably because the skin is growing thicker. It can be added that all tetrapod stem group members were predators, and that those from the Panderichthys node to the top of the stem group are all relatively large, about 0.8 to 1.5 metres in length. It is interesting to note that all the most dramatic changes are compressed onto one internode, between Panderichthys and Acanthostega + Ichthyostega (but in fact probably between Panderichthys and Elginerpeton; see Fig. 3). The time interval between Panderichthys and Elginerpeton is only about 5 million years (Ahlberg & Milner 1994, Ahlberg et al. 1996), suggesting that these changes took place remarkably quickly. This phenomenon needs to be considered from both ecological and developmental genetic perspectives. Environment and mode of life Almost all Devonian members of the tetrapod stem group come from “Old Red Sandstone” sediments. These represent a range of non-marine and marginal marine environments from lakes and rivers to lagoons, estuaries and deltas (see for example Kuršs 1992, Prichonnet et al. 1996, Chidiac 1996, and references therein), and frequently contain fossil land plants. It is not yet possible to determine whether the fish-tetrapod transition took place in a freshwater or brackish environment, but it seems unlikely to have occurred in a fully marine setting. The rhizodonts and osteolepiforms were clearly wholly aquatic, occupying a range of predatory fish niches, though outgroup comparison with lungfishes, coelacanths and primitive living actinopterygians indicate that they had functional lungs. Panderichthys gives the first hint of a changing mode of life: its dorsoventrally flattened body, loss of median fins, and eyes positioned on top the head under raised “eyebrows”, suggest that it may have operated in very shallow water, possibly using its raised eyes to look out above the surface. The earliest tetrapods, such as Acanthostega and Ichthyostega, differ significantly from Panderichthys in internal anatomy, particularly as regards the braincase, hyoid arch and


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limb girdles (Vorobyeva & Schultze 1991, Ahlberg et al. 1996), but their gross morphology is not very different. This is particularly true for Acanthostega, which has a large symmetrical tail fin, weak limbs, and persistent internal gills. These tetrapods were clearly still largely aquatic, and may have had a similar lifestyle to Panderichthys. Limbs may thus have evolved primarily for locomotion in shallow water rather than on land (Coates & Clack 1995). However, many of the tetrapod features which first appear at this point in the stem group (zygapophyses, sacrum, expanded ribcage, detachment of shoulder girdle from head) are functionally related to weight support. This suggests that the internode between Panderichthys and the earliest tetrapods was characterised by a rapid shift towards more activity in mechanically non-supportive conditions (water too shallow to support the body, or dry land). This trend continued up into the tetrapod crown group, with the loss of primitive aquatic features such as the tail fin, but even at this early stage of tetrapod evolution some taxa such as Crassigyrinus (Panchen & Smithson 1990) reverted to a more wholly aquatic life. Evolution and developmental patterning At present, the only part of tetrapod anatomy that is well enough understood in developmental genetic terms to permit an attempt at an evolutionary-developmental synthesis, is the limb skeleton. However, the principles underlying this synthesis will also be applicable to other parts of the anatomy once enough developmental data have been assembled. Morphological evidence: The osteolepiform part of the tetrapod stem group is characterised by paired fin endoskeletons in which humerus/femur, radius/tibia, ulna/ fibula and some wrist/ankle bones can be identified with confidence, but which lack digits. The appendage is terminated distally by a fin web supported by dermal lepidotrichia. Panderichthys shows essentially the same condition, though the distal part of the endoskeleton is somewhat simplified (Fig. 4C). The proximal elements, by contrast are more tetrapod-like in shape than those of osteolepiforms. In Acanthostega and Ichthyostega, the lepidotrichia have disappeared and an array of seven or eight endoskeletal digits has sprouted from the distal end of the appendage (Fig. 4D). The proximal elements on the other hand have not been greatly modified. Finally, in postDevonian tetrapods the number of digits is reduced to four or five. Overall, it appears that the osteolepiform / Panderichthys fin endoskeleton is equivalent to the arm/leg but not the hand/foot, and that the digits appeared rather abruptly as an addition to the distal end of the endoskeleton at the same time as the lepidotrichia disappeared. Developmental genetic evidence: Early appendage development is essentially similar in teleost fishes and tetrapods; in both groups it is, for example, associated with the expression of Hoxd-11 and Hoxd-13 in the posterior part of the appendage bud, and anteroposterior asymmetry is regulated by Sonic hedgehog (Sordino et al. 1995, Shubin et al. 1997). However, tetrapods also show a late phase of expression of the Hoxd genes in the distal part of the limb bud, in the area where the digits develop (Sordino et al. 1995, Shubin et al. 1997). There is no corresponding late phase in teleosts. Recently, it has been shown that distal mesenchyme proliferation in the tetrapod limb bud (which creates the mesenchyme in which the distal Hox expression occurs) is dependent on a distal

