ANTAGONISTIC VERSUS NONANTAGONISTIC MODELS OF BALANCING SELECTION: CHARACTERIZING THE RELATIVE TIMESCALES AND HITCHHIKING EFFECTS OF PARTIAL SELECTIVE SWEEPS

Antagonistically selected alleles‐–those with opposing fitness effects between sexes, environments, or fitness components‐–represent an important component of additive genetic variance in fitness‐related traits, with stably balanced polymorphisms often hypothesized to contribute to observed quantitative genetic variation. Balancing selection hypotheses imply that intermediate‐frequency alleles disproportionately contribute to genetic variance of life‐history traits and fitness. Such alleles may also associate with population genetic footprints of recent selection, including reduced genetic diversity and inflated linkage disequilibrium at linked, neutral sites. Here, we compare the evolutionary dynamics of different balancing selection models, and characterize the evolutionary timescale and hitchhiking effects of partial selective sweeps generated under antagonistic versus nonantagonistic (e.g., overdominant and frequency‐dependent selection) processes. We show that the evolutionary timescales of partial sweeps tend to be much longer, and hitchhiking effects are drastically weaker, under scenarios of antagonistic selection. These results predict an interesting mismatch between molecular population genetic and quantitative genetic patterns of variation. Balanced, antagonistically selected alleles are expected to contribute more to additive genetic variance for fitness than alleles maintained by classic, nonantagonistic mechanisms. Nevertheless, classical mechanisms of balancing selection are much more likely to generate strong population genetic signatures of recent balancing selection.

[1]  A. Pomiankowski,et al.  THE EFFECTS OF SELECTION AND GENETIC DRIFT ON THE GENOMIC DISTRIBUTION OF SEXUALLY ANTAGONISTIC ALLELES , 2012, Evolution; international journal of organic evolution.

[2]  A. Clark,et al.  A General Population Genetic Framework for Antagonistic Selection That Accounts for Demography and Recurrent Mutation , 2012, Genetics.

[3]  Peter L. Ralph,et al.  Patterns of Neutral Diversity Under General Models of Selective Sweeps , 2011, Genetics.

[4]  T. Mappes,et al.  Negative Frequency-Dependent Selection of Sexually Antagonistic Alleles in Myodes glareolus , 2011, Science.

[5]  D. L. Bell,et al.  Environment-dependent intralocus sexual conflict in a dioecious plant. , 2011, The New phytologist.

[6]  Z. Lewis,et al.  EVIDENCE FOR STRONG INTRALOCUS SEXUAL CONFLICT IN THE INDIAN MEAL MOTH, PLODIA INTERPUNCTELLA , 2011, Evolution; international journal of organic evolution.

[7]  A. Clark,et al.  SEX LINKAGE, SEX‐SPECIFIC SELECTION, AND THE ROLE OF RECOMBINATION IN THE EVOLUTION OF SEXUALLY DIMORPHIC GENE EXPRESSION , 2010, Evolution; international journal of organic evolution.

[8]  R. Calsbeek,et al.  FITNESS CONSEQUENCES OF SEX‐SPECIFIC SELECTION , 2010, Evolution; international journal of organic evolution.

[9]  R. Calsbeek,et al.  Cryptic Sex-Ratio Bias Provides Indirect Genetic Benefits Despite Sexual Conflict , 2010, Science.

[10]  P. Innocenti,et al.  The Sexually Antagonistic Genes of Drosophila melanogaster , 2010, PLoS biology.

[11]  B. Charlesworth,et al.  Elements of Evolutionary Genetics , 2010 .

[12]  Jeremiah D. Degenhardt,et al.  Targets of balancing selection in the human genome. , 2009, Molecular biology and evolution.

[13]  J. D. Fry THE GENOMIC LOCATION OF SEXUALLY ANTAGONISTIC VARIATION: SOME CAUTIONARY COMMENTS , 2009, Evolution; international journal of organic evolution.

[14]  D. Haig,et al.  Maintenance or Loss of Genetic Variation Under Sexual and Parental Antagonism at a Sex-Linked Locus , 2009, Evolution; international journal of organic evolution.

[15]  S. Chenoweth,et al.  Intralocus sexual conflict. , 2009, Trends in ecology & evolution.

[16]  P. Hedrick SEX: DIFFERENCES IN MUTATION, RECOMBINATION, SELECTION, GENE FLOW, AND GENETIC DRIFT , 2007, Evolution; international journal of organic evolution.

[17]  M. Kirkpatrick,et al.  The Intersexual Genetic Correlation for Lifetime Fitness in the Wild and Its Implications for Sexual Selection , 2007, PloS one.

[18]  P. Keightley,et al.  A Comparison of Models to Infer the Distribution of Fitness Effects of New Mutations , 2013, Genetics.

[19]  L. Kruuk,et al.  Sexually antagonistic genetic variation for fitness in red deer , 2007, Nature.

