The maintenance of genetic polymorphism underlying sexually antagonistic traits

Abstract

Selection often favours different trait values in males and females, leading to genetic conflicts between the sexes, or sexual antagonism. Theory suggests that such conflict can maintain genetic variation by generating balancing selection. However, most of this theory is based on insights from models of single loci with fixed fitness effects. It is thus unclear how readily sexual antagonism drives balancing selection at loci where the fitness effects are not arbitrarily set but emerge from the genotype-phenotype map and the fitness landscape. Here we use mathematical models and computer simulations to investigate the evolution of traits that have different optima in males and females and so experience sexually antagonistic selection. We examine the consequences of such selection for the maintenance and nature of genetic variation under different assumptions of genetic architecture and for different fitness landscapes. We show that the conditions necessary to maintain variation are significantly more restrictive than previously appreciated. This is because the majority of typical sex-specific fitness landscapes generate stabilising selection on traits, and so favour the fixation of a single homozygote genotype that encodes the phenotype with the highest sex-averaged fitness. Instead, the maintenance of genetic polymorphism requires extremely, if not implausibly, strong conflict between males and females in order to disfavour extreme and intermediate phenotypes by generating diversifying selection. Furthermore, in all cases, we find that distinctive patterns of genetic variation produced by sexual antagonism arise rarely and are often transient, and so are difficult to observe in genomic data. Taken together, our results indicate that sex-specific selection is not a straightforward source of balanced genetic polymorphism and leaves few traces in the genome. Rather, we suggest that sexual antagonism is most likely to maintain genetic variation when traits are determined by a single large effect locus where genetic constraints lead to a limited range of possible alleles.

Sex-specific Dominance and Its Effects on Allelic Diversity in Sexually Antagonistic Loci

“…We model for the first time the joint evolution of allelic diversity and sex-specific dominance for a shared phenotypic trait where males and females have different optima. Our analyses of this SA pleiotropy in part confirm previous modelling efforts, such that additivity and equal dominance between the sexes can generate a stable bi-allelic dimorphism only when selection is relatively strong and symmetric between the sexes (e.g., Kidwell et al, 1977;Connallon and Clark, 2012;Arnqvist et al, 2014;Flintham et al, 2023), but they also generate a series of novel insights. We show that sex-specific dominance for the shared trait evolves readily when allowed (as in Spencer and Priest, 2016), and this has several important implications.…”

“…In contrast to previous theoretical evaluations of sexually antagonistic pleiotropy, sex-specific dominance does not emerge from curved fitness functions (Connallon and Clark, 2014;Flintham et al, 2023) in our modelling approach. Instead, we assume that dominance occurs for trait expression (see also Wittmann et al, 2017) and we also allow sex-specific dominance to evolve.…”

“…S2). For an equivalent model, Flintham et al (2023) find, using a different functional form, that x * can be an evolutionary repeller when the map from trait to sex-specific performance is accelerating. We suggest, however, that their functional form leading to this outcome is biologically unrealistic as it entails that the performance function is cusp-shaped at the sex-specific optimum.…”

“…Perhaps the most general generator of balancing selection are trade-offs resulting in antagonistic pleiotropy, whereby alternative alleles are favoured by selection in different contexts (e.g., environmental conditions, ontogenetic stages, age classes or sexes). Previous theory suggests that the conditions under which antagonistic pleiotropy maintains biallelic polymorphism (BAP) at SA loci may be quite restricted (Prout, 2000), requiring symmetric and strong selection (e.g., Kidwell et al, 1977; Flintham et al, 2023), disassortative mating by genotype (Arnqvist, 2011), dominance under sex-linkage (Rice, 1984; Patten and Haig, 2009) or dominance reversal (Kidwell et al, 1977; Fry, 2010). Dominance reversal, where each allele shows dominance in the context in which it is beneficial and recessivity when it is disfavoured, has a particularly high potential capacity to promote the maintenance of genetic variation (Kidwell et al, 1977; Wilder et al, 2016; Wittmann et al, 2017; Grieshop and Arnqvist, 2018; Connallon and Chenoweth, 2019; Grieshop et al, 2024).…”

Dominance reversals: the resolution of genetic conflict and maintenance of genetic variation

“…Below, we provide a biophysically explicit proof-of-concept for what a dominance modifier could look like and analyse its evolution using forward-time individual-based population genetic simulations ( box 1 ; electronic supplementary material S2). Our example is a starting point for a theoretical approach that would be useful in assessing both of these outstanding issues, as well as whether antagonistic selection on a phenotype can maintain genetic variation [ 109 ], whether dominance reversals compete with gene duplications [ 110 ] or other forms of resolution, and evaluating patterns in empirical data [ 78 ].…”