Unit 11 - Evolution 3rd Edition [Ridley] (1).pdf

..  EVOLUTION....  EVOLUTION THIRD EDITION MARK RIDLEY.. © 2004 by Blackwell Science Ltd a Blackwell Publishing company 350 Main Street, Malden, MA 02148-5020, USA 108 Cowley Road, Oxford OX4 1JF, UK 550 Swanston Street, Carlton, Victoria 3053, Australia The right of Mark Rid...

..  EVOLUTION....  EVOLUTION THIRD EDITION MARK RIDLEY.. © 2004 by Blackwell Science Ltd a Blackwell Publishing company 350 Main Street, Malden, MA 02148-5020, USA 108 Cowley Road, Oxford OX4 1JF, UK 550 Swanston Street, Carlton, Victoria 3053, Australia The right of Mark Ridley to be identified as the Author of this Work has been asserted in accordance with the UK Copyright, Designs, and Patents Act 1988. All rights reserved. No part of this publication may be reproduced, stored in a retrieval system, or transmitted, in any form or by any means, electronic, mechanical, photocopying, recording or otherwise, except as permitted by the UK Copyright, Designs, and Patents Act 1988, without the prior permission of the publisher. First published 1993 Second edition 1996 Third edition 2004 Library of Congress Cataloging-in-Publication Data Ridley, Mark. Evolution / Mark Ridley. – 3rd ed. p. cm. Includes bibliographical references (p. ). ISBN 1-4051-0345-0 (pbk.: alk. paper) 1. Evolution (Biology) I. Title. QH366.2.R524 2003 576.8–dc21 2003000140 A catalogue record for this title is available from the British Library. Set in 9.5/12pt Minion by Graphicraft Limited, Hong Kong Printed and bound in Italy by G. Canale & C. SpA, Turin For further information on Blackwell Publishing, visit our website: http://www.blackwellpublishing.com..  Brief Contents Full Contents vii Preface xxii PART 1. INTRODUCTION 1 1. The Rise of Evolutionary Biology 3 2. Molecular and Mendelian Genetics 21 3. The Evidence for Evolution 43 4. Natural Selection and Variation 71 PART 2. EVOLUTIONARY GENETICS 93 5. The Theory of Natural Selection 95 6. Random Events in Population Genetics 137 7. Natural Selection and Random Drift in Molecular Evolution 155 8. Two-locus and Multilocus Population Genetics 194 9. Quantitative Genetics 222 PART 3. ADAPTATION AND NATURAL SELECTION 253 10. Adaptive Explanation 255 11. The Units of Selection 292 12. Adaptations in Sexual Reproduction 313 PART 4. EVOLUTION AND DIVERSITY 345 13. Species Concepts and Intraspecific Variation 347 14. Speciation 381 15. The Reconstruction of Phylogeny 423 16. Classification and Evolution 471 17. Evolutionary Biogeography 492.. vi Brief Contents PART 5. MACROEVOLUTION 521 18. The History of Life 523 19. Evolutionary Genomics 556 20. Evolutionary Developmental Biology 572 21. Rates of Evolution 590 22. Coevolution 613 23. Extinction and Radiation 643 Glossary 682 Answers to Study and Review Questions 690 References 699 Index 733 Color plate section between pp. 70 and 71..  Full Contents Preface xxii PART 1. INTRODUCTION 1 1. The Rise of Evolutionary Biology 3 1.1 Evolution means change in living things by descent with modification 4 1.2 Living things show adaptations 5 1.3 A short history of evolutionary biology 6 1.3.1 Evolution before Darwin 7 1.3.2 Charles Darwin 9 1.3.3 Darwin’s reception 10 1.3.4 The modern synthesis 14 Summary Further reading Study and review questions 2. Molecular and Mendelian Genetics 21 2.1 Inheritance is caused by DNA molecules, which are physically passed from parent to offspring 22 2.2 DNA structurally encodes information used to build the body’s proteins 23 2.3 Information in DNA is decoded by transcription and translation 25 2.4 Large amounts of non-coding DNA exist in some species 27 2.5 Mutational errors may occur during DNA replication 27 2.6 Rates of mutation can be measured 31 2.7 Diploid organisms inherit a double set of genes 33 2.8 Genes are inherited in characteristic Mendelian ratios 34 2.9 Darwin’s theory would probably not work if there was a non-Mendelian blending mechanism of heredity 37 Summary Further reading Study and review questions 3. The Evidence for Evolution 43 3.1 We distinguish three possible theories of the history of life 44 3.2 On a small scale, evolution can be observed in action 45 3.3 Evolution can also be produced experimentally 47 3.4 Interbreeding and phenotypic similarity provide two concepts of species 48.. viii Full Contents 3.5 Ring “species” show that the variation within a species can be extensive enough to produce a new species 50 3.6 New, reproductively distinct species can be produced experimentally 53 3.7 Small-scale observations can be extrapolated over the long term 54 3.8 Groups of living things have homologous similarities 55 3.9 Different homologies are correlated, and can be hierarchically classified 61 3.10 Fossil evidence exists for the transformation of species 64 3.11 The order of the main groups in the fossil record suggests they have evolutionary relationships 65 3.12 Summary of the evidence for evolution 66 3.13 Creationism offers no explanation of adaptation 67 3.14 Modern “scientific creationism” is scientifically untenable 67 Summary Further reading Study and review questions 4. Natural Selection and Variation 71 4.1 In nature, there is a struggle for existence 72 4.2 Natural selection operates if some conditions are met 74 4.3 Natural selection explains both evolution and adaptation 75 4.4 Natural selection can be directional, stabilizing, or disruptive 76 4.5 Variation in natural populations is widespread 81 4.6 Organisms in a population vary in reproductive success 85 4.7 New variation is generated by mutation and recombination 87 4.8 Variation created by recombination and mutation is random with respect to the direction of adaptation 88 Summary Further reading Study and review questions PART 2. EVOLUTIONARY GENETICS 93 5. The Theory of Natural Selection 95 5.1 Population genetics is concerned with genotype and gene frequencies 96 5.2 An elementary population genetic model has four main steps 97 5.3 Genotype frequencies in the absence of selection go to the Hardy– Weinberg equilibrium 98 5.4 We can test, by simple observation, whether genotypes in a population are at the Hardy–Weinberg equilibrium 102 5.5 The Hardy–Weinberg theorem is important conceptually, historically, in practical research, and in the workings of theoretical models 103 5.6 The simplest model of selection is for one favored allele at one locus 104 5.7 The model of selection can be applied to the peppered moth 108 5.7.1 Industrial melanism in moths evolved by natural selection 108 5.7.2 One estimate of the fitnesses is made using the rate of change in gene frequencies 109..  