GENE AVATARS THE NEO-DARWININAN THEORY OF EVOLUTION Pierre-Henri Gouyon Jean-Pierre Henry Jacques Arnould Translated by Tiiu Ojasoo KLUWER ACADEMIC PUBLISHERS NEW YORK, BOSTON, DORDRECHT, LONDON, MOSCOW eBook ISBN: 0-306-47570-7 Print ISBN: 0-306-46616-3 ©2002 Kluwer Academic Publishers New York, Boston, Dordrecht, London, Moscow Print ©2002 Kluwer Academic/Plenum Publishers New York All rights reserved No part of this eBook may be reproduced or transmitted in any form or by any means, electronic, mechanical, recording, or otherwise, without written consent from the Publisher Created in the United States of America Visit Kluwer Online at: http://kluweronline.com and Kluwer's eBookstore at: http://ebooks.kluweronline.com PREFACE France holds a rather unusual position in the field of evolutionary biology. Whereas French naturalists from Buffon, Cuvier and Lamarck onwards made great discoveries in centuries past, French biologists missed the turning when it came to genetics. Until the 1970s, most French biologists were convinced that genetics was not as interesting as developmental science (some "rare species", for example R. Chandebois, still hold this view). For them, the general principles of heredity resided in the cytoplasm rather than in the genome. This was not, however, as great an obstacle as one might have thought. For example, it did not prevent Malécot from being one of the most outstanding theoreticians of population genetics, L’Héritier and Teissier from inventing population cages for Drosophila, or Monod and Jacob from discovering messenger RNA or, for that matter, from conceiving major works such as “Chance and Necessity” or “Evolutionary tinkering”. In fact, it might even have been an advantage because, in France, the centralized vision of heredity rooted in Mendelian genetics was strongly tempered by the importance traditional biology conferred to the cytoplasm. Not unsurprisingly, therefore, it was in France that a mechanism whereby the cytoplasm regulates genetic information was discovered. It was in France also that the genetics of non-Mendelian elements like mitochondria and the ecological genetics of nucleo-cytoplasmic interactions (e.g. male-sterility, see Chapter 4) were developed. Until the 1980s, evolutionary genetics was chiefly the preserve of Great Britain and the USA. These countries published all the scientific journals in the field (Evolution, American Naturalist, Heredity, Genetics...). Continental Europe, however, built up enough strength to found a European Society of v vi Gene Avatars–The neo-Darwinian Theory of Evolution Evolutionary Biology and edit a society journal (“Journal of Evolutionary Biology”) which, with time, has acquired a good reputation and substantial impact. The first editor, of American origin, worked in Basel (Switzerland); the second was the first author of this book (the editorial office is now based in the Netherlands). A major reason for creating the journal was to counterbalance the dominance of Anglo-American culture in the field. Not that our colleagues were unfriendly. On the contrary, they helped us a lot in developing evolutionary genetics in France. We are deeply indebted to scientists like Bob Allard, Janis Antonovics, Herbert Baker, Arthur Cain, Deborah Charlesworth, Theodosius Dobzhansky, Chris Gliddon, John Harper and Ledyard Stebbins - among many others - for their advice and collaboration. The trouble was that not enough account was taken of the “cultural” differences between “Anglo-Americans” and Europeans in a field of study - evolution - with such close links to ethics and politics. (We shall not discuss the ambiguity of the position of Great Britain which belongs to both worlds). Evolutionary biology tells us that isolation, by preventing a group of individuals from being drowned in the average mass, can foster novelty. Protection from mainstream genetic and evolutionary thinking has certainly helped French biologists retain their strong interest in development. In France, it was obvious - maybe too obvious - that a synthetic theory of evolution had to take ontogeny and non-Mendelian genetics into account long before Gould and Lewontin made such a claim. The original French edition of this book was written in order to acquaint the French reader with the theory of evolution. To the English-speaking reader its interest lies not in any new theory but in the rather unfamiliar emphasis. The authors’ interest in evolutionary genetics was awakened by Georges Valdeyron's course on population genetics at the “Institut National Agronomique” in Paris. This book is dedicated to him. The French edition benefited from the ideas of Anne Atlan, Denis Couvet and Isabelle Olivieri and was improved by suggestions from Beatrice Albert, Irène Till-Bottraud, and many others. The authors are also grateful to John Maynard Smith and Andy Dobson for their judicious comments. Pierre-Henri Gouyon Professor at Paris-Sud University Lecturer at Ecole Polytechnique Consulting Professor at INAPG Director of UPRESA 8079 TABLE OF CONTENTS INTRODUCTION 1 The Biologist's