evolution THIRD EDITION DOUGLAS J. FUTUYMA Stony Brook University Chapter 20, "Evolution of Genes and Genomes" by Scott V. Edwards, Harvard University Chapter 21, "Evolution and Development" by John R. True, Stony Brook University SINAUER ASSOCIATES, INC. •Publishers Sunderland, Massachusetts U.S.A. © 2013 Sinauer Associates, Inc. This material cannot be copied, reproduced, manufactured or disseminated in any form without express written permission from the publisher. 00_EVOL3E_Frontmatter_U&lc.indd iii 2/14/13 8:05 AM Brief Contents 1 Evolutionary Biology 1 2 The Tree of Life: Classifi cation and Phylogeny 19 3 Patterns of Evolution 51 4 Evolution in the Fossil Record 77 5 A History of Life on Earth 103 6 The Geography of Evolution 135 7 The Evolution of Biodiversity 161 8 The Origin of Genetic Variation 189 9 Variation: The Foundation of Evolution 217 10 Genetic Drift: Evolution at Random 257 11 Natural Selection and Adaptation 281 12 The Genetic Theory of Natural Selection 309 13 Phenotypic Evolution 347 14 The Evolution of Life Histories 379 15 Sex and Reproductive Success 399 16 Confl ict and Cooperation 427 17 Species 459 18 Speciation 483 19 The Evolution of Interactions among Species 513 20 Evolution of Genes and Genomes 537 21 Evolution and Development 565 22 Macroevolution: Evolution above the Species Level 605 23 Evolutionary Science, Creationism, and Society 631 © 2013 Sinauer Associates, Inc. This material cannot be copied, reproduced, manufactured or disseminated in any form without express written permission from the publisher. 00_EVOL3E_Frontmatter_U&lc.indd vi 2/14/13 8:05 AM Contents CHAPTER 1 CHAPTER 3 Evolutionary Biology 1 Patterns of Evolution 51 What Is Evolution? 2 Inferring the History of Character Evolution 52 Before Darwin 4 Some Patterns of Evolutionary Change Inferred from Charles Darwin 5 Systematics 53 Darwin’s Evolutionary Theory 6 Most features of organisms have been modifi ed from pre-existing features 55 Philosophical Issues 8 Homoplasy is common 56 Ethics, Religion, and Evolution 9 Rates of character evolution differ 60 Evolutionary Theories after Darwin 10 Evolution is often gradual 61 The Evolutionary Synthesis 10 Change in form is often correlated with change in Fundamental principles of evolution 11 function 61 Evolutionary Biology since the Synthesis 12 Similarity among species changes throughout ontogeny 62 How Evolution Is Studied 13 Development and Morphological Evolution 63 Evolution as Fact and Theory 15 Individualization 63 Heterochrony 63 CHAPTER 2 Allometry 64 Heterotopy 66 The Tree of Life: Classifi cation and Increased and decreased complexity 66 Phylogeny 19 Phylogenetic Analysis Documents Evolutionary Trends 67 Classifi cation 21 Many Clades Display Adaptive Radiation 69 Inferring Phylogenetic History 25 Patterns of Evolution in Genes and Genomes 70 Phylogenetic trees 25 Convergent evolution 70 Data for inferring phylogenies 27 Genome size 71 Inferring phylogenies: The method of maximum Duplicated genes and genomes 73 parsimony 30 Parsimony analysis of DNA sequences: An example 32 CHAPTER 4 Statistical methods of phylogenetic analysis 34 Evaluating phylogenetic hypotheses 37 Evolution in the Fossil Record 77 Estimating Time of Divergence 39 Some Geological Fundamentals 78 Gene Trees and Species Trees 42 Plate tectonics 78 Horizontal gene transfer 42 Geological time 79 Incomplete lineage sorting 43 The geological time scale 79 Some Other Aspects of Phylogenetic Analysis 46 The Fossil Record 81 Applications and Extensions of Phylogenetics 47 Evolutionary changes within species 81 Origins of higher taxa 82 The Hominin Fossil Record 90 © 2013 Sinauer Associates, Inc. This material cannot be copied, reproduced, manufactured or disseminated in any form without express written permission from the publisher. 00_EVOL3E_Frontmatter_U&lc.indd vii 2/14/13 8:05 AM VIII CONTENTS Phylogeny and the Fossil Record 95 Geographic Range Limits: Ecology and Evolution 152 Evolutionary Trends 95 Ecological niches 152 Punctuated Equilibria 96 Range limits: An evolutionary problem 154 Rates of Evolution 99 Evolution of Geographic Patterns of Diversity 155 Community convergence 155 CHAPTER 5 Effects of history on patterns of diversity 157 A History of Life on Earth 103 CHAPTER 7 Patterns in the History of Life 104 The Evolution of Biodiversity 161 Before Life Began 104 The Emergence of Life 104 Estimating and Modeling Changes in Biological Diversity 162 Precambrian Life 107 Modeling rates of change in diversity 162 Paleozoic Life: The Cambrian Explosion 111 Diversity in the fossil record 163 Paleozoic Life: Ordovician to Devonian 114 Phylogenetic studies of diversity 164 Marine life 114 Diversity and Disparity through the Phanerozoic 166 Terrestrial life 115 Rates of origination and extinction 169 Paleozoic Life: Carboniferous and Permian 117 Do extinction rates change as clades age? 172 Terrestrial life 117 Causes of extinction 172 The End-Permian mass extinction 118 Mass extinctions 173 Mesozoic Life 119 Diversifi cation 176 Marine life 120 Does species diversity reach equilibrium? 