Full Contents ix 5.7.3 A second estimate of the fitnesses is made from the survivorship of the different genotypes in mark–recapture experiments 111 5.7.4 The selective factor at work is controversial, but bird predation was probably influential 112 5.8 Pesticide resistance in insects is an example of natural selection 115 5.9 Fitnesses are important numbers in evolutionary theory and can be estimated by three main methods 118 5.10 Natural selection operating on a favored allele at a single locus is not meant to be a general model of evolution 120 5.11 A recurrent disadvantageous mutation will evolve to a calculable equilibrial frequency 121 5.12 Heterozygous advantage 123 5.12.1 Selection can maintain a polymorphism when the heterozygote is fitter than either homozygote 123 5.12.2 Sickle cell anemia is a polymorphism with heterozygous advantage 124 5.13 The fitness of a genotype may depend on its frequency 127 5.14 Subdivided populations require special population genetic principles 129 5.14.1 A subdivided set of populations have a higher proportion of homozygotes than an equivalent fused population: this is the Wahlund effect 129 5.14.2 Migration acts to unify gene frequencies between populations 130 5.14.3 Convergence of gene frequencies by gene flow is illustrated by the human population of the USA 132 5.14.4 A balance of selection and migration can maintain genetic differences between subpopulations 132 Summary Further reading Study and review questions 6. Random Events in Population Genetics 137 6.1 The frequency of alleles can change at random through time in a process called genetic drift 138 6.2 A small founder population may have a non-representative sample of the ancestral population’s genes 140 6.3 One gene can be substituted for another by random drift 142 6.4 Hardy–Weinberg “equilibrium” assumes the absence of genetic drift 145 6.5 Neutral drift over time produces a march to homozygosity 145 6.6 A calculable amount of polymorphism will exist in a population because of neutral mutation 150 6.7 Population size and effective population size 151 Summary Further reading Study and review questions 7. Natural Selection and Random Drift in Molecular Evolution 155 7.1 Random drift and natural selection can both hypothetically explain molecular evolution 156.. x Full Contents 7.2 Rates of molecular evolution and amounts of genetic variation can be measured 159 7.3 Rates of molecular evolution are arguably too constant for a process controlled by natural selection 164 7.4 The molecular clock shows a generation time effect 167 7.5 The nearly neutral theory 170 7.5.1 The “purely” neutral theory faces several empirical problems 170 7.5.2 The nearly neutral theory of molecular evolution posits a class of nearly neutral mutations 171 7.5.3 The nearly neutral theory can explain the observed facts better than the purely neutral theory 173 7.5.4 The nearly neutral theory is conceptually closely related to the original, purely neutral theory 174 7.6 Evolutionary rate and functional constraint 175 7.6.1 More functionally constrained parts of proteins evolve at slower rates 175 7.6.2 Both natural selection and neutral drift can explain the trend for proteins, but only drift is plausible for DNA 177 7.7 Conclusion and comment: the neutralist paradigm shift 178 7.8 Genomic sequences have led to new ways of studying molecular evolution 179 7.8.1 DNA sequences provide strong evidence for natural selection on protein structure 180 7.8.2 A high ratio of non-synonymous to synonymous changes provides evidence of selection 181 7.8.3 Selection can be detected by comparisons of the dN/dS ratio within and between species 184 7.8.4 The gene for lysozyme has evolved convergently in cellulose- digesting mammals 186 7.8.5 Codon usages are biased 187 7.8.6 Positive and negative selection leave their signatures in DNA sequences 189 7.9 Conclusion: 35 years of research on molecular evolution 190 Summary Further reading Study and review questions 8. Two-locus and Multilocus Population Genetics 194 8.1 Mimicry in Papilio is controlled by more than one genetic locus 195 8.2 Genotypes at different loci in Papilio memnon are coadapted 197 8.3 Mimicry in Heliconius is controlled by more than one gene, but they are not tightly linked 197 8.4 Two-locus genetics is concerned with haplotype frequencies 199 8.5 Frequencies of haplotypes may or may not be in linkage equilibrium 199 8.6 Human HLA genes are a multilocus gene system 203 8.7 Linkage disequilibrium can exist for several reasons 204 8.8 Two-locus models of natural selection can be built 206..  Full Contents xi 8.9 Hitch-hiking occurs in two-locus selection models 210 8.10 Selective sweeps can provide evidence of selection in DNA sequences 210 8.11 Linkage disequilibrium can be advantageous, neutral, or disadvantageous 212 8.12 Wright invented the influential concept of an adaptive topography 214 8.13 The shifting balance theory of evolution 216 Summary Further reading Study and review questions 9. Quantitative Genetics 222 9.1 Climatic changes have driven the evolution of beak size in one of Darwin’s finches 223 9.2 Quantitative genetics is concerned with characters controlled by large numbers of genes 226 9.3 Variation is first divided into genetic and environmental effects 228 9.4 Variance of a character is divided into genetic and environmental effects 231 9.5 Relatives have similar genotypes, producing the correlation between relatives 234 9.6 Heritability is the proportion of phenotypic variance that is additive 235 9.7 A character’s heritability determines its response to artificial selection 236 9.8 Strength of selection has been estimated in many studies of natural populations 240 9.9 Relations between genotype and phenotype may be non-linear, producing remarkable responses to selection 242 9.10 Stabilizing selection reduces the genetic variability of a character 245 9.11 Characters in natural populations subject to stabilizing selection show genetic variation 246 9.12 Levels of genetic variation in natural populations are imperfectly understood 247 9.13 Conclusion 249 Summary Further reading Study and review questions PART 3. ADAPTATION AND NATURAL SELECTION 253 10. Adaptive Explanation 255 10.1 Natural selection is the only known explanation for adaptation 256 10.2 Pluralism is appropriate in the study of evolution, not of adaptation 259 10.3 Natural selection can in principle explain all known adaptations 259 10.4 New adaptations evolve in continuous stages from pre-existing adaptations, but the continuity takes various forms 263 10.4.1 In Darwin’s theory, no special process produces evolutionary novelties 263 10.4.2 The function of an adaptation may change with little change in its form 264 10.4.3 A new adaptation may evolve by combining unrelated parts 265.. xii Full Contents 10.5 Genetics of adaptation 266 10.5.1 Fisher proposed a model, and microscope analogy, to explain why the genetic changes in adaptive evolution will be small 266 10.5.2 An expanded theory is needed when an organism is not near an adaptive peak 268 10.5.3 The genetics of adaptation is being studied experimentally 268 10.5.4 Conclusion: the genetics of adaptation 270 10.6 Three main methods are used to study adaptation 270 10.7 Adaptations in nature are not perfect 272 10.7.1 Adaptations may be imperfect because of time lags 272 10.7.2 Genetic constraints may cause imperfect adaptation 274 10.7.3 Developmental constraints may cause adaptive imperfection 275 10.7.4 Historic constraints may cause adaptive imperfection 281 10.7.5 An organism’s design may be a trade-off between different adaptive needs 284 10.7.6 Conclusion: constraints on adaptation 284 10.8 How can we recognize adaptations? 286 10.8.1 The function of an organ should be distinguished from the effects it may have 286 10.8.2 Adaptations can be defined by engineering design or reproductive fitness 287 Summary Further reading Study and review questions 11. The Units of Selection 292 11.1 What entities benefit from the adaptations produced by selection? 293 11.2 Natural selection has produced adaptations that benefit various levels of organization 294 11.2.1 Segregation distortion benefits one gene at the expense of its allele 294 11.2.2 Selection may sometimes favor some cell lines relative to other cell lines in the same body 295 11.2.3 Natural selection has produced many adaptations to benefit organisms 296 11.2.4 Natural selection working on groups of close genetic relatives is called kin selection 298 11.2.5 Whether group selection ever produces adaptations for the benefit of groups has been controversial, though most biologists now think it is only a weak force in evolution 301 11.2.6 Which level in the hierarchy of organization levels will evolve adaptations is controlled by which level shows heritability 305 11.3 Another sense of “unit of selection” is the entity whose frequency is adjusted directly by natural selection 306..  