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promoter of Bone Morphogenesis Protein (BMP) receptor type IB (Baur et al. 2000). The corresponding, possibly paralogous proximal promoter is involved in the regulation of brain development (Baur et al. 2000). Synthesis: The conservation of early appendage development between recent teleost fishes and tetrapods implies that the same developmental pathways were present in the tetrapod stem group. This inference is supported by the morphological stability of the proximal endoskeletal elements throughout the tetrapod stem group, which suggests that the patterning of these elements did not change significantly across the fish-tetrapod transition. We can infer that distal mesenchyme proliferation and late distal Hox expression originated at the internode between Panderichthys and Ichthyostega + Acanthostega, possibly in connection with duplication of a promoter of BMP receptor IB. Questions for the future: This tentative synthesis still leaves many questions unanswered. Some of the more important ones are: a) Is the distal promoter of BMP receptor IB really unique to tetrapods? b) The proximal appendage endoskeleton of sarcopterygian fishes (not only members of the tetrapod stem group, but also other groups like coelacanths and lungfishes) contains elements (humerus/femur, radius/tibia, ulna/fibula) which cannot be identified in the teleost fin. Thus, in addition to the gene expressions that are conserved between teleosts and tetrapods (and therefore general to the Osteichthyes as a whole) there must exist a more restricted set of sarcopterygian expression patterns regulating the morphology of these elements. What are these expression patterns? c) How does the distal mesenchyme proliferation and emergence of digits relate to the loss of the lepidotrichia? Are the two directly linked, or simply coincident? d) What controls digit number? e) Given that the proximal promoter of BMP receptor IB in tetrapods is involved in brain patterning, could there be a genetic link between the evolution of digits and the simultaneous rebuilding of the tetrapod braincase? Conclusion Recent work has done much to illuminate the details of the origin of tetrapods. We can now see that it was a fairly gradual affair, with the transition from aquatic to fully terrestrial life stretching across the upper part of the stem group from the Panderichthys node to the base of the crown group and occupying a time interval of about 15-20 million years from the late Middle Devonian to the Early Carboniferous. However, within this extended period of change lies a brief pulse of much more rapid and dramatic morphological evolution, the traditionally recognised “origin of tetrapods”, which occupied about 5 million years and corresponds to the internode between Panderichthys and Elginerpeton. This phase of rapid change was probably driven by selection pressure for terrestrial or extreme shallow-water competence, but it is possible that pleiotropic effects due to linked gene expression patterns were also involved in some of the changes. Phylogenetic and developmental genetic data can at present only be synthesised (in a preliminary manner) in relation to the evolution of limbs. However, in the long run it will be possible to extend this synthesis to other parts of the anatomy such as the braincase and middle ear; this will be crucial to understanding


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how our distant ancestors generated the new morphologies that allowed them to make the transition from water to land. References AHLBERG P.E. 1991. Tetrapod or near-tetrapod fossils from the Upper Devonian of Scotland. Nature 354: 298-301. AHLBERG P.E. 1995. Elginerpeton pancheni and the earliest tetrapod clade. Nature 373: 420-425. AHLBERG P.E. 1998. Postcranial stem tetrapod remains from the Devonian of Scat Craig, Morayshire, Scotland. Zoological Journal of the Linnean Society 122: 99-141. AHLBERG P.E. & J.A. CLACK 1998. Lower jaws, lower tetrapods - a review based on the Devonian genus Acanthostega. Transactions of the Royal Society of Edinburgh: Earth Sciences 89: 11-46. AHLBERG P.E. & Z. JOHANSON 1998. Osteolepiforms and the ancestry of tetrapods. Nature 395: 792-794 AHLBERG P.E. & A.R. MILNER 1994. The origin and early diversification of tetrapods. Nature 368: 507-514. ˇ E. & O. LEBEDEV 1994. The first tetrapod finds from the DevoAHLBERG, P.E., LUKŠEVI CS nian (Upper Famennian) of Latvia. Philosophical Transactions of the Royal Society of London B 343: 303-328. ˇ E. & J.A. CLACK 1996. Rapid braincase evolution between PanderAHLBERG P.E., LUKŠEVICS ichthys and the earliest tetrapods. Nature 381: 61-64 ˇ E. & E. MARK-KURIK 2000. A near-tetrapod from the Baltic MidAHLBERG P.E., LUKŠEVICS dle Devonian. Palaeontology 43: 533-548. BAUR S.T., MAI J.J. & S.M. DYMECKI 2000. Combinatorial signalling through BMP receptor IB and GDF5: shaping of the distal mouse limb and the genetics of distal limb diversity. Development 127: 605-619 CAMPBELL K.S.W. & R.E. BARWICK 1984. Speonesydrion, an early Devonian dipnoan with primitive tooth plates. Palaeoichthyologica 2: 1-48. CHIDIAC Y. 1996. Paleoenvironmental interpretation of the Escuminac Formation based on geochemical evidence. In Schultze H.-P. & R. Cloutier (eds), Devonian Fishes and Plants of Miguasha, Quebec, Canada. Verlag Dr. Friedrich Pfeil, München, pp. 47-53. CLACK J.A. 1994. Earliest known tetrapod braincase and the evolution of the stapes and fenestra ovalis. Nature 369: 392-94. CLACK J.A. 1998. The neurocranium of Acanthostega gunnari Jarvik and the evolution of the otic region in tetrapods. Zoological Journal of the Linnean Society 122: 61-97. CLOUTIER R. & P.E. AHLBERG 1996. Morphology, characters and the interrelationships of basal sarcopterygians. In Stiassny M.L.J., Parenti L.R. & G.D. Johnson (eds), Interrelationships of Fishes. Academic Press, San Diego, pp. 445-479. COATES M.I. 1996. The Devonian tetrapod Acanthostega gunnari Jarvik: postcranial anatomy, basal tetrapod interrelationships and patterns of skeletal evolution. Transactions of the Royal Society of Edinburgh: Earth Sciences 87: 363-421. COATES M.I. & J.A. CLACK 1990. Polydactyly in the earliest known tetrapod limbs. Nature 347: 66-69. COATES M.I. & J.A. CLACK 1991. Fish-like gills and breathing in the earliest known tetrapod. Nature 352: 234-36.

