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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 Groups—genetics. 2. Variation (Genetics) 3. Animal Population Groups—anatomy & histology. 4. Evolution, Molecular. 5. Gene Expression.

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

QH390.C37 2005 572.8'38—dc22 2003027991

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

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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 toolkit—organizers, 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 Hox complex 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

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 cz's-regulatory DNA 215

The evolution of regulatory DNA and morphological diversity 230

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