Full Contents xiii 11.4 The two senses of “unit of selection” are compatible: one specifies the entity that generally shows phenotypic adaptations, the other the entity whose frequency is generally adjusted by natural selection 310 Summary Further reading Study and review questions 12. Adaptations in Sexual Reproduction 313 12.1 The existence of sex is an outstanding, unsolved problem in evolutionary biology 314 12.1.1 Sex has a 50% cost 314 12.1.2 Sex is unlikely to be explained by genetic constraint 315 12.1.3 Sex can accelerate the rate of evolution 316 12.1.4 Is sex maintained by group selection? 318 12.2 There are two main theories in which sex may have a short-term advantage 320 12.2.1 Sexual reproduction can enable females to reduce the number of deleterious mutations in their offspring 320 12.2.2 The mutational theory predicts U > 1 321 12.2.3 Coevolution of parasites and hosts may produce rapid environmental change 323 12.3 Conclusion: it is uncertain how sex is adaptive 327 12.4 The theory of sexual selection explains many differences between males and females 327 12.4.1 Sexual characters are often apparently deleterious 327 12.4.2 Sexual selection acts by male competition and female choice 328 12.4.3 Females may choose to pair with particular males 329 12.4.4 Females may prefer to pair with handicapped males, because the male’s survival indicates his high quality 331 12.4.5 Female choice in most models of Fisher’s and Zahavi’s theories is open ended, and this condition can be tested 332 12.4.6 Fisher’s theory requires heritable variation in the male character, and Zahavi’s theory requires heritable variation in fitness 333 12.4.7 Natural selection may work in conflicting ways on males and females 335 12.4.8 Conclusion: the theory of sex differences is well worked out but incompletely tested 336 12.5 The sex ratio is a well understood adaptation 337 12.5.1 Natural selection usually favors a 50 : 50 sex ratio 337 12.5.2 Sex ratios may be biased when either sons or daughters disproportionately act as “helpers at the nest” 339 12.6 Different adaptations are understood in different levels of detail 341 Summary Further reading Study and review questions.. xiv Full Contents PART 4. EVOLUTION AND DIVERSITY 345 13. Species Concepts and Intraspecific Variation 347 13.1 In practice species are recognized and defined by phenetic characters 348 13.2 Several closely related species concepts exist 350 13.2.1 The biological species concept 351 13.2.2 The ecological species concept 353 13.2.3 The phenetic species concept 354 13.3 Isolating barriers 355 13.3.1 Isolating barriers prevent interbreeding between species 355 13.3.2 Sperm or pollen competition can produce subtle prezygotic isolation 356 13.3.3 Closely related African cichlid fish species are prezygotically isolated by their color patterns, but are not postzygotically isolated 357 13.4 Geographic variation within a species can be understood in terms of population genetic and ecological processes 359 13.4.1 Geographic variation exists in all species and can be caused by adaptation to local conditions 359 13.4.2 Geographic variation may also be caused by genetic drift 360 13.4.3 Geographic variation may take the form of a cline 362 13.5 “Population thinking” and “typological thinking” are two ways of thinking about biological diversity 363 13.6 Ecological influences on the form of a species are shown by the phenomenon of character displacement 366 13.7 Some controversial issues exist between the phenetic, biological, and ecological species concepts 367 13.7.1 The phenetic species concept suffers from serious theoretical defects 368 13.7.2 Ecological adaptation and gene flow can provide complementary, or in some cases competing, theories of the integrity of species 369 13.7.3 Both selection and genetic incompatibility provide explanations of reduced hybrid fitness 373 13.8 Taxonomic concepts may be nominalist or realist 374 13.8.1 The species category 374 13.8.2 Categories below the species level 375 13.8.3 Categories above the species level 376 13.9 Conclusion 377 Summary Further reading Study and review questions 14. Speciation 381 14.1 How can one species split into two reproductively isolated groups of organisms? 382..  Full Contents xv 14.2 A newly evolving species could theoretically have an allopatric, parapatric, or sympatric geographic relation with its ancestor 382 14.3 Reproductive isolation can evolve as a by-product of divergence in allopatric populations 383 14.3.1 Laboratory experiments illustrate how separately evolving populations of a species tend incidentally to evolve reproductive isolation 384 14.3.2 Prezygotic isolation evolves because it is genetically correlated with the characters undergoing divergence 386 14.3.3 Reproductive isolation is often observed when members of geographically distant populations are crossed 387 14.3.4 Speciation as a by-product of divergence is well documented 389 14.4 The Dobzhansky–Muller theory of postzygotic isolation 389 14.4.1 The Dobzhansky–Muller theory is a genetic theory of postzygotic isolation, explaining it by interactions among many gene loci 389 14.4.2 The Dobzhansky–Muller theory is supported by extensive genetic evidence 391 14.4.3 The Dobzhansky–Muller theory has broad biological plausibility 392 14.4.4 The Dobzhansky–Muller theory solves a general problem of “valley crossing” during speciation 394 14.4.5 Postzygotic isolation may have ecological as well as genetic causes 395 14.4.6 Postzygotic isolation usually follows Haldane’s rule 396 14.5 An interim conclusion: two solid generalizations about speciation 399 14.6 Reinforcement 399 14.6.1 Reproductive isolation may be reinforced by natural selection 399 14.6.2 Preconditions for reinforcement may be short lived 401 14.6.3 Empirical tests of reinforcement are inconclusive or fail to support the theory 402 14.7 Some plant species have originated by hybridization 405 14.8 Speciation may occur in non-allopatric populations, either parapatrically or sympatrically 408 14.9 Parapatric speciation 409 14.9.1 Parapatric speciation begins with the evolution of a stepped cline 409 14.9.2 Evidence for the theory of parapatric speciation is relatively weak 411 14.10 Sympatric speciation 411 14.10.1 Sympatric speciation is theoretically possible 411 14.10.2 Phytophagous insects may split sympatrically by host shifts 412 14.10.3 Phylogenies can be used to test whether speciation has been sympatric or allopatric 413 14.11 The influence of sexual selection in speciation is one current trend in research 413.. xvi Full Contents 14.12 Identification of genes that cause reproductive isolation is another current trend in research 415 14.13 Conclusion 417 Summary Further reading Study and review questions 15. The Reconstruction of Phylogeny 423 15.1 Phylogenies express the ancestral relations between species 424 15.2 Phylogenies are inferred from morphological characters using cladistic techniques 425 15.3 Homologies provide reliable evidence for phylogenetic inference, and homoplasies provide unreliable evidence 427 15.4 Homologies can be distinguished from homoplasies by several criteria 430 15.5 Derived homologies are more reliable indicators of phylogenetic relations than are ancestral homologies 431 15.6 The polarity of character states can be inferred by several techniques 433 15.6.1 Outgroup comparison 434 15.6.2 The fossil record 435 15.6.3 Other methods 436 15.7 Some character conflict may remain after cladistic character analysis is complete 436 15.8 Molecular sequences are becoming increasingly important in phylogenetic inference, and they have distinct properties 437 15.9 Several statistical techniques exist to infer phylogenies from molecular sequences 439 15.9.1 An unrooted tree is a phylogeny in which the common ancestor is unspecified 439 15.9.2 One class of molecular phylogenetic techniques uses molecular distances 440 15.9.3 Molecular evidence may need to be adjusted for the problem of multiple hits 442 15.9.4 A second class of phylogenetic techniques uses the principle of parsimony 445 15.9.5 A third class of phylogenetic techniques uses the principle of maximum likelihood 447 15.9.6 Distance, parsimony, and maximum likelihood methods are all used, but their popularity has changed over time 449 15.10 Molecular phylogenetics in action 449 15.10.1 Different molecules evolve at different rates and molecular evidence can be tuned to solve particular phylogenetic problems 449 15.10.2 Molecular phylogenies can now be produced rapidly, and are used in medical research 451 15.11 Several problems have been encountered in molecular phylogenetics 451 15.11.1 Molecular sequences can be difficult to align 452..  