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COATES M.I. & J.A. CLACK 1995. Romer’s gap: tetrapod origins and terrestriality. Bulletin du Muséum National d’Histoire Naturelle, Paris, 4e série 17(C) (1-4): 373-388. DENISON R.H. 1968. Early Devonian lungfishes from Wyoming, Utah and Idaho. Fieldiana, Geology 17: 353-413. DE QUEIROZ K. & J. GAUTHIER 1990. Phylogeny as a central principle in taxonomy: phylogenetic definitions of taxon names. Systematic Zoology 23: 449-480. GODFREY S.J. 1989. The postcranial skeletal anatomy of the Carboniferous tetrapod Greererpeton burkemorani Romer 1969. Philosophical Transactions of the Royal Society of London B 323: 75-133. LOMBARD R.E. & J.R. BOLT 1995. A new primitive tetrapod Whatcheeria deltae from the Lower Carboniferous of Iowa. Palaeontology 38: 471-94. JARVIK E. 1980. Basic Structure and Evolution of Vertebrates, volume 1. Academic Press, London, 575 p. JOHANSON Z. & P.E. AHLBERG 1998. A complete primitive rhizodont from Australia. Nature 394: 569-572 KURŠS V. 1992. Depositional environment and burial conditions of fish remains in Baltic Middle Devonian. In Mark-Kurik E. (ed.), Fossil Fishes as Living Animals. Academia 1, Tallinn, pp. 251-264. PANCHEN A.L. & T.R. SMITHSON 1990. The pelvic girdle and hind limb of Crassigyrinus scoticus (Lydekker) from the Scottish Carboniferous and the origin of the tetrapod pelvic skeleton. Transactions of the Royal Society of Edinburgh: Earth Sciences 81: 31-44. PATTERSON C. 1994. Bony fishes. In Spencer R.S. (ed.), Major Features of Vertebrate Evolution (short courses in paleontology 7). Paleontological Society, pp. 57-84. PRICHONNET G., DI VERGILIO M. & Y. CHIDIAC 1996. Stratigraphical, sedimentological and paleontological context of the Escuminac Formation: Paleoenvironmental hypotheses. In Schultze H.-P. & R. Cloutier (eds), Devonian Fishes and Plants of Miguasha, Quebec, Canada. Verlag Dr. Friedrich Pfeil, München, pp. 23-36. SHUBIN N., TABIN C. & S. CARROLL 1997. Fossils, genes and the evolution of animal limbs. Nature 388: 639-648. SMITHSON T.R. 1982. The cranial morphology of Greererpeton burkemorani Romer (Amphibia: Temnospondyli). Zoological Journal of the Linnean Society 76: 29-90. SORDINO P., VAN DER HOEVEN F. & D. DUBOULE 1995. Hox gene expression in teleost fins and the origin of vertebrate digits. Nature 375: 678-681. VOROBYEVA E.I. 1992. The role of development and function in formation of “tetrapod-like” pectoral fins. Zhurnal Obshei Biologii 53: 149-158. VOROBYEVA E.I. & H.P. SCHULTZE 1991. Description and systematics of panderichthyid fishes with comments on their relationship to tetrapods. In Schultze H.-P. & L. Trueb (eds), Origins of the Higher Groups of Tetrapods: Controversy and Consensus. Cornell Publishing Associates, Ithaca, pp. 68-109.