[20]  Mark J. Fitzpatrick,et al.  Maintaining a behaviour polymorphism by frequency-dependent selection on a single gene , 2007, Nature.

[21]  W. Rice,et al.  Genetic models of homosexuality: generating testable predictions , 2006, Proceedings of the Royal Society B: Biological Sciences.

[22]  Pardis C Sabeti,et al.  Positive Natural Selection in the Human Lineage , 2006, Science.

[23]  D. Charlesworth Balancing Selection and Its Effects on Sequences in Nearby Genome Regions , 2006, PLoS genetics.

[24]  J. Pritchard,et al.  A Map of Recent Positive Selection in the Human Genome , 2006, PLoS biology.

[25]  R. Nielsen Molecular signatures of natural selection. , 2005, Annual review of genetics.

[26]  H. A. Orr,et al.  A Pseudohitchhiking Model of X vs. Autosomal Diversity , 2004, Genetics.

[27]  Sean H. Rice,et al.  Evolutionary Theory: Mathematical and Conceptual Foundations , 2004 .

[28]  Timothy A Mousseau,et al.  Female mating bias results in conflicting sex-specific offspring fitness , 2004, Nature.

[29]  Pardis C Sabeti,et al.  Detecting recent positive selection in the human genome from haplotype structure , 2002, Nature.

[30]  W. Rice,et al.  Intersexual ontogenetic conflict , 2001 .

[31]  W. Rice,et al.  Negative genetic correlation for adult fitness between sexes reveals ontogenetic conflict in Drosophila. , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[32]  J. Gillespie Genetic drift in an infinite population. The pseudohitchhiking model. , 2000, Genetics.

[33]  L. Kruuk,et al.  A comparison of multilocus clines maintained by environmental adaptation or by selection against hybrids. , 1999, Genetics.

[34]  P. Hedrick Antagonistic pleiotropy and genetic polymorphism: a perspective , 1999, Heredity.

[35]  Nicholas H. Barton,et al.  The effect of hitch-hiking on neutral genealogies , 1998 .

[36]  A. Møller,et al.  A resolution of the lek paradox , 1995, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[37]  T. Prout,et al.  Antagonistic Pleiotropy, Reversal of Dominance, and Genetic Polymorphism , 1994, The American Naturalist.

[38]  F. B. Livingstone Polymorphism and differential selection for the sexes. , 1992, Human biology.

[39]  B. Golding The prospects for polymorphisms shared between species , 1992, Heredity.

[40]  W. Rice SEX CHROMOSOMES AND THE EVOLUTION OF SEXUAL DIMORPHISM , 1984, Evolution; international journal of organic evolution.

[41]  T. Nagylaki Selection in dioecious populations , 1979, Annals of Human Genetics.

[42]  J H Gillespie,et al.  A general model to account for enzyme variation in natural populations. V. The SAS--CFF model. , 1978, Theoretical population biology.

[43]  S. Wright Evolution and the Genetics of Populations, Volume 3: Experimental Results and Evolutionary Deductions , 1977 .

[44]  P. Hedrick,et al.  Genetic Polymorphism in Heterogeneous Environments , 1976 .

[45]  M. Kimura,et al.  An introduction to population genetics theory , 1971 .

[46]  J. M. Smith What use is sex? , 1971, Journal of theoretical biology.

[47]  W. Ewens,et al.  Heterozygote selective advantage , 1970 .

[48]  A. Robertson Selection for heterozygotes in small populations. , 1962, Genetics.

[49]  H. Levene,et al.  Genetic Equilibrium When More Than One Ecological Niche is Available , 1953, The American Naturalist.

[50]  S. Wright,et al.  Genetics of Natural Populations. Xii. Experimental Reproduction of Some of the Changes Caused by Natural Selection in Certain Populations of Drosophila Pseudoobscura. , 1946, Genetics.

[51]  Mandy J. Haldane,et al.  A Mathematical Theory of Natural and Artificial Selection, Part V: Selection and Mutation , 1927, Mathematical Proceedings of the Cambridge Philosophical Society.

[52]  J. B. S. Haldane,et al.  A mathematical theory of natural and artificial selection—I , 1927, Mathematical Proceedings of the Cambridge Philosophical Society.

[53]  R Core Team,et al.  R: A language and environment for statistical computing. , 2014 .

[54]  J. L. Tomkins,et al.  On the resolution of the lek paradox. , 2008, Trends in ecology & evolution.

[55]  W. Ewens Mathematical Population Genetics : I. Theoretical Introduction , 2004 .

[56]  D. Houle Comparing evolvability and variability of quantitative traits. , 1992, Genetics.

[57]  P. Hedrick GENETIC POLYMORPHISM IN HETEROGENEOUS ENVIRONMENTS: A DECADE LATER , 1986 .

[58]  J. Felsenstein The theoretical population genetics of variable selection and migration. , 1976, Annual review of genetics.

[59]  J. M. Smith,et al.  The hitch-hiking effect of a favourable gene. , 1974, Genetical research.