Full Contents xvii 15.11.2 The number of possible trees may be too large for them all to be analyzed 452 15.11.3 Species in a phylogeny may have diverged too little or too much 455 15.11.4 Different lineages may evolve at different rates 456 15.11.5 Paralogous genes may be confused with orthologous genes 457 15.11.6 Conclusion: problems in molecular phylogenetics 458 15.12 Paralogous genes can be used to root unrooted trees 459 15.13 Molecular evidence successfully challenged paleontological evidence in the analysis of human phylogenetic relations 460 15.14 Unrooted trees can be inferred from other kinds of evidence, such as chromosomal inversions in Hawaiian fruitflies 463 15.15 Conclusion 466 Summary Further reading Study and review questions 16. Classification and Evolution 471 16.1 Biologists classify species into a hierarchy of groups 472 16.2 There are phenetic and phylogenetic principles of classification 472 16.3 There are phenetic, cladistic, and evolutionary schools of classification 474 16.4 A method is needed to judge the merit of a school of classification 475 16.5 Phenetic classification uses distance measures and cluster statistics 476 16.6 Phylogenetic classification uses inferred phylogenetic relations 479 16.6.1 Hennig’s cladism classifies species by their phylogenetic branching relations 479 16.6.2 Cladists distinguish monophyletic, paraphyletic, and polyphyletic groups 481 16.6.3 A knowledge of phylogeny does not simply tell us the rank levels in Linnaean classification 483 16.7 Evolutionary classification is a synthesis of phenetic and phylogenetic principles 485 16.8 The principle of divergence explains why phylogeny is hierarchical 487 16.9 Conclusion 489 Summary Further reading Study and review questions 17. Evolutionary Biogeography 492 17.1 Species have defined geographic distributions 493 17.2 Ecological characteristics of a species limit its geographic distribution 496 17.3 Geographic distributions are influenced by dispersal 496 17.4 Geographic distributions are influenced by climate, such as in the ice ages 497 17.5 Local adaptive radiations occur on island archipelagos 500 17.6 Species of large geographic areas tend to be more closely related to other local species than to ecologically similar species elsewhere in the globe 503.. xviii Full Contents 17.7 Geographic distributions are influenced by vicariance events, some of which are caused by plate tectonic movements 505 17.8 The Great American Interchange 512 17.9 Conclusion 517 Summary Further reading Study and review questions PART 5. MACROEVOLUTION 521 18. The History of Life 523 18.1 Fossils are remains of organisms from the past and are preserved in sedimentary rocks 524 18.2 Geological time is conventionally divided into a series of eras, periods, and epochs 525 18.2.1 Successive geological ages were first recognized by characteristic fossil faunas 525 18.2.2 Geological time is measured in both absolute and relative terms 526 18.3 The history of life: the Precambrian 529 18.3.1 The origin of life 529 18.3.2 The origin of cells 531 18.3.3 The origin of multicellular life 533 18.4 The Cambrian explosion 535 18.5 Evolution of land plants 538 18.6 Vertebrate evolution 540 18.6.1 Colonization of the land 540 18.6.2 Mammals evolved from the reptiles in a long series of small changes 542 18.7 Human evolution 545 18.7.1 Four main classes of change occurred during hominin evolution 545 18.7.2 Fossil records show something of our ancestors for the past 4 million years 547 18.8 Macroevolution may or may not be an extrapolated form of microevolution 550 Summary Further reading Study and review questions 19. Evolutionary Genomics 556 19.1 Our expanding knowledge of genome sequences is making it possible to ask, and answer, questions about the evolution of genomes 557 19.2 The human genome documents the history of the human gene set since early life 558 19.3 The history of duplications can be inferred in a genomic sequence 559 19.4 Genome size can shrink by gene loss 561..  Full Contents xix 19.5 Symbiotic mergers, and horizontal gene transfer, between species influence genome evolution 563 19.6 The X/Y sex chromosomes provide an example of evolutionary genomic research at the chromosomal level 565 19.7 Genome sequences can be used to study the history of non-coding DNA 567 19.8 Conclusion 569 Summary Further reading Study and review questions 20. Evolutionary Developmental Biology 572 20.1 Changes in development, and the genes controlling development, underlie morphological evolution 573 20.2 The theory of recapitulation is a classic idea (largely discredited) about the relation between development and evolution 573 20.3 Humans may have evolved from ancestral apes by changes in regulatory genes 578 20.4 Many genes that regulate development have been identified recently 579 20.5 Modern developmental genetic discoveries have challenged and clarified the meaning of homology 580 20.6 The Hox gene complex has expanded at two points in the evolution of animals 582 20.7 Changes in the embryonic expression of genes are associated with evolutionary changes in morphology 583 20.8 Evolution of genetic switches enables evolutionary innovation, making the system more “evolvable” 585 20.9 Conclusion 587 Summary Further reading Study and review questions 21. Rates of Evolution 590 21.1 Rates of evolution can be expressed in “darwins,” as illustrated by a study of horse evolution 591 21.1.1 How do population genetic, and fossil, evolutionary rates compare? 593 21.1.2 Rates of evolution observed in the short term can explain speciation over longer time periods in Darwin’s finches 595 21.2 Why do evolutionary rates vary? 596 21.3 The theory of punctuated equilibrium applies the theory of allopatric speciation to predict the pattern of change in the fossil record 599 21.4 What is the evidence for punctuated equilibrium and for phyletic gradualism? 