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From DNA to diversity: molecular genetics and the evolution of animal design PDF

270 Pages·2010·59.451 MB·English
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FDTA01 7/14/04 16:35 Page x FDTA01 7/14/04 16:35 Page i From DNA to Diversity FDTA01 7/14/04 16:35 Page ii To our families “From DNA to Diversity is written for a general audience, including undergraduates, with an interest in developmental and evolutionary biology, and it is a joy to read. Using striking examples, the authors summarize the current state of thinking on the interconnectedness between developmental genetics and evolutionary diversification.” Axel Meyer, University of Konstanz; Nature “This book helps to fill a gap in the teaching of evolutionary theory that arose because developmental biology was not a direct participant in the evolutionary synthesis....This is an outstanding account of the latest findings in molecular developmental biology.” James W. Valentine, Professor Emeritus, University of California, Berkeley “The authors have done an excellent job of distilling the large and complex literature on molecular genetics that is pertinent to understanding how gene networks evolve...The writing is consistently clear, concise, and engaging.” Gregory A. Wray, Duke University; Science “Carroll, Weatherbee, and Grenier have produced a wonderful and exciting introduction to the field of evolutionary developmental biology...Newcomers and aficionados will find this a compelling read.” Martin J. Cohn, University of Florida; Evolution and Development “...this is one book that everybody should read who wants to know why ‘evo-devo’ is such a hot topic right now.” Manfred Laubichler, Arizona State University “From DNA to Diversity can be, and should be read by College and University students as well as scientists out of the field, who want to be informed of what is new and promising in biology.” Jean Deutsch, Universite Phillippe et Marie Curie, Paris; BioEssays FDTA01 7/14/04 16:35 Page iii From DNA to Diversity Molecular Genetics and the Evolution of Animal Design 2nd edition Sean B. Carroll Jennifer K. Grenier Scott D. Weatherbee Howard Hughes Medical Institute and University of Wisconsin Sloan Kettering Institute, New York FDTA01 7/14/04 16:35 Page iv © 2001, 2005 by Sean Carroll BLACKWELL PUBLISHING 350 Main Street, Malden, MA 02148-5020, USA 108 Cowley Road, Oxford OX4 1JF, UK 550 Swanston Street, Carlton, Victoria 3053, Australia The right of Sean B. Carroll, Jennifer K. Grenier, and Scott. D. Weatherbee to be identified as the Authors of this Work has been asserted in accordance with the UK Copyright, Designs, and Patents Act 1988. All rights reserved. No part of this publication may be reproduced, stored in a retrieval system, or transmitted, in any form or by any means, electronic, mechanical, photocopying, recording or otherwise, except as permitted by the UK Copyright, Designs, and Patents Act 1988, without the prior permission of the publisher. First edition published 2001 by Blackwell Publishing Ltd Second edition published 2005 Library of Congress Cataloging-in-Publication Data Carroll, Sean B. From DNA to diversity: molecular genetics and the evolution of animal design / Sean B. Carroll, Jennifer K. Grenier, Scott D. Weatherbee.a2nd ed. p. ; cm. Includes bibliographical references and index. ISBN 1-4051-1950-0 (pbk. : alk. paper) 1. Evolutionary genetics. 2. Molecular genetics. 3. Biological diversity. 4. Morphology (Animals) [DNLM: 1. Animal Population Groupsagenetics. 2. Variation (Genetics) 3. Animal Population Groupsaanatomy & histology. 4. Evolution, Molecular. 5. Gene Expression. QH 408 C319f 2005] I. Grenier, Jennifer K. II. Weatherbee, Scott D. III. Title. QH390.C37 2005 572.8′38adc22 2003027991 A catalogue record for this title is available from the British Library. Set in 10/12pt Garamond by Graphicraft Limited, Hong Kong Printed and bound in the United Kingdom by The Bath Press The publisher’s policy is to use permanent paper from mills that operate a sustainable forestry policy, and which has been manufactured from pulp processed using acid-free and elementary chlorine-free practices. Furthermore, the publisher ensures that the text paper and cover board used have met acceptable environmental accreditation standards. For further information on Blackwell Publishing, visit our website: http://www.blackwellpublishing.com FDTA01 7/14/04 16:35 Page v Contents PREFACE . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .vii CHAPTER 1 A Brief History of Animals........................................................................1 Animal origins and the fossil record..............................................................2 The animal tree..............................................................................................6 General features of animal design and diversity...........................................8 Evolution and development: DNA and diversity........................................13 CHAPTER 2 The Genetic Toolkit for Development..................................................17 Before the toolkitaorganizers, fields, and morphogens............................18 The genetic toolkit.......................................................................................20 