EDITED BY MASSIMO PIGLIUCCI AND GERD B. MÜLLER E V O L U T I O N E V O L U T I O N E V O L U T I O N E V O L U T I O N EE VV OO LL UU TT II OO NN T H E E X T E N D E D SY N T H E S I S Evolution—the Extended Synthesis EVOLUTION—THE EXTENDED SYNTHESIS edited by Massimo Pigliucci and Gerd B. Müller The MIT Press Cambridge, Massachusetts London, England © 2010 Massachusetts Institute of Technology All rights reserved. No part of this book may be reproduced in any form by any electronic or mechanical means (including photocopying, recording, or information storage and retrieval) without permission in writing from the publisher. MIT Press books may be purchased at special quantity discounts for business or sales promotional use. For information, please email [email protected] or write to Special Sales Department, The MIT Press, 55 Hayward Street, Cambridge, MA 02142. This book was set in Times Roman by Toppan Best-set Premedia Limited. Printed and bound in the United States of America. Library of Congress Cataloging-in-Publication Data Evolution—the extended synthesis / edited by Massimo Pigliucci and Gerd B. Müller. p. cm. Includes bibliographical references and index. ISBN 978-0-262-51367-8 (pbk. : alk. paper) 1. Evolution (Biology) 2. Evolutionary genetics. 3. Developmental biology. I. Pigliucci, Massimo, 1964– II. Müller, Gerd B. QH366.2.E8627 2010 576.8—dc22 2009024587 10 9 8 7 6 5 4 3 2 1 Contents Preface vii I INTRODUCTION 1 1 Elements of an Extended Evolutionary Synthesis 3 Massimo Pigliucci and Gerd B. Müller II VARIATION AND SELECTION 19 2 Reconsidering the Importance of Chance Variation 21 John Beatty 3 High-Dimensional Fitness Landscapes and Speciation 45 Sergey Gavrilets 4 Multilevel Selection and Major Transitions 81 David Sloan Wilson III EVOLVING GENOMES 95 5 Integrating Genomics into Evolutionary Theory 97 Gregory A. Wray 6 Complexities in Genome Structure and Evolution 117 Michael Purugganan IV INHERITANCE AND REPLICATION 135 7 Transgenerational Epigenetic Inheritance 137 Eva Jablonka and Marion J. Lamb 8 Niche Inheritance 175 John Odling-Smee vi Contents 9 Chemical, Neuronal, and Linguistic Replicators 209 Chrisantha Fernando and Eörs Szathmáry V EVOLUTIONARY DEVELOPMENTAL BIOLOGY 251 10 Facilitated Variation 253 Marc W. Kirschner and John C. Gerhart 11 Dynamical Patterning Modules 281 Stuart A. Newman 12 Epigenetic Innovation 307 Gerd B. Müller VI MACROEVOLUTION AND EVOLVABILITY 333 13 Origination Patterns and Multilevel Processes in Macroevolution 335 David Jablonski 14 Phenotypic Plasticity 355 Massimo Pigliucci 15 Evolution of Evolvability 379 Günter P. Wagner and Jeremy Draghi VII PHILOSOPHICAL DIMENSIONS 401 16 Rethinking the Structure of Evolutionary Theory for an Extended Synthesis 403 Alan C. Love 17 The Dialectics of Dis/Unity in the Evolutionary Synthesis and Its Extensions 443 Werner Callebaut Contributors 483 Index 485 Preface The biological sciences evolve at a perplexing pace. Since the mid- twentieth century we have witnessed the molecular revolution, a dra- matic technical turn in all fi elds of biology, and the rise and spread of computation, jointly leading to vast amounts of new data, concepts, and models about the organic world. Fundamentally different kinds of infor- mation are now available as compared with the time of the last major conceptual integration in the biosciences, the Modern Synthesis of the 1930s and 1940s—memorably summarized by Julian Huxley and newly accessible in the companion to this volume. As a consequence, but less noted than many of the spectacular empirical advances, the core theo- retical framework underlying the biological sciences is undergoing ferment. Evolutionary theory, as practiced today, includes a consider- able number of concepts that were not part of the foundational structure of the Modern Synthesis. Which of these will actually coalesce into a new kind of synthesis, augmenting the traditional framework in a sub- stantial fashion, is a major challenge for the theorists of today. To begin to meet that challenge, a group of 16 prominent evolutionary biologists and philosophers of science convened at the Konrad Lorenz Institute for Evolution and Cognition Research in Altenberg, Austria, in July 2008. The “Altenberg 16,” as the group was labeled by the media, met over three days to discuss the new information, both empirical and theoretical, from a large number of different fi elds. Conceptual change was seen to emerge from traditional domains of evolutionary biology, such as quantitative genetics, as well as from entirely new fi elds of research, such as genomics or EvoDevo. The structure of the present volume refl ects the areas in which the conceptual progress was perceived to be most signifi cant. The modifi cations and additions to the Modern Synthesis presented in this volume are combined under the term Extended Synthesis, not viii Preface because anyone calls for a radically new theory, but because the current scope and practice of evolutionary biology clearly extend beyond the boundaries of the classical framework. The Altenberg group jointly con- cluded that by incorporating the new results and insights into our under- standing of evolution, the explanatory power of evolutionary theory is greatly expanded within biology and beyond. As is the nature of science, some of the new ideas will stand the test of time, while others will be substantially modifi ed over the course of the next few years. Nonetheless, the authors agree that there is much justifi ed excitement in evolutionary biology today. This is a propitious time to engage the scientifi c commu- nity in a vast interdisciplinary effort to further our understanding of how life evolves. An extended evolutionary framework will be key for this endeavor. The editors wish to thank all those who made this work possible. Foremost, we express our gratitude to the workshop participants and authors who contributed their expertise in so many areas of evolution- ary biology. We are grateful to the staff of the KLI for their dedicated assistance in preparing and running the workshop, and we are equally grateful to the devoted editors at the MIT Press—Katherine Almeida, Susan Buckley, and Bob Prior—without whose experience, patience, and encouragement this volume and its companion would not have happened. I INTRODUCTION