602 21.4.1 A satisfactory test requires a complete stratigraphic record and biometrical evidence 602 21.4.2 Caribbean bryozoans from the Upper Miocene and Lower Pliocene show a punctuated equilibrial pattern of evolution 603.. xx Full Contents 21.4.3 Ordovician trilobites show gradual evolutionary change 605 21.4.4 Conclusion 605 21.5 Evolutionary rates can be measured for non-continuous character changes, as illustrated by a study of “living fossil” lungfish 606 21.6 Taxonomic data can be used to describe the rate of evolution of higher taxonomic groups 609 21.7 Conclusion 611 Summary Further reading Study and review questions 22. Coevolution 613 22.1 Coevolution can give rise to coadaptations between species 614 22.2 Coadaptation suggests, but is not conclusive evidence of, coevolution 616 22.3 Insect–plant coevolution 616 22.3.1 Coevolution between insects and plants may have driven the diversification of both taxa 616 22.3.2 Two taxa may show mirror-image phylogenies, but coevolution is only one of several explanations for this pattern 618 22.3.3 Cophylogenies are not found when phytophagous insects undergo host shifts to exploit phylogenetically unrelated but chemically similar plants 620 22.3.4 Coevolution between plants and insects may explain the grand pattern of diversification in the two taxa 622 22.4 Coevolutionary relations will often be diffuse 623 22.5 Parasite–host coevolution 623 22.5.1 Evolution of parasitic virulence 625 22.5.2 Parasites and their hosts may have cophylogenies 630 22.6 Coevolution can proceed in an “arms race” 632 22.6.1 Coevolutionary arms races can result in evolutionary escalation 634 22.7 The probability that a species will go extinct is approximately independent of how long it has existed 637 22.8 Antagonistic coevolution can have various forms, including the Red Queen mode 638 22.9 Both biological and physical hypotheses should be tested on macroevolutionary observations 640 Summary Further reading Study and review questions 23. Extinction and Radiation 643 23.1 The number of species in a taxon increases during phases of adaptive radiation 644 23.2 Causes and consequences of extinctions can be studied in the fossil record 646 23.3 Mass extinctions 648 23.3.1 The fossil record of extinction rates shows recurrent rounds of mass extinctions 648..  Full Contents xxi 23.3.2The best studied mass extinction occurred at the Cretaceous–Tertiary boundary 651 23.3.3 Several factors can contribute to mass extinctions 653 23.4 Distributions of extinction rates may fit a power law 655 23.5 Changes in the quality of the sedimentary record through time are associated with changes in the observed extinction rate 657 23.6 Species selection 658 23.6.1 Characters that evolve within taxa may influence extinction and speciation rates, as is illustrated by snails with planktonic and direct development 658 23.6.2 Differences in the persistence of ecological niches will influence macroevolutionary patterns 664 23.6.3 When species selection operates, the factors that control macroevolution differ from the factors that control microevolution 665 23.6.4 Forms of species selection may change during mass extinctions 666 23.7 One higher taxon may replace another, because of chance, environmental change, or competitive replacement 669 23.7.1 Taxonomic patters through time can provide evidence about the cause of replacements 669 23.7.2 Two bryozoan groups are a possible example of a competitive replacement 670 23.7.3 Mammals and dinosaurs are a classic example of independent replacement, but recent molecular evidence has complicated the interpretation 671 23.8 Species diversity may have increased logistically or exponentially since the Cambrian, or it may have increased little at all 674 23.9 Conclusion: biologists and paleontologists have held a range of views about the importance of mass extinctions in the history of life 677 Summary Further reading Study and review questions Glossary 682 Answers to Study and Review Questions 690 References 699 Index 733 Color plate section between pp. 70 and 71.. Preface The theory of evolution is outstandingly the most important theory in biology, and it is always a pleasure to be a member, facing in either direction, of the class that is fortunate enough to be studying it. No other idea in biology is so powerful scientifically, or so stimulating intellectually. Evolution can add an extra dimension of interest to the most appealing sides of natural history a we shall see, for example, how modern evolution- ary biologists tend to argue that the existence of sex is the profoundest puzzle of all, and quite possibly a mistake that half the living creatures of this planet would be better off without. Evolution gives meaning to the drier facts of life too, and it is one of the delights of the subject to see how there are ideas as well as facts within the disorienting technicalities of the genetics laboratory, and how deep theories about the history of life can hinge on measurements of the width of a region called “prodissoconch II” in the larval shell of a snail, or the number of ribs in a trilobite’s tail. So great is the depth and range of evolutionary biology that every other classroom on campus must feel (as you can sort of tell) locked in with more superficial and ephemeral materials. The theory of evolution, as I have arranged it here, has four main components. Population genetics provides the fundamental theory of the subject. If we know how any property of life is controlled genetically, population genetics can be applied to it directly. We have that knowledge particularly for molecules (together with some, mainly morphological, properties of whole organisms), and molecular evolution and population genetics are therefore well integrated. Part 2 of the book considers them together. The second component is the theory of adaptation, and it is the subject of Part 3. Evolution is also the key to understanding the diversity of life, and in Part 4 we consider such topics as what a species is, how new species originate, and how to classify and reconstruct the history of life. Finally, Part 5 is about evolution on the grand scale a on a timescale of tens or hundreds of millions of years. We look at the history of life, both genetically and paleontologically, at rates of evolution, and at mass extinctions. Controversy is always tricky to deal with in an introductory text, and evolutionary biology has more than its fair share of it. When I have come to a controversial topic, my first aim has been to explain the competing ideas in such a way that they can be under- stood on their own terms. In some cases (such as cladistic classification) I think the controversy is almost settled and I have taken sides. In others (such as the relative empirical importance of gradual and punctuated change in fossils) I have not. I am well aware that not everyone will agree with the positions I have taken, or indeed with my decisions in some cases not to take a position; but in a way these are secondary matters. The book’s success mainly depends on how well it enables a reader who has not studied the subject much before to understand the various ideas and come to a sensible view- point about them...  Preface xxiii The great (or at any rate, one of the great) events in evolutionary biology as I have been writing the third edition is the way genetics is becoming a macroevolutionary, as well as a microevolutionary, subject. Historically, there has been a good working distinction between evolutionary research on short and long timescales a between micro- and macroevolutionary research. The distinction was one not simply of timescales but of research methods and even institutionalized academic disciplines. Genetics, and experimental methods generally, were used to study evolution on the timescale of research projects a of a few years, at most. That work was done mainly in departments of biology. Long-term evolution, over approximately 10–1,000 million years, was studied by comparative morphology in living and fossil life forms. That work was done more in museums and departments of geology or earth sciences, than in biology departments. I see the distinction between micro- and macroevolutionary research as breaking down, in perhaps three ways. The first is through the use of molecular phylogenetics. A phylogeny is a family tree for a group of species, and they were classically inferred from morphological evidence. Molecular evidence started to be used in the 1960s, but it somehow trapped itself (I caricature a little) in about 20 years of obsessive behavior, as a small number