Fitness Variation Due to Sexual Antagonism and Linkage Disequilibrium

Patten, Manus M.; Haig, David; Úbeda, Francisco

doi:10.1111/j.1558-5646.2010.01100.x

Cited by 42 publications

(89 citation statements)

References 25 publications

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“…However, two genes, E592 and E219, are at least 8 cM from the MSY (see table 3 of Bergero et al 2013) and have high diversity (Table 1), and our tests gave no evidence of paralogues in the species' genome that could create a false appearance of high diversity. At such loose linkage, SA polymorphisms may appear no more plausible than in autosomal regions, where such polymorphisms are unlikely to be maintained (Patten et al 2010;Jordan and Charlesworth 2012). A possibility that is consistent with high diversity at such distal locations is that linked SA polymorphisms are expected to develop LD with one another (Patten et al 2010;Jordan and Charlesworth 2012).…”

Section: Discussionmentioning

confidence: 99%

“…The first is to further test for partial sex linkage, using population genetic data. The data were primarily collected for our second goal, which was to perform analyses to ask whether PAR genes show the expected footprints of polymorphism due to sexually antagonistic selection: high diversity, other evidence of balancing selection maintaining alleles polymorphic for a long evolutionary time, and evidence of LD between the PAR and the fully Y-linked, or male-specific, region (Patten et al 2010;Úbeda et al 2011).…”

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Testing for the Footprint of Sexually Antagonistic Polymorphisms in the Pseudoautosomal Region of a Plant Sex Chromosome Pair

Qiu¹,

Bergero²,

Charlesworth

2013

Genetics

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The existence of sexually antagonistic (SA) polymorphism is widely considered the most likely explanation for the evolution of suppressed recombination of sex chromosome pairs. This explanation is largely untested empirically, and no such polymorphisms have been identified, other than in fish, where no evidence directly implicates these genes in events causing loss of recombination. We tested for the presence of loci with SA polymorphism in the plant Silene latifolia, which is dioecious (with separate male and female individuals) and has a pair of highly heteromorphic sex chromosomes, with XY males. Suppressed recombination between much of the Y and X sex chromosomes evolved in several steps, and the results in Bergero et al. (2013) show that it is still ongoing in the recombining or pseudoautosomal, regions (PARs) of these chromosomes. We used molecular evolutionary approaches to test for the footprints of SA polymorphisms, based on sequence diversity levels in S. latifolia PAR genes identified by genetic mapping. Nucleotide diversity is high for at least four of six PAR genes identified, and our data suggest the existence of polymorphisms maintained by balancing selection in this genome region, since molecular evolutionary (HKA) tests exclude an elevated mutation rate, and other tests also suggest balancing selection. The presence of sexually antagonistic alleles at a locus or loci in the PAR is suggested by the very different X and Y chromosome allele frequencies for at least one PAR gene.

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Section: Discussionmentioning

confidence: 99%

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confidence: 99%

Testing for the Footprint of Sexually Antagonistic Polymorphisms in the Pseudoautosomal Region of a Plant Sex Chromosome Pair

Qiu¹,

Bergero²,

Charlesworth

2013

Genetics

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“…This may seem surprising given the intensity of interest (e.g., Bonduriansky and Chenoweth 2009;van Doorn 2009;Stewart et al 2010) and the considerable theoretical tradition regarding antagonistic selection and variation (e.g., Owen 1953;Bennett 1957;Parsons 1961;Haldane 1962;Haldane and Jayakar 1964;Li 1967;Mérat 1969;Mandel 1971;Kidwell et al 1977;Pamilo 1979;Curtsinger 1980;Rose 1982Rose , 1985Rice 1984;Curtsinger et al 1994;Babcock and Asmussen 1996;Hedrick 1999Hedrick , 2007Prout 2000;Gavrilets and Rice 2006;Unckless and Herren 2009;Patten and Haig 2009a,b;Fry 2010;Patten et al 2010;Úbeda et al 2011;Arnqvist 2011;Jordan and Charlesworth 2011). Prior theory has thoroughly described the requisite parameter criteria for balancing selection, yet it has neglected the impact of recurrent mutation and finite population size on genetic variability.…”

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A General Population Genetic Framework for Antagonistic Selection That Accounts for Demography and Recurrent Mutation

2012

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Antagonistic selection-where alleles at a locus have opposing effects on male and female fitness ("sexual antagonism") or between components of fitness ("antagonistic pleiotropy")-might play an important role in maintaining population genetic variation and in driving phylogenetic and genomic patterns of sexual dimorphism and life-history evolution. While prior theory has thoroughly characterized the conditions necessary for antagonistic balancing selection to operate, we currently know little about the evolutionary interactions between antagonistic selection, recurrent mutation, and genetic drift, which should collectively shape empirical patterns of genetic variation. To fill this void, we developed and analyzed a series of population genetic models that simultaneously incorporate these processes. Our models identify two general properties of antagonistically selected loci. First, antagonistic selection inflates heterozygosity and fitness variance across a broad parameter range-a result that applies to alleles maintained by balancing selection and by recurrent mutation. Second, effective population size and genetic drift profoundly affect the statistical frequency distributions of antagonistically selected alleles. The "efficacy" of antagonistic selection (i.e., its tendency to dominate over genetic drift) is extremely weak relative to classical models, such as directional selection and overdominance. Alleles meeting traditional criteria for strong selection (N e s .. 1, where N e is the effective population size, and s is a selection coefficient for a given sex or fitness component) may nevertheless evolve as if neutral. The effects of mutation and demography may generate population differences in overall levels of antagonistic fitness variation, as well as molecular population genetic signatures of balancing selection. P LEIOTROPY may impose widespread evolutionary genetic constraints against adaptation (Fisher 1958, Orr 1998, Otto 2004. Allocation tradeoffs between fitness components, coupled with a shared genetic basis between them, may limit evolutionary opportunities to simultaneously maximize individual components of fitness (Houle 1991). Conflicting selection may emerge at underlying loci, so that alleles improving one fitness component reduce othersa scenario referred to as "antagonistic pleiotropy" (Rose 1982;Curtsinger et al. 1994). A similar scenario arises when patterns of selection differ between males and females. Opposing, sex-specific selection, or "sexual antagonism," arises when mutations favorable within one sex are costly when expressed in the other Bonduriansky and Chenoweth 2009;van Doorn 2009).Antagonistic selection may play an important role in maintaining genetic variation related to fitness and driving patterns of genome evolution. Direct estimates of sex-and context-specific selection on quantitative traits confirm that pleiotropic and sexually antagonistic fitness tradeoffs are ubiquitous (Curtsinger et al. 1994;Roff 1996;Delph 2007;Cox and Calsbeek 2009;Poissant and Coltma...

