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Evolutionary Genetics from Molecules to Morphology P1: AKA/FKA P2: SDL CB208-FM April 27, 2000 Evolutionary Genetics From Molecules to Morphology Edited by R. S. SINGH McMaster University C. B. KRIMBAS University of Athens v P1: AKA/FKA P2: SDL CB208-FM April 27, 2000 PUBLISHED BY THE PRESS SYNDICATE OF THE UNIVERSITY OF CAMBRIDGE The Pitt Building, Trumpington Street, Cambridge, United Kingdom CAMBRIDGE UNIVERSITY PRESS The Edinburgh Building, Cambridge CB2 2RU, UK www.cup.cam.ac.uk 40 West 20th Street, New York, NY 10011-4211, USA www.cup.org 10 Stamford Road, Oakleigh, Melbourne 3166, Australia Ruiz de Alarc´on 13, 28014 Madrid, Spain C Cambridge University Press 1999 This book is in copyright. Subject to statutory exception and to the provisions of relevant collective licensing agreements, no reproduction of any part may take place without the written permission of Cambridge University Press. First published 1999 Printed in the United States of America Typeface New Baskerville 9.75/12 pt. System LATEX2ε [tb] A catalog record for this book is available from the British Library. Library of Congress Cataloging-in-Publication Data Evolutionary genetics : from molecules to morphology / edited by R. S. Singh and C. Krimbas. p. cm. Includes bibliographical references and index. ISBN 0-521-57123-5 1. Evolutionary genetics. 2. Lewontin, Richard C., 1929– . I. Singh, R. S. II. Krimbas, Costas B. QH390.E96 1999 576.8–dc21 99-14415 CIP ISBN 0 521 57123 5 hardback vi P1: AKA/FKA P2: SDL CB208-FM April 27, 2000 Contents List of Contributors page xi Preface xv Section A. Population Genetics: Problems, Foundations, and Historical Perspectives Introductory Remarks – Costas Krimbas 1 The Problems of Population Genetics 5 richard lewontin 2 The Mathematical Foundations of Population Genetics 24 warren ewens 3 A Natural Historian’s View of Heterosis and Related Topics 41 bruce wallace 4 The Molecular Foundation of Population Genetics 52 rama s. singh, walter f. eanes, donal a. hickey, lynn m. king, and margaret a. riley Section B. Molecular Variation and Evolution Introductory Remarks – Martin Kreitman 5 The Population and Evolutionary Genetics of Codon Bias 82 martin kreitman and marcos antezana 6 Gene Conversion Is a Major Determinant of Genetic Diversity at the DNA Level 102 andrew berry and antonio barbadilla 7 Evidence for Balancing, Directional, and Background Selection in Molecular Evolution 124 stephen w. schaeffer and montserrat aguad´e vii P1: AKA/FKA P2: SDL CB208-FM April 27, 2000 viii CONTENTS Section C. Selection and Genetic Polymorphism Introductory Remarks – Philip Hedrick and Timothy Prout 8 Aspects of Fitness 146 freddy bugge christiansen and timothy prout 9 How Well Does Opposing Selection Maintain Variation? 157 timothy prout 10 Analysis of Selection in Laboratory and Field Populations 182 einararnason ´ and j. s. f. barker 11 Genetics of Complex Polymorphisms: Parasites and Maintenance of the Major Histocompatibility Complex Variation 204 philip w. hedrick and timothy j. kim 12 The Population Biology of Antibiotic Resistance 235 bruce r. levin Section D. Linkage, Breeding Systems, and Evolution Introductory Remarks – Ian R. Franklin 13 The Equilibrium Theory of One- and Two-Locus Systems 258 ian r. franklin and marcus w. feldman 14 Inversion Polymorphisms in Drosophila 284 costar krimbas and jeffrey powell 15 The Evolution of Breeding Systems 300 marcy k. uyenoyama 16 The Evolution of Sex and Recombination 317 donal a. hickey Section E. Quantitative Genetics and Phenotypic Evolution Introductory Remarks – Richard Frankham 17 Quantitative Genetics and Phenotypic Evolution 335 russell lande 18 Nature of Quantitative Genetic Variation 351 richard frankham and kenneth weber 19 The Maintenance of Genetic Variation in Life-History Traits 369 brian charlesworth and kimberly a. hughes 20 Population Genetics and Life-History Evolution 393 lloyd demetrius P1: AKA/FKA P2: SDL CB208-FM April 27, 2000 CONTENTS ix Section F. Gene Flow, Population Structure, and Evolution Introductory Remarks – Montgomery Slatkin 21 A Coalescent View of Population Structure 418 montgomery slatkin 22 Population Genetics and Evolution of Animal Mitochondrial DNA 430 eleftherios zouros and david m. rand 23 Genetic Structure and Evolution in Parthenogenetic Animals 456 e. davis parker jr. and monica niklasson 24 Genetic Structure of Prokaryotic Populations 475 frederick m. cohan Section G. Population Genetics and Speciation Introductory Remarks – Rama S. Singh 25 Sexual Selection in Populations: The Facts Require a Change in the Genetic Definition of the Species 495 hampton l. carson 26 The Role of Selection in Speciation 513 judith masters 27 The Evolutionary Genetics of Speciation 532 jerry a. coyne and h. allen orr 28 Toward a Unified Theory of Speciation 570 rama s. singh Section H. Behavior, Ecology, and Evolution Introductory Remarks – Subodh Jain 29 From Population Genetics to Evolutionary Genetics: A View through the Trees 609 joseph felsenstein 30 Attitudes to Animal Behavior 628 john maynard smith 31 The Evolution of Social Behavior 641 deborah m. gordon 32 Population Genetics and