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

Abstract

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...

Intralocus Sexual Conflict and the Tragedy of the Commons in Seed Beetles

“…Recent studies have pointed to the importance of ecology and genetic architecture in determining the efficacy of the second mechanism and, therefore, the overall effect of sexual selection (e.g., Long et al 2012;Arbuthnott et al 2014;Berger et al 2014a;Bonduriansky 2014;Connallon and Clark 2014;Connallon 2015). Our study provides a novel type of experimental evidence for the hypothesis that sexual selection can maintain male-beneficial SA genetic variation that, in concert with IeSC, reduces the overall viability of natural populations.…”

“…First, idiosyncrasies of the mating system, leading to differences in the extent of IeSC and associated female harm, are likely to play a decisive role in settling the outcome of sexual selection (e.g., Holland and Rice 1999;Hollis and Houle 2011;PlesnarBielak et al 2012;Chenoweth et al 2015). Second, much of the discrepancy between experiments may be rooted in differences in the genetic architecture of the studied populations and/ or the environmental conditions used in the experiments, which can affect the relative expression of, and selection on, allelic variation (Long et al 2012;Berger et al 2014a;Connallon and Clark 2014;Duffy et al 2014;Punzalan et al 2014).…”

“…IaSC occurs when selection favors alternative alleles in males and females at a given locus (Rice 1992;Chippindale et al 2001) and can act to maintain standing genetic variation with sexually antagonistic (SA) effects on fitness (Kidwell 1977;Connallon and Clark 2012;Arnqvist et al 2014). As a consequence, the degree of SA genetic variation in well-adapted populations may be large relative to genetic variation for overall viability.…”

“…1). Further, IaSC should generate strong selection for the evolution of sex-specific gene expression, ultimately resulting in the evolution of pronounced sexual dimorphism and a resolution of genetic conflict (Lande 1980;Rice 1984Rice , 1992Bonduriansky and Rowe 2005;Cox and Calsbeek 2009;Poissant et al 2010;Connallon and Clark 2011). However, a resolution to IaSC would allow both sexes to reach their independent phenotypic optima (e.g., increased courtship intensity and high mating rates in males versus increased mating resistance and low remating rates in females).…”

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

“…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...…”