A. Legakis, S. Sfenthourakis, R. Polymeni & M. Thessalou-Legaki (eds.) Feathered dinosaurs and thePanorama origin ofof birds The New Animal Evolution Proc. 18th Int. Congr. Zoology, pp. 55-60, 2003

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Feathered dinosaurs and the origin of birds P.J. Currie Royal Tyrrell Museum of Palaeontology, Box 7500, Drumheller, Alberta T0J 0Y0, Canada

Abstract Since 1996, specimens from at least six families of non-avian theropod dinosaurs have been found with preserved feathers and feather-like structures. Feathers seem to have originated from simple branching structures in primitive coelurosaurian dinosaurs like Sinosauropteryx, where they presumably served as insulation. From these developed longer, stiffer structures on the arms of velociraptorine dromaeosaurids like Sinornithosaurus and Beipiaosaurus. These may have been display structures, but may also have functioned to cover eggs in the nests of brooding females. True feathers are found on the arms and tails of the non-avian theropods Caudipteryx and Protarchaeopteryx, and may represent more elaborate display structures. These were relatively short and had symmetrical vanes, and were still clearly not adapted for flight. Archaeopteryx, the earliest bird, is the first true flier known in the theropod-bird lineage. Theropods less derived than Archaeopteryx should be considered as non-avians, whereas those more derived are true birds.

With the development and spread in the 1970s of the idea that dinosaurs might be warm-blooded animals that were the direct ancestors of birds (Bakker 1975, Ostrom 1974, Paul 1988), paleontologists started to consider the possibility that some dinosaurs had feathers. Logic suggested that if dinosaurs were warm-blooded, then smaller ones would have needed insulation to help stabilize their body temperatures. Furthermore, if theropods were the ancestors of birds, it would make sense that the insulation used by dinosaurs would have been some form of feather. Most paleontologists believe that feathers had to have developed before birds were able to incorporate them into their flight mechanism. Although we normally think of birds as being the only animals covered with feathers, in truth it is their form of powered flight that sets them apart from all other life forms. Warm-blooded dinosaurs and the dinosaurian origin of birds were two of the biggest controversies in palaeontology at the end of the twentieth century. When first proposed, there were far more people opposed to these hypotheses than there were in support of them. This trend has reversed now, largely because of some remarkable specimens from northeastern China that appeared after the discovery of an extremely rich source of early Cretaceous bird fossils (Chiappe et al. 1999). These specimens include fossilized feathers, which only preserve under exceptional circumstances (Davis & Briggs 1995).

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In 1996, Ji & Ji announced the discovery of the first “feathered” dinosaur, Sinosauropteryx prima, in a paper published in Chinese. Additional specimens of this small, chicken-sized animal were discovered and described shortly after (Chen et al. 1998, Ji & Ji 1997b). A downy coat of simple branching structures covered the head, neck, thorax, limbs and tail of Sinosauropteryx (Currie & Chen 2001), and presumably functioned to insulate the animal. Although Chen et al (1998) took a conservative view and referred to these as “integumentary structures”, everyone was aware that they represent potential protofeathers. This triggered escalation in the controversies on the ancestry of birds and warm-bloodedness in dinosaurs (Brush et al. 1997, Currie 1997, 2000, Ruben et al. 1997). More “feathered” dinosaurs have been subsequently described, and represent theropod families distinct from that of Sinosauropteryx. Beipiaosaurus inexpectus (Xu et al. 1999a) is a larger, approximately man-sized dinosaur that had a relatively small head with leaf-like teeth, a long neck, long arms and a relatively short tail. This animal belongs to an unusual group of theropod dinosaurs that are called therizinosaurs. Its body was covered with structures similar to those that covered Sinosauropteryx, but it also has long, stiff, feather-like structures on the backs of its arms. Another “feathered” dinosaur is Sinornithosaurus millenii (Xu et al. 1999b, Ji et al. 2001), which is a dog-sized animal with sharp serrated teeth and raptorial claws. The pattern of body covering is similar to that of Beipiaosaurus. It is a dromaeosaurid that is closely related to Velociraptor. Microraptor zhaoianus (Xu et al. 2000) is another “feathered” dromaeosaurid from Liaoning. This animal was smaller than Archaeopteryx, has a shorter tail than other dromaeosaurids, and has several adaptations in the feet that suggest it may have been arboreal. As in Sinosauropteryx (Currie & Chen 2001) and Sinornithosaurus (Xu et al. 2001), the “feathers” of Microraptor seem to have been simple branching structures. Protarchaeopteryx robusta is a feathered theropod described by Ji & Ji (1997a). Whereas Sinosauropteryx is a small dinosaur with short arms and an extremely long tail, Protarchaeopteryx has long arms and a relatively short tail. In addition to having downy, feather-like structures covering its body, Protarchaeopteryx also has long quill-like feathers at the end of the tail. With this animal, there is no doubt concerning the identification of true feathers, each of which has a central rachis, barbs and barbules. Another feathered dinosaur was also discovered in 1997, and was originally misidentified as Protarchaeopteryx. In addition to having long feathers at the end of the tail, it has true feathers behind the arms. The six specimens recovered represent another species of feathered dinosaur (Ji et al. 1998), now known as Caudipteryx zoui. Distantly related to Oviraptor (Barsbold et al. 2000), Caudipteryx was a turkey-sized dinosaur with relatively long legs that suggest it was strongly cursorial. The feathers make its arms look like rudimentary wings, although the feathers, which have symmetrical vanes, and arms are both too short to have allowed it to fly. It is more likely that the elongate feathers on the arms and at the end of the tail were used for display (Currie 1998). Dinosaurs were highly visual animals that evolved a fantastic array of ornamentation (crests, frills, horns, spikes, etc.) to attract mates, warn potential rivals, and otherwise enhance their interactive behavior. Once dinosaurs had acquired feathers for insulation, it would have been relatively easy to adapt them into display structures that are lightweight, strong, colorful, and can be shed and replaced. Display may not have been