Sharing of the genetic toolkit among animals.............................................46 The toolkit and animal design.....................................................................51 CHAPTER 3 Building Animals......................................................................................55 Gene regulation in metazoans.....................................................................55 The architecture of genetic regulatory hierarchies......................................57 The insect body plan....................................................................................61 The vertebrate body plan.............................................................................83 Review: the general logic and mechanisms controlling gene expression in cellular fields.....................................................................95 CHAPTER 4 Evolution of the Toolkit........................................................................103 The history of gene families.......................................................................104 Case study: evolution of the Hoxcomplex................................................114 Interpreting the toolkit: inferences about animal evolution.....................119 The toolkit as developmental potential.....................................................127 CHAPTER 5 Diversification of Body Plans and Body Parts..................................131 Diversity of anterior/posterior body organization within arthropods and vertebrates....................................................................132 Morphological diversity within a conserved body plan............................142 Regulatory evolution and the diversification of homologous body parts...............................................................................................154 FDTA01 7/14/04 16:35 Page vi vi Contents CHAPTER 6 The Evolution of Morphological Novelties........................................159 What is morphological novelty?.................................................................160 Novel functions from older morphological structures..............................161 The evolution of vertebrate novelties........................................................170 Evolution of radical body plan changes....................................................178 Regulatory evolution and the origin of novelties......................................185 CHAPTER 7 Morphological Variation and Species Divergence...........................191 Evolution of animal color patterns............................................................192 Nodal points in regulatory networks and the evolution of character number and pattern................................................................201 Qualitative and quantitative aspects of skeletal evolution in stickleback fish.......................................................................................205 More variation than meets the eye: cryptic genetic variation and the potential for morphological evolution.............................................206 Regulatory evolution and species divergence...........................................208 CHAPTER 8 From DNA to Diversity: The Primacy of Regulatory Evolution.....213 Why is regulatory evolution a primary force in morphological evolution?................................................................................................213 The function and evolution of cis-regulatory DNA...................................215 The evolution of regulatoryDNAand morphological diversity...............230 GLOSSARY...............................................................................................................................239 INDEX......................................................................................................................................245 FDTA01 7/14/04 16:35 Page vii Preface T he Earth is now populated by between 1 million and perhaps as many as 20 million animal species, which represent probably less than 1% of all animal species that have ever existed. An even more remarkable fact is that all of this diversityaaardvarks and ostriches, butterflies and pythons, dinosaurs, and earthwormsadescended from a common bilaterally symmetrical ancestor that lived in Precambrian seas more than 540 million years ago. Traditionally approached through paleontology, systematics, and comparative anatomy, the story of animal evolution has, until recently, been sorely missing one huge chaptera namely, genetics. Animals diverge from common ancestors through changes in their DNA. The major ques- tion, then, is, Which changes in DNA account for morphological diversity? The answer to this question has eluded us for the half-century since the Modern Synthesis was proposed and the structure of DNA was discovered. Although many reasons exist to explain this omission, foremost among them is that biology first had to address another central genetic mysterya that is, which genes out of the thousands in any species control morphology? One of the most important biological discoveries of the past two decades is that most animals, no matter how divergent in form, share specific families of genes that regulate major aspects of body pattern. The discovery of this common genetic “toolkit” for