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“…Whether balanced, sexual antagonistic alleles are common within populations has important and wide-ranging biological implications for the genetic basis of quantitative traits (Rice 1984;Turelli and Barton 2004;Bonduriansky and Chenoweth 2009), genetic loads and extinction risk (Kokko and Brooks 2003;Whitlock and Agrawal 2009;Holman and Kokko 2013), mating system evolution (Seger and Trivers 1986;Albert and Otto 2005;Blackburn et al 2010;Roze and Otto 2012), and the evolution of genomes and genetic systems (Charlesworth and Charlesworth 1980;Day and Bonduriansky 2004;Ellegren and Parsch 2007;van Doorn and Kirkpatrick 2007, 2010;Mank 2009;Connallon and Clark 2010, 2011, 2013aParsch and Ellegren 2013;Wright and Mank 2013;Charlesworth et al 2014;Kirkpatrick and Guerrero 2014). Although prior theory clearly defines the parameter criteria for balancing selection by sexual antagonism (e.g., Kidwell et al 1977;Pamilo 1979;Patten and Haig 2009;Unckless and Herren 2009;Fry 2010;Patten et al 2010Patten et al , 2013Arnqvist 2011;Connallon and Clark 2012;Mullon et al 2012;Jordan and Charlesworth 2012), it remains unclear how often such conditions might be expected to arise in dioecious populations. A recent extension of Fisher's geometric model provides a theoretical framework for predicting the sex-specific distribution of mutant fitness effects (Connallon and Clark 2014), yet this the...…”

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confidence: 99%

Balancing Selection in Species with Separate Sexes: Insights from Fisher’s Geometric Model

2014

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How common is balancing selection, and what fraction of phenotypic variance is attributable to balanced polymorphisms? Despite decades of research, answers to these questions remain elusive. Moreover, there is no clear theoretical prediction about the frequency with which balancing selection is expected to arise within a population. Here, we use an extension of Fisher's geometric model of adaptation to predict the probability of balancing selection in a population with separate sexes, wherein polymorphism is potentially maintained by two forms of balancing selection: (1) heterozygote advantage, where heterozygous individuals at a locus have higher fitness than homozygous individuals, and (2) sexually antagonistic selection (a.k.a. intralocus sexual conflict), where the fitness of each sex is maximized by different genotypes at a locus. We show that balancing selection is common under biologically plausible conditions and that sex differences in selection or sex-by-genotype effects of mutations can each increase opportunities for balancing selection. Although heterozygote advantage and sexual antagonism represent alternative mechanisms for maintaining polymorphism, they mutually exist along a balancing selection continuum that depends on population and sex-specific parameters of selection and mutation. Sexual antagonism is the dominant mode of balancing selection across most of this continuum.O NE of the primary goals of population genetics is to evaluate how processes of mutation, selection, migration, recombination, and genetic drift account for the maintenance of genetic variation in natural populations. This "great obsession" with genetic variation (Gillespie 2004, p. 154) is reflected by a massive body of theoretical and empirical research that seeks to connect empirical patterns of population and quantitative genetic variability with the specific evolutionary processes that might account for them.Balancing selection-selection that maintains genetic variation at a locus-could potentially account for an important fraction of observed quantitative genetic variability (Dobzhansky 1955;Lewontin 1974;Charlesworth and Hughes 1999). Although relatively few unambiguous cases of balancing selection have been documented to date (see Charlesworth 2006;Hedrick 2012;Johnston et al. 2013;Leffler et al. 2013), empirical methods for detecting their population genetic signatures are highly conservative and may fail to identify many (or most) instances of balancing selection within a genome (Charlesworth 2006;Charlesworth and Charlesworth 2010). Furthermore, balanced polymorphisms may plausibly account for several empirical observations that are not easily explained by alternative models of variation maintained by recurrent mutation. For example, the high genetic variance in life history and reproductive traits (Houle 1992;Pomiankowski and Moller 1995) and the presence of intermediate-frequency alleles with large phenotypic effects (Long et al. 2000) are each potentially attributable to a subset of loci that segrega...

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Fitness Variation Due to Sexual Antagonism and Linkage Disequilibrium

Cited by 42 publications

References 25 publications

Testing for the Footprint of Sexually Antagonistic Polymorphisms in the Pseudoautosomal Region of a Plant Sex Chromosome Pair

Testing for the Footprint of Sexually Antagonistic Polymorphisms in the Pseudoautosomal Region of a Plant Sex Chromosome Pair

A General Population Genetic Framework for Antagonistic Selection That Accounts for Demography and Recurrent Mutation

Balancing Selection in Species with Separate Sexes: Insights from Fisher’s Geometric Model

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