176 Terrestrial plants and arthropods 120 Why are some kinds of organisms more diverse than Vertebrates 122 others? 180 The Cenozoic Era 125 Effects of organisms’ features on diversifi cation 182 Aquatic life 126 Adaptive radiation 183 Terrestrial life 126 Other infl uences on diversity 185 The adaptive radiation of mammals 126 Pleistocene events 129 CHAPTER 8 CHAPTER 6 The Origin of Genetic Variation 189 The Geography of Evolution 135 Genes and Genomes 190 Biogeographic Evidence for Evolution 136 Mutations: An Overview 192 Major Patterns of Distribution 137 Kinds of mutations 193 Historical Factors Affecting Geographic Examples of mutations 197 Distributions 140 Rates of mutation 198 Testing Hypotheses in Historical Biogeography 142 Phenotypic effects of mutations 202 Examples of historical biogeographic analyses 143 Effects of mutations on fi tness 204 The composition of regional biotas 147 The limits of mutation 207 Phylogeography 148 Mutation as a Random Process 208 Pleistocene population shifts 149 Alterations of the Karyotype 209 Modern human origins 149 Polyploidy 209 Chromosome rearrangements 211 © 2013 Sinauer Associates, Inc. This material cannot be copied, reproduced, manufactured or disseminated in any form without express written permission from the publisher. 00_EVOL3E_Frontmatter_U&lc.indd viii 2/14/13 8:05 AM CONTENTS ix CHAPTER 9 Founder effects 265 Genetic drift in real populations 266 Variation: The Foundation of The Neutral Theory of Molecular Evolution 268 Evolution 217 Principles of the neutral theory 269 Support for the neutral theory 271 Sources of Phenotypic Variation 219 Molecular clocks, revisited 272 Genetic and environmental sources of variation 219 Gene Flow and Genetic Drift 273 Nongenetic inherited variation 221 Gene trees and population history 274 Understanding Evolution: Fundamental Principles of Genetic Variation 223 The origin of modern Homo sapiens revisited 276 Frequencies of alleles and genotypes: The Hardy-Weinberg principle 224 CHAPTER 11 An example: The human MN locus 226 The signifi cance of the Hardy-Weinberg principle: Natural Selection and Factors in evolution 227 Adaptation 281 Frequencies of alleles, genotypes, and phenotypes 228 Adaptations in Action: Some Examples 282 Inbreeding 229 Genetic Variation in Natural Populations: The Nature of Natural Selection 284 Individual Genes 231 Design and mechanism 284 Morphology and viability 231 Defi nitions of natural selection 285 Inbreeding depression 232 Natural selection and chance 286 Genetic variation at the molecular level 233 Selection of and selection for 287 Genetic Variation in Natural Populations: The effective environment depends on the organism 287 Multiple Loci 235 Examples of Natural Selection 288 Linkage and linkage disequilibrium 236 Experimental evolution 288 Variation in quantitative traits 239 Male reproductive success 289 Variation among Populations 245 Group selection 290 Patterns of geographic variation 245 Kin selection 291 Gene fl ow 247 Selfi sh genetic elements 292 Allele frequency differences among populations 248 Levels of Selection 292 Human genetic variation 250 Selection of organisms and groups 293 Species selection 294 CHAPTER 10 The Nature of Adaptations 296 Defi nitions of adaptation 296 Genetic Drift: Evolution at Recognizing adaptations 297 Random 257 Adaptive Evolution Observed 301 Random Processes in Evolution 258 What Not to Expect of Natural Selection and Adaptation 304 The Theory of Genetic Drift 258 The necessity of adaptation 304 Genetic drift as sampling error 258 Perfection 304 Coalescence 259 Progress 304 Random fl uctuations in allele frequencies 261 Harmony and the balance of nature 305 Evolution by Genetic Drift 263 Morality and ethics 305 Effective population size 263 © 2013 Sinauer Associates, Inc. This material cannot be copied, reproduced, manufactured or disseminated in any form without express written permission from the publisher. 00_EVOL3E_Frontmatter_U&lc.indd ix 2/14/13 8:05 AM X CONTENTS CHAPTER 12 How genetic correlation affects evolution 362 Can Genetics Predict Long-Term Evolution? 363 The Genetic Theory of Natural Norms of Reaction 366 Selection 309 Canalization 366 Phenotypic plasticity 367 Fitness 310 Evolution of variability 368 Modes of selection 310 Adaptation and Constraint 372 Defi ning fi tness 312 Genetic constraints on adaptation 372 Components of fi tness 313 Can adaptation rescue species from extinction? 373 Models of Selection 315 Directional selection 315 Deleterious