Grenier Jennifer Weatherbee Scott Carroll Sean B. - From DNA to Diversity

2001, 2005 by Sean Carroll

BLACKWELL PUBLISHING

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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.

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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.2nd 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 Groupsgenetics. 2. Variation (Genetics) 3. Animal Population Groupsanatomy & histology. 4. Evolution, Molecular. 5. Gene Expression.

QH 408 C319f 2005] I. Grenier, Jennifer K. II. Weatherbee, Scott D. III. Title.

QH390.C37 2005

57238dc22

2003027991

A catalogue record for this title is available from the British Library.

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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

Preface

The 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 diversityaardvarks and ostriches, butterflies and pythons, dinosaurs, and earthwormsdescended 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 chapternamely, genetics.

Animals diverge from common ancestors through changes in their DNA. The major question, 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 mysterythat 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 development 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 embryology 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 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 13) 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.