Evolutionary Ecology: A Progress Re- port 653 subodh jain Publications of R. C. Lewontin 679 Index 691 P1: DBJ CB208-01 June 22, 1999 CHAPTER ONE The Problems of Population Genetics richard lewontin The science of population genetics is the auto mechanics of evolutionary bio- logy. Organic evolution, in the Darwinian scheme, is a consequence of the con- version of variation among members of an ensemble into differences between ensembles in time and space. Classically those ensembles are collections of in- dividual organisms, populations in the usual sense, but the Darwinian scheme can be applied as well to ensembles of organelles within cells or to collections of populations that make up a species. The essential features of the Darwinian scheme that determine both the subject and form of population genetics are that 1. there are processes that produce variation among individuals within a population, 2. there are processes that result in changes in the relative frequencies of the variants within a generation, 3. there is a hereditary process across generations that may result in further change in the relative frequencies of the different variants, but population frequencies are correlated across generational lines so that the frequency distribution of variants in any time interval is some nontrivial function of their distribution in the previous interval of time. It is the relation between the processes of the generation and the modulation of variation within generations in features 1 and 2 and the processes occur- ring between generations in feature 3 that both create the science of pop- ulation genetics and pose its methodological dilemmas and its shape as an inquiry. These relations are most easily understood as the transformations in the state of the population, shown in Fig. 1.1 (from Lewontin, 1974). The population change can be represented both in a genotypic and a phenotypic space, and the complete laws of transformation make use of both these spaces. R. S. Singh and C. B. Krimbas, eds., Evolutionary Genetics: From Molecules to Morphology, vol. 1. c Cambridge University Press 1999. Printed in the United States of America. ISBN 0-521- 57123-5. All rights reserved. 5 P1: DBJ CB208-01 June 22, 1999 6 Richard Lewontin Figure 1.1. Schematic representation of the paths of transformation of population genotype from one generation to the next. G and P are the spaces of genotypic and phenotypic 0 0 description. G1, G , G2, and G are genotypic descriptions at various points in time within 1 0 2 0 successive generations. P1, P1, P2, and P2 are phenotypic descriptions. T1, T2, T3, and T4 are laws of transformation. Details are given in the text. (From Evolutionary Genetics by R. C. Lewontin. Copyright c 1974 by Columbia University Press. Reprinted with permission of the publisher.) G1, G2, P1, and P2 are genotypic and phenotypic descriptions at different points within a generation, while the same quantities with primes are the descriptions of the equivalent states in the next generation. The laws of transformation are T1: a set of epigenetic laws that gives the distribution of phenotypes, including fitness, that results from the development of various genotypes in various environments. T2: the laws of mating, migration, and natural selection including stochastic elements that transform the phenotypic array of potential reproducing units in a population within a generation. T3: the set of reverse epigenetic transformations that allows inferences about the distribution of genotypes G2 corresponding to the distribution of phenotypes P2. P1: DBJ CB208-01 June 22, 1999 THE PROBLEMS OF POPULATION GENETICS 7 T4: the phenomenology of genetics such as segregation, recombination, mu- tation, horizontal transfer, etc., including stochastic elements, that allows us to predict the probability distribution of genotypes in the next generation produced from gametogenesis and fertilization, given an array of parental genotypes. This representation of the structure of population genetic inference points immediately to two major sources of difficulty that have shaped the problems of population from its beginnings and still do so. First there is the problem of development. T4, the complete apparatus of genetics that carries the popula- tion transformation across generations, is operating in the genotypic space to transform genotypic frequencies and cannot be framed in phenotypic terms. But T2 that specifies the transformation of frequencies within generations is a set of physiological, ecological, and behavioral relations that operates in the phenotypic space. In the absence of a knowledge of the epigenetic transfor- mations, the circuit is cut and nothing can be done. Nor can one depend on developmental genetics to provide the missing laws, because the main direction of developmental biology has never been, and shows no promise of ever being, to understand the environmental contingency of variations in development. Much of the past and the present problems of population genetics can be un- derstood only as an attempt to finesse the unsolved problem of an adequate description of development.
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