Feathered dinosaurs and the origin of birds

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the only function for these longer, stiffened feathers. Specimens of the related Oviraptor have been found on nests of eggs (Dong & Currie 1996), and taphonomic analysis suggests that long feathers on the backs of the arms might have helped protect the eggs from the elements (Hopp & Orsen 1998). The presence of a fan of feathers on the end of the tail presumably led to the reduction in number of tail vertebrae in these oviraptorosaurs, and even to the development of a pygostyle in Nomingia (Barsbold et al. 2000). There are now six species of “feathered” dinosaurs from northeastern China. Evidence also shows that alvarezsaurids (which are classified by different workers as either nonavian theropods or as birds) had feathers (Schweitzer et al. 1997), as well as the oviraptorosaur Nomingia (Barsbold et al. 2000). More “feathered” dinosaurs are in the process of being described from northeastern China, where the sedimentary rocks are extremely fossiliferous and are being excavated on an unprecedented scale. The described “feathered” species represent six different families of non-avian theropods. Sinosauropteryx is a compsognathid theropod, closely related to the European Compsognathus (Ostrom 1978). Protarchaeopteryx is only known from a single specimen, but might be the non-avian theropod most closely related to the earliest bird, Archaeopteryx. Both Caudipteryx and Nomingia are oviraptorosaurs, but represent two distinct families. Beipiaosaurus is a therizinosauroid, whereas Sinornithosaurus and Microraptor are dromaeosaurids. As already pointed out, alvarezsaurids are sometimes classified as non-avian theropods and sometimes as birds. All of these families belong to the Coelurosauria (Hutchinson & Padian 1997). The fact that the known “feathered” dinosaurs represent such a diverse assemblage of coelurosaurians strongly suggests that many, if not most, of the meat-eating dinosaurs were probably feathered. Because Tyrannosaurus is on the coelurosaurian branch of the Theropoda (Holtz 1994, 2000), it is possible that even it had feathers somewhere on its body at some stage in its life. Such a large animal would not have needed feathers for insulation as an adult, and pebbly skin impressions with no indication of feathers are preserved for the related tyrannosaurs Gorgosaurus and Daspletosaurus. However, it is not impossible that newborn tyrannosaurs might have had some sort of insulating down, or that the adults used feathers somewhere on their bodies for display. The presence of feathers on dinosaurs does not by itself prove that birds came from dinosaurs. There is much stronger evidence in the skeleton to suggest that birds and dinosaurs are more closely related to each other than either is to any other type of animal (Gauthier 1986, Chiappe 1995, Holtz 2000, Sumida & Brochu 2000). However, feathers are such complex structures that the discovery of feathered dinosaurs has done far more to convince people that birds are living representatives of the Dinosauria than all of the details of skeletal anatomy have. Still, not everyone is convinced (see, for example, Feduccia 1996, Ruben et al. 1997), and some of these people are more vocal than the majority of paleontologists who accept that birds descended from dinosaurs. However, lack of a convincing alternative for bird ancestry, and use of circular reasoning undermine their arguments. For example, they have long argued that the structure of the ankle is different in theropod dinosaurs and birds. Although they claim that Caudipteryx is a secondarily flightless bird (Jones et al. 2000) because it has feathers, this animal has the same ankle structure as theropod dinosaurs like Velociraptor and Tyrannosaurus.