Dream CHAPTER 1 5 Waiting for Darwin From pre-Socratic myths to the transformism of Lamarck 1. Before evolutionism: Metamorphosis, fixism, spontaneous generation 7 2. The concept of evolution. A French discovery 17 3. Lamarck, founding father of transformism 31 CHAPTER 2 45 The Darwinian paradigm 1. The Darwinian revolution 45 2. The origins of genetics: A story about peas 56 3. Biometricians versus geneticists 60 4. Eugenics and Lysenkoism 68 CHAPTER 3 81 Population genetics and ecological genetics 1. Population genetics 81 2. Heyday and decline of ecological genetics 98 3. Gene polymorphism 111 4. Neutral theory and the molecular clock of evolution 124 vii viii Gene Avatars–The neo-Darwinian Theory of Evolution CHAPTER 4 135 The key to genes 1. Male opposition 136 2. Individual, where are you? 141 3. What is life? Erwin Schrödinger's "essentialist" answer 143 4. An update on information 149 5. Genetic information 151 6. Genetic information and avatars 152 7. Individuals: Gene inventions for gene reproduction 155 8. Selection levels 156 9. Rules governing the evolution of information 160 CHAPTER 5 165 Conflict and cooperation 1. The genome, an array of compartments in constant conflict 165 2. Let's play! 175 3. The splendour and woes of sociobiology 180 CHAPTER 6 199 Eros and Thanatos revisited 1. Death at our heels? 200 2. What use is sex? 204 CHAPTER 7 221 What can be done, what can't be done 1. A visit to St. Mark's 221 2. Brachiopod architecture or "Seilacher's triangle" 223 3. Constraints and biological evolution 226 4. Was life wonderful in the Cambrian? 228 5. Struggle for life and a royal race 231 6. Finalism revisited 234 CONCLUSION 243 From an ideal to a tinkered world MATHEMATICAL APPENDICES 245 MA1. Evolutionary pressures 245 MA2. Inbreeding coefficient 247 MA3. Lethal mutations 248 MA4. Genetic load 248 MA5. Fixation of neutral alleles 249 MA6. Game theory 250 Contents ix GLOSSARY 255 BIBLIOGRAPHY 263 INDEX 269 GENE AVATARS THE NEO-DARWINIAN THEORY OF EVOLUTION Introduction THE BIOLOGIST'S DREAM In the 4th century Saint Augustine wrote: "What then is time? If no one asks me, I know; but if I am asked and wish to explain, I do not know." 1 Augustine's query about time seems to apply also to life. Can any biologist claim to know the ultimate definition of life? If he did, he might be offered an honorary chair on the National Ethics Committee but it is more likely that he would be in real danger of taking himself for yet another Faust or successor to Dr. Frankenstein. Would he not have acquired the knowledge and thus the power held by the gods? Would he not have become God? These epistemological and metaphysical issues have not stopped biologists from pursuing their quest to understand living things, nor prevented the deep changes that have occurred during the last two centuries in a field of biology - reproduction and heredity - that has always fascinated mankind. We are far from Montaigne's outcry (Essays, Book II): What kind of monster is the drop of seed from which we are produced and that encapsulates the impressions not only of bodily form but also of the thoughts and inclinations of our fathers? Where does this drop of water harbour these infinite forms? and how does it pass on those similarities that progress in so bold and disordered a fashion that the great-grandson looks like his great-grandfather, the nephew like his uncle? Jean Rostand (1894-1977), a French biologist and prolific author, considered this passage by Montaigne exceptional on many counts. It asks how not only physical characters are passed on but also mental traits. It conveys the process' capricious nature and the onlooker's feeling of surprise 1 2 Gene Avatars–The neo-Darwinian Theory of Evolution and alarm. It is a milestone we can use to judge how far our understanding has progressed over the last four centuries. Modern science has unveiled many of the secrets of reproduction and provided answers (albeit rudimentary ones) to the questions: "Why are we - living beings, human beings - here?", "Why are we born to die?", "Is there a reason to life?" It has also provided tools for modifying human inheritance, i.e. the genome. Part of the biologist's dream is embodied in the techniques of genetic engineering. Some of our contemporaries fear this dream will turn into a nightmare. Where will biological science and techniques take us? Might they not reach down to the very foundations of life and shatter them? The spectres of Hiroshima and Nagasaki still haunt many minds, imparting virulence to the claims of ecologists and increasing fear of all that is undertaken in genetic engineering. There are Ethics Committees everywhere, in hospitals, research departments, government institutions, and international organisations. Ethical issues are being introduced into the syllabuses of schools, universities and polytechnics. Our intention is not to discredit these initiatives; all efforts to make research-workers, practitioners, and citizens more conscious of - and responsible for - their individual and collective behaviour are welcome.