of case studies a particularly human evolution a were endlessly rehashed. Molecular phylogenetics broke out into life as a whole during the 1980s, and the result has been a huge increase in the number of species for which we know, or have evidence concerning, their phylogenetic relations. The research program of molecular phylogenetics may have been established for almost an academic generation, and it is certainly flourishing, but it has still only just begun. A recent estimate is that only about 50,000 of the 1.75 million or so described species have been put in any kind of “minitree” a that is, a phylogenetic tree with their close relations. Sydney Brenner has remarked that the next generation of biologists has the prospect of finding the tree of life, something that all previous generations of post- Darwinian biologists could only dream about. In Chapter 15, we look at how the work is being done. The new phylogenetic knowledge is not only interesting in itself, but is also enabling many other kinds of work that were formerly impossible. We shall see how phylogenies are being exploited in studies of coevolution and biogeography, among other topics. The other two ways in which molecular genetics is being used in macroevolutionary research are more recent. I have added chapters on evolutionary genomics (Chap- ter 19) and “evo-devo” (Chapter 20). The addition of these two chapters in Part 5 of the book is a small symbol of the way macroevolution has become genetic as well as paleo- biological: in my first two editions, Part 5 was almost exclusively paleontological. The introduction of new techniques into the study of macroevolution creates an excitement of its own. It has also resulted in a number of controversies, where the two methods (molecular genetic and paleontological) seem to point to conflicting conclusions. We shall look at several of those controversies, including the nature of the Cambrian explosion and the significance of the Cretaceous–Tertiary mass extinction. This book is about evolution as a “pure” science, but that science has practical applications a in social affairs, in business, in medicine. Stephen Palumbi has recently estimated that evolutionary change induced by human action costs the US economy about $33–50 billion a year (Palumbi 2001a). The costs come from the way microbes.. xxiv Preface evolve resistance to drugs, pests evolve resistance to pesticides, and fish evolve back against our fishing procedures. Palumbi’s estimate is approximate and preliminary, and probably an underestimate. But whatever the exact number is, the economic con- sequences of evolution must be huge. The economic benefits of understanding evolu- tion could be proportionally huge. In this edition I have added a number of special boxes within chapters, on “Evolution and human affairs.” The examples I discuss are only a sample, which happen to fit in with themes in the text. Bull & Wichman (2001) discuss many further examples of “applied evolution,” from directed evolution of enzymes to evolutionary computation. The book is intended as an introductory text, and I have subordinated all other aims to that end. I have aimed to explain concepts, wherever possible by example, and with a minimum of professional clutter. The principal interest, I believe, of the theory of evolution is as a set of ideas to think about, and I have therefore tried in every case to move on to the ideas as soon as possible. The book is not a factual encyclopedia, nor (primarily) a reference work for research biologists. I do not provide many references in the main text, though in this edition I have referred to the sources for the examples in formal “scientific” reference format. For readers who are unfamiliar with this format, I should say that references are given in the way I wrote “Palumbi (2001a)” and “Bull & Wichman (2001)” in the previous paragraph. The reference has the author’s (or authors’) name and a date. In the reference list at the end you will find the full bibliographic details, listing the authors alphabetically. There is also a convention for papers with multiple authors. When a paper has more than two (or three, with some publishers), it is referred to by the name of the first author with an “et al.” and the date: Losos et al. (1998), for example. The “et al.” means “and others.” It is a space-saving device, and is abbreviated to avoid problems with Latin declension. For instance, if the reference is the subject of the sentence the full version would be “Losos et alii (1998) studied lizards....” But other phases require other full versions: “the work of Losos et aliorum (1998)...” or “the work by Losos et aliis (1998).” In all, “al.” could stand for 12–18 full versions. Anyhow, all the authors are usually listed in the main reference list a I say “usually” because some authorial teams have grown so huge that they are not all given. Blackwell house style is that for papers with more than seven authors, the reference list has the first three and then an “et al.” Although I have referred to the specific papers under discussion in the text, I do not give general references there. The reason is that I do not want to spoil the most power- ful textual positions, such as the end of a paragraph or a section, with a list of further reading. The way I have things, those textual positions can be occupied by summary sentences and other more useful matter. The “further reading” section at the end of each chapter is the main vehicle for general references, and for references to other studies like those in the text. I have referred to recent reviews when they exist, and the historic bibliography of each topic can be traced through them. In summary, this new edition contains: two types of box a one featuring practical applications and the other related infor- mation, which supply added depth without interrupting the flow of the text margin comments that paraphrase and highlight key concepts study and review questions to help students review their understanding at the end of each chapter, while new challenge questions prompt students to synthesize the chapter concepts to reinforce the learning at a deeper level..  Preface xxv two new chapters a one on evolutionary genomics and one on evolution and devel- opment bring state-of-the-art information to the coverage of evolutionary study There is also a dedicated website at www.blackwellpublishing.com/ridley which provides an interactive experience of the book, with illustrations downloadable to PowerPoint, and a full supplemental package complementing the book. Scattered margin icons indicate where there is relevant information included on the dedicated website. Finally, my thanks to the many people who have helped me with queries and reviews as I have prepared the new edition a Theodore Garland, University of Wisconsin; Michael Whiting, Brigham Young University; William Brown, SUNY Fredonia; Geoff Oxford, University of York; C.P. Kyriacou, Leicester University; Chris Austin, University of North Dakota; David King, University of Illinois; Paul Spruell, University of Montana; Daniel J. O’Connell, University of Texas, Arlington; Susan J. Mazer, University of California, Santa Barbara; Greg C. Nelson, University of Oregon a and to those students (now “Evil Syst” at Oxford rather than ANT 362 or BIO 462 at Emory) who, perhaps not on purpose, inspire much of the writing. Mark Ridley....  