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Fig. 1. Phylogenetic relationships of some feathered theropods.

Most scientists agree Archaeopteryx is the earliest known bird, and therefore represents the dividing line between dinosaurs and birds. Related animals more derived or advanced than Archaeopteryx are birds. But species that are more primitive are not. Using this concept, birds are animals that fly using wings that incorporate specialized feathers, or are derived from such animals. Feathers separate birds from all other living animals, but they cannot be used to define birds because they would also have been present in avian ancestors that could not fly. Birds could be diagnosed as all feathered animals, but we would then have to reclassify all feathered dinosaurs as birds, as well as all of their direct descendants. Because preservation of feathers is rare, we do not know, and may never know, how widespread feathers were amongst other types of dinosaurs. Although an adult Tyrannosaurus rex probably did not have feathers, its ancestors and closest relatives did (Fig. 1). Rather than classify this animal as a bird, it would be more logical to emphasize flight, rather than feathers, in the diagnosis of Aves. The fact that we are having trouble classifying many of the new “feathered” fossils emphasizes how closely related dinosaurs and birds are to each other. As we draw towards consensus on the ancestry of birds, attention is shifting to equally interesting problems – the evolution of feathers (Prum 1999), and the origin of flight.

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References BAKKER R.T. 1975. Dinosaur renaissance. Scientific American 232(4): 58-78. BARSBOLD R., OSMÓLSKA H., WATABE M., CURRIE P.J. & K. TSOGTBAATAR 2000. A new oviraptorosaur (Dinosauria, Theropoda) from Mongolia: the first dinosaur with a pygostyle. Acta Palaeontologica Polonica 45: 97-106. BRUSH A., MARTIN L. D., OSTROM J. H., & P. WELLNHOFER 1997. Bird or Dinosaur? — statement of a team of specialists. Episodes 20: 46. CHEN P.J. DONG Z.M. & S.N. ZHENG 1998. An exceptionally well-preserved theropod dinosaur from the Yixian Formation of China. Nature 391: 147-152. CHIAPPE L.M. 1995. The first 85 million years of avian evolution. Nature 378: 353. CHIAPPE L.M., JI S.-A., JI Q. & M.A. NORELL 1999. Anatomy and systematics of the Confuciusornithidae (Theropoda: Aves) from the Late Mesozoic of northeastern China. American Museum of Natural History, Bulletin 242: 1-89. CURRIE P.J. 1997. Feathered dinosaurs. In Currie P.J. & K. Padian (eds), The Encyclopedia of Dinosaurs. Academic Press, San Diego, p. 241. CURRIE P.J. 1998. Caudipteryx revealed. National Geographic Magazine 194 (1): pp. 86-89. CURRIE P.J. 2000. Feathered dinosaurs. In Gregory S. (ed.), The Scientific American Book of Dinosaurs. Paul. St. Martin’s Press, New York, pp. 183-189. CURRIE P.J. & P.-J. CHEN (2001). Anatomy of Sinosauropteryx prima from Liaoning, northeastern China. Canadian Journal of Earth Sciences 38: 1705-1727. DAVIS P.G. & D.E.G. BRIGGS 1995. Fossilization of feathers. Geology 23: 783-786. DONG Z.M., & P.J. CURRIE 1996. On the discovery of an oviraptorid skeleton on a nest of eggs at Bayan Mandahu, Inner Mongolia, People’s Republic of China. Canadian Journal of Earth Sciences 33: 631-636. FEDUCCIA A. 1996. The Origin and Evolution of Birds. Yale University Press. 420p. GAUTHIER J. 1986. Saurischian monophyly and the origin of birds. In Padian K. (ed.), The Origin of Birds and the Evolution of Flight. California Academy of Sciences, San Francisco, pp. 1-55. HOLTZ T.R. 1994. The phylogenetic position of the Tyrannosauridae: implications for theropod systematics. Journal of Paleontology 68: 1100-1117. HOLTZ T.R., Jr. 2000. A new phylogeny of the carnivorous dinosaurs. Gaia 15: 5-61. HOPP T. & M. ORSEN 1998. Dinosaur brooding behavior and the origin of flight feathers. In Wolberg D.L., Gittis K., Miller S., Carey L. & A.Raynor (eds), Dinofest International Symposium, Program and Abstracts, Academy of Natural Sciences, Philadelphia, p. 27. HUTCHINSON J.R. & K. PADIAN 1997. Coelurosauria. In Currie P.J. & K. Padian (eds), Encyclopedia of Dinosaurs. Academic Press, San Diego, pp. 129-133. JI Q., CURRIE P.J., NORELL M.A. & S.-A. JI 1998. Two feathered dinosaurs from northeastern China. Nature 393: 753-761. Ji Q. & Ji S. A. 1996. On discovery of the earliest bird fossil in China and the origin of birds. Chinese Geology 233: 30-33 (in Chinese). JI Q. & S.-A. JI 1997a. Protarchaeopterygid bird (Protarchaeopteryx gen. nov.) - fossil remains of archaeopterygids from China. Chinese Geology 238: 38-41 (in Chinese). JI Q. & S.-A. JI 1997b. Advances in the study of the avian Sinosauropteryx prima. Chinese Geology 242: 30-32 (in Chinese).

