Evolution: A Developmental Approach

PART I Foundations 3

1 Introduction 4

1.1 From Darwin to Development 4

1.2 Development; and Evolutionary Changes in Development 9

1.3 Development and the Realm of Multicellularity 11

2 What is Evo-Devo? 15

2.1 Forerunners of Evo-Devo 15

2.2 Nineteenth-Century Comparative Embryology 16

2.3 Diverse Antecedents—1900–1980 19

2.4 Conclusions from History; Messages for the Present 24

2.5 The Advent of Evo-Devo in the 1980s 25

2.6 Broad and Narrow Views of Evo-Devo 27

2.7 Too Few Laws, Too Many Facts? 28

3 Development, Cells and Molecules 34

3.1 Analysing the Developing Organism 34

3.2 Cells and Development: The Basics 37

3.3 Genes: Structure, Expression and Developmental Function 40

3.4 Signalling Pathways Within and Between Cells 45

3.5 Signalling: From Cell to Embryo 48

3.6 Long-Range Signalling and Developmental Processes 51

4 Natural Populations 54

4.1 The Ecological Theatre and the Evolutionary Play 54

4.2 Types of Creature; Types of Population 55

4.3 Spatial Structure 60

4.4 Age Structure 64

4.5 Genetic Structure 65

4.6 Natural Selection 67

PART II Developmental Repatterning 75

5 Mutation and Developmental Repatterning 77

5.1 Mutation in Terms of Altered DNA Sequence 77

5.2 Mutation in Terms of Proximate Functional Consequences 80

5.3 Developmental Repatterning at Molecular and Higher Levels 82

5.4 Developmental Repatterning at the Level of the Whole Organism 88

5.5 Developmental Repatterning and Fitness 89

6 Heterochrony 93

6.1 What is Heterochrony? 93

6.2 Types and Levels of Heterochrony 94

6.3 Heterochrony at the Organismic Level 95

6.4 Heterochrony at the Molecular Level 99

6.5 Heterochrony and Fitness 102

7 Heterotopy 106

7.1 What is Heterotopy? 106

7.2 Heterotopic Processes Involving Left-Right Asymmetry 107

7.3 Heterotopic Processes Involving the A-P and D-V Axes 112

7.4 Other Types of Heterotopy 116

7.5 Concluding Remarks 119

8 Heterometry 121

8.1 What is Heterometry? 121

8.2 Increasing Relative Size 122

8.3 Decreasing Relative Size 124

8.4 Bi-directional Heterometry 128

8.5 Heterometric Compensation 132

9 Heterotypy 135

9.1 What is Heterotypy? 135

9.2 Altered Products of Developmental Genes 137

9.3 Altered Pigmentation 139

9.4 Altered Morphology and the Origin of Novelty 140

9.5 The Origin of New Cell Types 144

10 The Integrative Nature of Repatterning 148

10.1 Repatterning is a Complex Process 148

10.2 Different Kinds of Repatterning can Produce a Similar Result 149

10.3 Compound Repatterning at a Single Level of Organisation 151

10.4 The Kind of Repatterning can Change Between Levels of Organisation 155

10.5 Categories and Subcategories of Repatterning 157

10.6 The Causes of Repatterning 159

11 Mapping Repatterning to Trees 161

11.1 Pattern, Process, Homology and Trees 161

11.2 The Origin(s) of Animal Segmentation 163

11.3 The Vertebrate Fin-to-Limb Transition 169

11.4 The Origin of Flowers 176

11.5 General Conclusions on Repatterning and Selection 179

PART III The Direction of Evolution 183

12 Adaptation, Coadaptation and Exaptation 185

12.1 Natural Selection on a Continuously Variable Character 185

12.2 Natural Selection on Two Characters; and the Idea of an Adaptive Landscape 190

12.3 Developmental and Functional Coadaptation 191

12.4 Morphological Geometry and Selection 194

12.5 Long-term Evolution and Exaptation 196

13 Developmental Bias and Constraint 200

13.1 A Key Question about Evolution's Direction 200

13.2 Making Sure the Question is about Processes, not Terminology 204

13.3 Dependence versus Independence of Different Characters 208

13.4 Evo-Devo Meets Quantitative Genetics 209

13.5 Developmental Bias and ‘Routine’ Evolution 211

13.6 Developmental Bias and the Origin of Evolutionary Novelties 216

14 Developmental Genes and Evolution 218

14.1 The Direction of Evolution at the Developmental/Genetic Level 218

14.2 Developmental Genes: An Overview 219

14.3 Developmental Genes: Examples 223

14.4 The Hox Genes 225

14.5 Gene-Level Forms of Developmental Bias and Coadaptation 230

14.6 Changes in Regulatory versus Coding Regions of Genes 231

15 Gene Co-option as an Evolutionary Mechanism 234

15.1 What is Gene Co-option? 234

15.2 Co-option in the Evolution of Segments and Eyes 237

15.3 Appendage Evolution and Gene Co-option 241

15.4 Co-option in the Evolution of Zygomorphic Flowers 244

15.5 Evolution of the 'Genetic Toolkit' 245

15.6 Co-option, Exaptation and Developmental Bias 249

16 Developmental Plasticity and Evolution 252

16.1 Types of Developmental Plasticity 252

16.2 Discrete Variants: Winged and Wingless Forms of Insects 254

16.3 Meristic Variation: the Number of Segments in Centipedes 257

16.4 Continuous Variation: Plant Growth 259

16.5 Plasticity and Developmental Genes 260

16.6 The Evolution of Patterns of Plasticity 261

17 The Origin of Species, Novelties and Body Plans 272

17.1 Is Evolution Scale-dependent? 272

17.2 Speciation 273

17.3 The Origin of Novelties 281

17.4 Body Plans I: Overview 284

17.5 Body Plans II: the Origin of the Vertebrates 285

17.6 Body Plans III: the 'Cambrian Explosion' 286

18 The Evolution of Complexity 291

18.1 Defining Complexity 291

18.2 The Lack of a 'Law of Increasing Complexity' 293

18.3 Increases in the Complexity of Adults 299

18.4 Changes in the Complexity of Life-histories 302

18.5 Complexity at the Molecular Level 306

PART IV Conclusions 311

19 Key Concepts and Connections 312

19.1 Introduction: From Original Idea to Mature Scientific Discipline 312

19.2 A List of The Book's Main Points, and the Emergence of Key Concepts 314

19.3 How do They Inter-Connect? 319

20 Prospects 327

20.1 Introduction: From the Present into the Future 327

20.2 Molecular Evo-Devo 327

20.3 Integrative Evo-Devo and General Evolutionary Theory 332

20.4 Wider Challenges 334

Glossary 336

Appendix 1: A Little Bit of History 355

Appendix 2: Naming of Genes and Proteins 359

Appendix 3: Geological Time 363

Appendix 4: Inferring Evolutionary Trees from Comparative Data 366

References 370

Index 383

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