Part one Introduction W hen Darwin put forward his theory of evolution by natural selection, he lacked a satisfactory theory of inheritance, and the importance of natural selection was widely doubted until it was shown in the 1920s and 1930s how natural selection could operate with Mendelian inheritance. The two key events in the history of evolutionary thought are therefore Darwin’s discovery of evolution by natural selection and the synthesis of Darwin’s and Mendel’s theories a a synthesis variously called the modern synthesis, the synthetic theory of evolution, and neo-Darwinism. Chapter 1 discusses the rise of evolution- ary theory historically, and introduces some of its main figures. During the twentieth cen- tury, the sciences of evolutionary biology and genetics have developed together and some knowledge of genetics is essential for understanding the modern theory of evolution. Chapter 2 provides an elementary review of the main genetic mechanisms. In Chapter 3, we move on to consider the evidence for evolution a the evidence that species have evolved from other, ancestral species rather than having separate origins and remaining forever fixed in form. The classic case for evolution was made in Darwin’s On the Origin of Species and his general arguments still apply; but it is now possible to use more recent molecular and genetic evidence to illustrate them. Chapter 4 introduces the concept of natural selec- tion. It considers the conditions for natural selection to operate, and the main kinds of natural selection. One crucial condition is that the population should be variable, that is, individuals should differ from one another; the chapter shows that variation is common in nature. New variants originate in mutation. Chapter 2 reviews the main kinds of mutation, and how mutation rates are measured. Chapter 4 looks at how mutations contribute to vari- ation, and discusses why mutation can be expected to be adaptively undirected.....  1 The Rise of Evolutionary Biology he chapter first defines biological evolution, and T contrasts it with some related but different concepts. It then discusses, historically, the rise of modern evolutionary biology: we consider Darwin’s main precursors; Darwin’s own contribution; how Darwin’s ideas were received; and the development of the modern “synthetic theory” of evolution... 4 PART 1 / Introduction 1.1 Evolution means change in living things by descent with modification Evolutionary biology is a large science, and is growing larger. A list of its various subject areas could sound rather daunting. Evolutionary biologists now carry out research in some sciences, like molecular genetics, that are young and move rapidly, and in others like morphology and embryology, that have accumulated their discoveries at a more stately speed over a much longer period. Evolutionary biologists work with materials as diverse as naked chemicals in test tubes, animal behavior in the jungle, and fossils collected from barren and inhospitable rocks. Evolution is a big theory in biology However, a beautifully simple and easily understood idea a evolution by natural selection a can be scientifically tested in all these fields. It is one of the most powerful ideas in all areas of science, and is the only theory that can seriously claim to unify bio- logy. It can give meaning to facts from the invisible world in a drop of rain water, or from the many colored delights of a botanic garden, to thundering herds of big game. The theory is also used to understand such topics as the geochemistry of life’s origins and the gaseous proportions of the modern atmosphere. As Theodosius Dobzhansky, one of the twentieth century’s most eminent evolutionary biologists, remarked in an often quoted but scarcely exaggerated phrase, “nothing in biology makes sense except in the light of evolution” (Dobzhansky 1973). Evolution means change, change in the form and behavior of organisms between generations. The forms of organisms, at all levels from DNA sequences to macroscopic morphology and social behavior, can be modified from those of their ancestors during Evolution can be defined... evolution. However, not all kinds of biological change are included in the definition (Figure 1.1). Developmental change within the life of an organism is not evolution in the strict sense, and the definition referred to evolution as a “change between genera- tions” in order to exclude developmental change. A change in the composition of an ecosystem, which is made up of a number of species, would also not normally be counted as evolution. Imagine, for example, an ecosystem containing 10 species. At time 1, the individuals of all 10 species are, on average, small in body size; the average member of the ecosystem is therefore “small.” Several generations later, the ecosystem may still contain 10 species, but only five of the original small species remain; the other five have gone extinct and have been replaced by five species with large-sized indi- viduals, that have immigrated from elsewhere. The average size of an individual (or species) in the ecosystem has changed, even though there has been no evolutionary change within any one species. Most of the processes described in this book concern change between generations within a population of a species, and it is this kind of change we shall call evolution. When the members of a population breed and produce the next generation, we can imagine a lineage of populations, made up of a series of populations through time. Each population is ancestral to the descendant population in the next generation: a lineage is an “ancestor–descendant” series of populations. Evolution is then change between generations within a population lineage. Darwin defined evolution as “descent with modification,” and the word “descent” refers to the way evolutionary modification takes place in a series of populations that are descended from one..  CHAPTER 1 / The Rise of Evolutionary Biology 5 (a) Population (b) Individual development (c) Ecosystem a' a' a' a' a' a' Generation 3 a a' a' a a reproduction a a' a' a' a' a' Generation 2 a' a a reproduction a a a' a' adult a' a' a Generation 1 birth a a a a a' individual 1 2 3 4 individual 1 2 species 1 2 3 4 Figure 1.1 increased body size. (b) Individual developmental change is not Evolution refers to change within a lineage of populations evolution in the strict sense. The composition of the population between generations. (a) Evolution in the strict sense of the has not changed between generations and the developmental word. Each line represents one individual organism, and the changes (from a to a′) of each organism are not evolutionary. organisms in one generation are reproduced from the (c) Change in an ecosystem is not evolution in the strict sense. organisms in the previous generation. The composition of the Each line represents one species. The average composition population has changed, evolutionarily, through time. The of the ecosystem changes through time: from 2a : 1a′ at letter a′ represents a different form of the organism from a. generation 1 to 1a : 2a′ at generation 3. But within each species For instance, a organisms might be smaller in size than there is no evolution. a′ organisms. Evolution has then been in the direction of another. Recently, Harrison (2001) defined evolution as “change over time via descent with modification.”... and has distinct properties Evolutionary modification in living things has some further distinctive properties. Evolution does not proceed along some grand, predictable course. Instead, the details of evolution depend on the environment that a population happens to live in and the genetic variants that happen to arise (by almost random processes) in that population. Moreover, the evolution of life has proceeded in a branching, tree-like pattern. The modern variety of species has been generated by the repeated splitting of lineages since the single common ancestor of all life. Changes that take place in human politics, economics, history, technology, and even scientific theories, are sometimes loosely described as “evolutionary.” In this sense, evolutionary means mainly that there has been change through time, and perhaps not in a preordained direction. Human ideas and institutions can sometimes split during their history, but their history does not have such a clear-cut, branching, tree-like structure as does the history of life. Change, and splitting, provide two of the main themes of evolutionary theory. 