From DNA to Diversity

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1 From DNA to Diversity Molecular Genetics and the Evolution of Animal Design Sean B. Carroll Jennifer K. Grenier Scott D. Weatherbee Howard Hughes Medical Institute and University of Wisconsin Madison, Wisconsin b Blackwell Science Technische Universitat Darmstadt FACHBEREICH 10 BIOLOGfE Bibllothek SchnittspahnstraBe 10 D Darmstadt friv.-nr.

2 Contents Chapter 1 A Brief History of Animals 1 Chapter 2 The Genetic Toolkit for Development 15 Chapter 3 Building Animals _ 51 Chapter 4 Evolution of the Toolkit 97 Chapter 5 Diversification of Body Plans and Body Parts 123 Chapter 6 The Evolution of Morphological Novelties 149 Chapter 7 From DNA to Diversity: The Primacy of Regulatory Evolution 173 Glossary 197 Index 203

3 ble of Contents PREFACE' xiii 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 Selected Readings 13 CHAPTER 2 The Genetic Toolkit for Development 15 Before the Toolkit Organizers, Fields, and Morphogens 15 The Genetic Toolkit 18 The Drosophila Toolkit 19 Classifying genes according to their developmental function 19 Homeotic genes and segmental identity 19 The homeobox 26 Field-specific selector genes 26 Compartment selector genes 28 Cell-type-specific selector genes 31 Formation of the body axes 32 Systematic searches for developmental genes in Drosophila 32 The anteroposterior axis 33 The dorsoventral axis 35 Expression of toolkit genes 35 Toolkit gene products: transcription factors and signaling pathway components 36 Pleiotropy of toolkit genes 39 Sharing of the Genetic Toolkit Among Animals 43 Hox genes 43 Field- and cell-type-specific selector genes 44 Signaling pathways: classical organizers and morphogens 46 The Toolkit and Animal Design 47 Selected Readings 48 CHAPTER 3 Building Animals 51 Gene Regulation in Metazoans 51 The Architecture of Genetic Regulatory Hierarchies 53 General features and approach 53 Regulatory logic pathways, circuits, batteries, feedback loops, networks, and the connectivity of genes 55

4 Model regulatory hierarchies and the key genetic switches that operate them 57 The Insect Body Plan 57 From egg to segments: the anteroposterior coordinate system 58 Generation of maternal transcription factor gradients 60 Transcriptional activation of and cross-regulation by gap genes 60 Initiation of periodic pair-rule gene expression 6l Regulation of segment polarity genes by pair-rule proteins 62 General lessons from the segmentation genes 62 The dorsoventral axis coordinate system 65 The Hox ground plan 65 Secondary fields: integrating the anteroposterior and dorsoventral coordinate systems 68 The limb fields 69 The wing primordia 69 The salivary gland 69 Neural and muscle precursors 70 Patterning within secondary fields: organizing signals and selector genes 71 The anteroposterior coordinate system 72 The dorsoventral coordinate system 72 Signal integration by the vestigial field-specific selector gene 72 Combinatorial regulation of wing patterning by signaling proteins and the Vg/Sd selector proteins 74 The response to organizing signals 74 The action of the Vg/Sd selector genes 74 The modification of regulatory hierarchies in secondary fields by Hox genes 75 The Vertebrate Body Plan 77 The anteroposterior axis: somite formation and segmentation 77 The vertebrate Hox ground plan 80 Vertebrate limb development ; 82 Positioning of the limb buds along the rostrocaudal axis 84 Outgrowth of the limb bud: dorsoventral and anteroposterior regulatory hierarchies 84 Integration of organizing signals to form the proximodistal axis and deployment of Hox genes in the limb field 87 Regulatory networks controlling the differentiation of major limb pattern elements 89 The regulation of forelimb and hindlimb identity by selector genes 89 Review: The General Logic and Mechanisms Controlling Gene Expression in Cellular Fields 90 Selected Readings 92

5 CHAPTER 4 Evolution of the Toolkit 97 The History of Gene Families 98 r Conservation of developmental regulatory genes: phylogenetic >' inferences about animal ancestors 98 Gene duplication.;., 101 Mapping gene duplication events onto an animal phylogeny 104 Gene divergence 105 Assembly of the toolkit: the first animals 105 Case Study: Evolution of the Hox Complex Expansion of the Hox complex 108 The ParaHox genes: a sister complex to the Hox genes 110 New functions for some insect Hox genes '., Ill Interpreting the Toolkit: Inferences About Animal Evolution 112 Expansion of the toolkit and the evolution of morphological complexity 112 Conserved genes, conserved biochemical functions 113 Conserved developmental functions: rebuilding the bilaterian ancestor from phylogenetic inference 114 The Toolkit as Developmental Potential 117 Selected Readings 119 CHAPTER 5 Diversification of Body Plans and Body Parts 123 Diversity of Anterior/Posterior Body Organization within Arthropods and Vertebrates 124 Evolution of the genetic control of segmentation in arthropods 125 Shifts in trunk Hox gene expression that mirror changes in arthropod body architecture 127 Hox genes and the evolution of arthropod heads 130 Annelid Hox expression patterns 131 Correlation of vertebrate axial patterning with Hox expression domains 131 How do Hox domains shift during evolution? 133 Morphological Diversity Within a Conserved Body Plan 135 Evolution of the limbless insect abdomen 135 Evolution of insect wing number 136 Diversification of insect wing morphology 139 Modulations in Hox expression patterns within fields that contribute to insect diversity 140 Vertebrate limb diversity: regulatory changes downstream of other selector genes 142 Regulatory Evolution and the Diversification of Homologous Body Parts 145 Selected Readings 146

6 CHAPTERS The Evolution of Morphological Novelties 149 What Is Morphological Novelty? 150 Novel Functions from Older Morphological Structures 150 Epithelial appendages: scales, feathers, and hair 150 The evolution of insect wings from dorsal leg structures 152 Butterfly wing color scales: an evolutionary canvas 154 Evolution of the butterfly eyespot 155 The Evolution of Vertebrate Novelties 159 Fins to limbs: paired appendages and the tetrapod hand 159 Evolution of the neural crest and the vertebrate brain 161 Evolution of the notochord 163 Evolution of Radical Body Plan Changes 163, Loss of the ascidian tail: a chordate lacking chordate features 163 Limbless'tetrapods, or how the snake lost its legs 165 Evolution of the echinoderm body plan 166 Regulatory Evolution and the Origin of Novelties 167 Selected Readings 169 CHAPTER 7 From DNA to Diversity: The Primacy of Regulatory Evolution Why Is Regulatory Evolution a Primary Force in Morphological Evolution? 173 The Function and Evolution of Cfe-Regulatory DNA 175 Functions of c/s-regulatory elements 175 Evolution of czs-regulatory elements 175 De novo evolution of c\s-regulatory elements from preexisting nonfunctional DNA sequences 176 Evolution ofcis-regulatory elements from existing elements 180 The evolution of gene repression versus gene activation 181 Case studies in czs-regulatory evolution 182 Conservation of functional elements among widely divergent taxa 182 The dynamics of sequence turnover in cis- regulatory DNA 183 Functional modification of cis- regulatory DNA sequences 186 The Role of Czs-Regulatory DNA in Morphological Variation and the Response to Selection 186 Cryptic genetic variation and the potential for morphological evolution 188 The Evolution of Regulatory DNA and Morphological Diversity 190 Extrapolating from bristles to body plans 190 Selected Readings 194 GLOSSARY 197 INDEX 203

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