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JI Q., NORELL M.A., GAO K.-Q., JI S.-A. & D. REN 2001. The distribution of integumentary structures in a feathered dinosaur. Nature 410: 1084-1088. JONES T. D., FARLOW J.O., RUBEN J.A., HENDERSON D.M. & W.J. HILLENIUS 2000. Cursoriality in bipedal archosaurs. Nature 406: 716-718. OSTROM J.H. 1974. Reply to “Dinosaurs as reptiles”. Evolution 28: 491-493. OSTROM J.H. 1978. The osteology of Compsognathus longipes Wagner. Zitteliana 4: 73-118. PAUL G.S. 1988. Predatory Dinosaurs of the World. Simon and Schuster, New York, 464p. PRUM R.O. 1999. Development and evolutionary origin of feathers. Journal of Experimental Zoology 285: 291-306. RUBEN J.A., JONES T.D. & N.R. GEIST 1997. Lung structure and ventilation in theropod dinosaurs and early birds. Science 278: 1267-1270. SCHWEITZER M.H., WATT J., FORSTER C., NORELL M. & L. CHIAPPE 1997. Keratinous structures preserved with two Late Cretaceous avian theropods from Madagascar and Mongolia. Journal of Vertebrate Paleontology 17: 74A. SUMIDA S.S. & C.A. BROCHU 2000. Phylogenetic context for the origin of feathers. American Zoologist 40: 486-503. XU X., TANG Z.-L. & X.-L. WANG 1999a. A therizinosaur dinosaur with integumentary structures from China. Nature 399: 350-354. XU X., WANG X.-L. & X.-C. WU 1999b. A dromaeosaurid dinosaur with a filamentous integument from the Yixian Formation of China. Nature 401: 262-266. XU X., ZHOU Z.-H. & R.O. PRUM 2001. Branched integumental structures in Sinornithosaurus and the origin of feathers. Nature 410: 200-204.



Evolution of Dental Capability in Eurasian ... Evolution 61 TheWestern New Panorama of Animal Proc. 18th Int. Congr. Zoology, pp. 61-67, 2003

Evolution of Dental Capability in Western Eurasian Large Mammal Plant-Eaters 22-2 Million Years Ago: A Case for Environmental Forcing Mediated by Biotic Processes M. Fortelius Department of Geology, University of Helsinki, P.O. Box 11, FIN-00014 Helsinki, Finland

Abstract The development of computerised databases of fossil organisms that include ecomorphological information on species as well as the conventional data on locality occurrence and taxonomy has enabled “taxon-free” study of community structure and evolution. The Neogene large mammal plant-eater communities of western Eurasia can be shown to exhibit strong geographic and temporal patterns of dental capability (molar crown height times number of cutting edges), with the proportion of dentally capable forms increasing over time as well as in geographic gradients from east to west and south to north. These patterns correspond to an expected general increase in environmental harshness beginning in the interior of the continent and progressively advancing over time towards the climatically moderated oceanic rim. Consistent differences between climatically continental and maritime areas are seen during 20 million years in both body size and dental morphology, with parallel trends advancing at the same rate but at different levels. Closer scrutiny of the dental functional evolution of individual groups shows that the gradual increase seen at the community level is underlain by a considerable diversity of morphologically distinct solutions and rates of change. The combination of long-term trends of change and sustained regional contrasts is strong evidence for direct and precise environmental control over the community structure and functional evolution of the herbivorous large mammals of the Neogene. The fact that the patterns are re-established after brief turnover-driven anomalies seen at about 10 and 5 Ma reinforces the impression of environmental forcing mediated by biotic processes being the main factor responsible for them.

Introduction From the point of view of understanding the relationship between long-term evolution and community structure any example of long-term evolutionary change in a persisting biotic community is of interest, especially if the changes observed can be related to function and environmental conditions in some relatively straightforward fashion.