1.2 Living things show adaptations Adaptation is another of evolutionary theory’s crucial concepts. Indeed, it is one of the main aims of modern evolutionary biology to explain the forms of adaptation that we.. 6 PART 1 / Introduction find in the living world. Adaptation refers to “design” in life a to those properties of living things that enable them to survive and reproduce in nature. The concept is easiest to understand by example. Many of the attributes of a living organism could be used to illustrate the concept of adaptation, because many details of the structure, metabolism, and behavior of an organism are well designed for life. Examples exist of adaptation The woodpecker provided Darwin’s favorite examples of adaptation. The wood- pecker’s most obvious adaptation is its powerful, characteristically shaped beak. It enables the woodpecker to excavate holes in trees. They can thus feed on the year- round food supply of insects that live under bark, insects that bore into the wood, and the sap of the tree itself. Tree holes also make safe sites to build a nest. Woodpeckers have many other design features as well as their beaks. Within the beak is a long, prob- ing tongue, which is well adapted to extract insects from inside a tree hole. They have a stiff tail that is used as a brace, short legs, and their feet have long curved toes for grip- ping on to the bark; they even have a special type of molting in which the strong central pair of feathers (that are crucial in bracing) are saved and molted last. The beak and body design of the woodpecker is adaptive. The woodpecker is more likely to survive, in its natural habitat, by possessing them. Camouflage is another, particularly clear, example of adaptation. Camouflaged spe- cies have color patterns and details of shape and behavior that make them less visible in their natural environment. Camouflage assists the organism to survive by making it less visible to its natural enemies. Camouflage is adaptive. Adaptation, however, is not an isolated concept referring to only a few special properties of living things a it applies to almost any part of the body. In humans, hands are adapted for grasping, eyes for seeing, the alimentary canal for digesting food, legs for movement: all these functions assist us to survive. Although most of the obvious things we notice are adaptive, not every detail of an organism’s form and behavior is necessarily adaptive (Chapter 10). Adaptation has to be explained,... Adaptations are, however, so common that they have to be explained. Darwin regarded adaptation as the key problem that any theory of evolution had to solve. In Darwin’s theory a as in modern evolutionary biology a the problem is solved by natural selection.... and is, by natural selection Natural selection means that some kinds of individual in a population tend to contrib- ute more offspring to the next generation than do others. Provided that the offspring resemble their parents, any attribute of an organism causing it to leave more offspring than average will increase in frequency in the population over time. The composition of the population will then change automatically. Such is the simple, but immensely powerful, idea whose ramifying consequences we shall be exploring in this book. 1.3 A short history of evolutionary biology We shall begin with a brief sketch of the historic rise of evolutionary biology, in four main stages: 1. Evolutionary and non-evolutionary ideas before Darwin. 2. Darwin’s theory (1859). 3. The eclipse of Darwin (c. 1880–1920). 4. The modern synthesis (1920s to 1950s)...  CHAPTER 1 / The Rise of Evolutionary Biology 7 1.3.1 Evolution before Darwin The history of evolutionary biology really begins in 1859, with the publication of Charles Darwin’s On the Origin of Species. However, many of Darwin’s ideas have an older pedigree. The most immediately controversial claim in Darwin’s theory is that species are not permanently fixed in form, but that one species evolves into another. (“Fixed” here means unchanging.) Human ancestry, for instance, passes through a continuous series of forms leading back to a unicellular stage. Species fixity was the Evolutionary thinkers existed before orthodox belief in Darwin’s time, though that does not mean that no one then or before Darwin, but either lacked,... had questioned it. Naturalists and philosophers a century or two before Darwin had often speculated about the transformation of species. The French scientist Maupertuis discussed evolution, as did encyclopédistes such as Diderot. Charles Darwin’s grand- father, Erasmus Darwin, is another example. However, none of these thinkers put for- ward anything we would now recognize as a satisfactory theory to explain why species change. They were mainly interested in the factual possibility that one species might change into another. The question was brought to an issue by the French naturalist Jean-Baptiste Lamarck (1744–1829). The crucial work was his Philosophie Zoologique (1809), in which he argued that species change over time into new species. The way in which he thought species changed was importantly different from Darwin’s and our modern idea of evolution. Historians prefer the contemporary word “transformism” to describe Lamarck’s idea.1 Figure 1.2 illustrates Lamarck’s conception of evolution, and how it differs from Darwin’s and our modern concept. Lamarck supposed that lineages of species persisted indefinitely, changing from one form into another; lineages in his system did not branch and did not go extinct. Lamarck had a two-part explanation of why species... or proposed, unsatisfactory change. The principal mechanism was an “internal force” a some sort of unknown mechanisms to drive evolution mechanism within an organism causing it to produce offspring slightly different from itself, such that when the changes had accumulated over many generations the lineage would be visibly transformed, perhaps enough to be a new species. Lamarck’s second (and possibly to him less important) mechanism is the one he is now remembered for: the inheritance of acquired characters. Biologists use the word “character” as a short-hand for “characteristic.” A character is any distinguishable property of an organism; it does not here refer to character in the sense of personality. As an organism develops, it acquires many individual characters, in this biological sense, due to its particular history of accidents, diseases, and muscular exercises. Lamarck suggested that a species could be transformed if these individually acquired modifications were inherited by the individual’s offspring. In his famous discussion of the giraffe’s neck, he argued that ancestral giraffes had stretched to reach leaves higher 1 The historic change in the meaning of the term “evolution” is a fascinating story in itself. Initially, it meant something more like what we mean by development (as in growing up from an egg to an adult) than by evolu- tion: an unfolding of predictable forms in a preprogramed order. The course of evolution, in the modern sense, is not preprogramed; it is unpredictable in much the same way that human history is unpredictable. The change of meaning occurred around the time of Darwin; he did not use the word in The Origin of Species (1859), exce