animal develop- ment has had two major implications for researchers. First, it has enabled biologists to uncover widely conserved molecular, cellular, and developmental processes whose existence was concealed by previously incomparable anatomies. Second, it has focused the study of the genetic basis of animal diversity on how the number, regulation, and function of genes within the toolkit have changed over the course of animal evolution. The genetic picture of morphological diversity presented in this book is highly influenced by the legacy of previous successes of genetic logic. The mysteries of enzyme induction in bacteria and bacteriophage life cycles were, through formal genetic logic and molecular biology, ultimately reduced to elegant genetic switches that determined the on/off state of groups of genes. This success laid the foundation for understanding the regulation of genes in different cell types of multicellular organisms and, in turn, the regulation of genes in space and over time during the development of individual organisms. Similarly, recent advances in understanding how the toolkit operates in the design of just a few model species has laid the foundation for studies of the evolution of a wide variety of animal structures and patterns. The presentation in this book lies at the intersection of evolutionary biology with embry- ology and genetics. Comprehensive treatment of any of these long-established, fast-growing disciplines can be found in full textbooks dedicated to each. Because our goal is to elucidate general principles about the genetic basis of morphological change, we will focus on those FDTA01 7/14/04 16:35 Page viii viii Preface genes, developmental processes, and taxa that are best known and best illustrate these principles. The book is organized into two parts. The first part (Chapters 1–3) focuses on the history of animals and on animal developmental genetics and regulatory mechanisms. We first examine some of the major trends in animal design and evolution illustrated in the fossil record and by modern forms (Chapter 1). Next, we take an inventory of the genetic toolkit for the development of model species (Chapter 2). Finally, we analyze the regulation and function of these genes in the complex hierarchies that govern animal development (Chapter 3). This crucial background knowledge of the major transitions in animal evolution and the genetic logic of animal design sets the stage for the analysis of mechanisms of morphological evolution. The second part of the book examines the genetic mechanisms underlying the evolution of animals at different morphological levels. We take a case study approach by focusing on the best-understood examples of the evolution of the genetic toolkit, the diversity of body plans and body parts, and novel structures. In the final chapter, we discuss why and how changes in gene regulation have played a primary role in the evolution of diversity across the morphological spectrumafrom small-scale differences within or between species, to the large-scale differences that distinguish higher taxa. We have provided selected references for further reading at the end of each chapter. By no means should these citations (or this book) be taken as the primary or exclusive references on a topic. For both brevity and to circumvent questions of priority in ideas or evidence, we have avoided attributions to specific authors in the text. One of the inspirations for our approach was Mark Ptashne’s classic A Genetic Switch, in which many of the basic physiological and molecular principles of gene regulation were illuminated by focusing on the bacteriophage λ. In the preface, Ptashne stated that “one of the charms of molecular biology is that the answers it provides to fundamental questions for the most part can be easily visualized.” Few fields in biology can rival the aesthetic appeal of the new comparative embryology. Indeed, the visualization of members of the genetic toolkit in action during the development of different species has already become a surrogate for analyzing final forms. For those who find conceptual beauty in the logic and molecular anatomy of genetic switches, the genetic switches controling animal anatomy may be even more appealing. Not only do they control the striking patterns of gene expression within developing embryos, but as we shall see, they are also key to understanding how the won- derful, but presently dwindling, diversity of animal forms has evolved. CHANGES IN THE SECOND EDITION The revision and expansion of From DNA to Diversity for this second edition is driven by advances on many fronts. Increased understanding of developmental mechanisms, system- atic exploration and comparisons of animal genomes, and inquiries into new models of morphological evolution have provided a wealth of case studies from which we have selected new material. Much of the new coverage in this edition is found in the second part of the book, which has been expanded to five chapters (Chapters 4–8) from four in the first edition. Information and references have been updated throughout the book. Again, we stress that these citations are selective and that neither they nor this book should be taken as the primary or exclusive reference on a topic.

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