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Suitable fossil data compilations are rare, but the NOW database (Fortelius et al. 1996) of Neogene Old World mammals offers data that do lend themselves to such an investigation. The NOW data are especially useful because they are “taxon free” (Damuth 1992) in the sense that all species carry morphological and inferred functional attributes, so that analyses can be carried out regardless of which individual taxa happen to be represented in any given interval or geographic location. The NOW data also offer a relatively dense sampling of Western Eurasia, with multiple occurrences of individual taxa in temporally and geographically defined subsets. This in combination with the taxon-free characterization of species allows the use of a computationally trivial but useful methodological ploy, which we have previously referred to as “SPLOC-analysis” (Fortelius & Hokkanen 2001). In contrast to traditional analyses based on faunal lists, SPLOC-analysis makes use of all the available data and weights the impact of individual species in proportion to their frequency of locality occurrence, a non-specific proxy for geographic range and/or local abundance. The most suitable functional complex offered by fossil mammals for this purpose is the chewing apparatus, and in particular the molar dentition. In this study two aspects of the molar dentition were selected: hypsodonty and the number and orientation of cutting edges on the occlusal surface, the latter based on the “crown type” scheme of Jernvall (1995). Neither aspect offers a direct one-to-one relationship with either food or environment, but both have well understood functional roles, and both do show strong general correlation patterns with both diet and habitat (Van Valen 1960, Fortelius 1985, Janis 1988, Janis & Fortelius 1988, Solounias et al. 1994, Popowics & Fortelius 1997, Jernvall et al. 2000, Damuth et al. 2000, Fortelius & Solounias 2000). Using these variables singly and in different combinations offers a means of functional dissection of the temporal, geographic and taxonomic changes observed, and suggests possible causal interpretations of the patterns. Materials and Methods The data used were downloaded from the NOW database on March 9, 2000. A subset limited to Eurasia west of 60 degrees longitude and the time interval 22-2 Ma was selected (Fig. 1). Based on previous work (Fortelius et al. 1996, Fortelius & Hokkanen 2001) the geographic area was divided into blocks, East separated from West at 20 degrees eastern longitude and North from South at 45 degrees northern latitude. All Insectivora, Chiroptera, Rodentia, Lagomorpha, Pinnipedia and Cetacea were deleted from the dataset, as were all indeterminate and “cf.” species attributions. All analyses reported here were limited to species characterized as plant-eaters or plant-dominated omnivores. Hypsodonty was ranked according to the following scheme: brachydont=1, mesodont=2, hypsodont or hypselodont=3. Molar crowns were scored according to the crown type scheme of Jernvall (1995), and the number of longitudinal and transverse lophs was extracted from the crown type formulae. Molar capability was defined as ranked hypsodonty times total loph count. The dataset is available from the author, and the latest public NOW dataset can be downloaded from http://www.helsinki.fi/science/ now/, where further details regarding the data may also be obtained. Mean values for lophedness, hypsodonty and molar capability were calculated for subsets of the data

Evolution of Dental Capability in Western Eurasian ...

63

Fig. 1. Map of Western Eurasia showing localities included in the study. The vertical line at 20 degrees eastern longitude separates West from East, the horizontal line at 45 degrees northern latitude separates North from South (see under Materials and Methods). Width of field ca 5 500 km.

defined by time units, designed to correspond to the biochronologic MN-units according to the correlation tables of Steininger et al. (1996). Results Selected results for overall trends are shown in Figures 2-3. Longitudinal and transverse lophedness are negatively correlated in the interval studied (Fig. 2), as would be expected from the strong known association between transverse lophs and leaf-eating, a relationship violated only by advanced elephantids at the end of the study interval. Transverse lophedness accordingly peaks in the “forested” Middle Miocene, and both graphs show rapid shifts (in opposite directions) at 10 Ma, the major mammal turnover event known in western and central Europe as the “Vallesian Crisis” (Agustí & MoyàSolà 1990). Total loph count (Fig. 3) shows virtually no change except for a rise at the end, while hypsodonty shows a sustained rise, again including a rapid shift at 10 Ma. Fig. 4 shows the evolution of mean molar capability separately for the East and West blocks. Molar capability is persistently higher in the more continental (seasonal) East

64


Fig. 2. Bivariate scatter plot of longitudinal and transverse loph counts against time units. Fitted lines are LOWESS-smoothed with tension 0.5.

Fig. 3. Bivariate scatter plot of hypsodonty and total loph count against time units. Fitted lines are LOWESS-smoothed with tension 0.5.

except for two turnover events, the Vallesian Crisis at 10 Ma and the Miocene-Pliocene boundary at 5 Ma. Fig. 5 shows the same for the North and South blocks. Molar capability is consistently higher in South than in North except for an interval around 10-7 Ma, beginning with the Vallesian Crisis and continuing into a time that is very poorly sampled for Europe north of the Alps. For both comparisons the difference between blocks is statistically highly significant (Kruskal-Wallis test, P

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