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

Abstract Sexually antagonistic (SA) selection, favouring different alleles in males and females, can contribute to the maintenance of genetic diversity. Current theory predicts that biallelic polymorphism can be maintained in SA loci under strong selection or dominance reversal in the sexes. Yet, selection should often be weak, several candidate SA loci harbour more than two segregating alleles and dominance reversal may not be common. We present a general model to explore the evolution of alleles at autosomal and X-linked loci under SA selection, affecting a quantitative trait with distinct female and male optima. We confirm that additive allelic effects predict biallelic polymorphism, but only under symmetric and relatively strong selection. However, polyallelic polymorphism can evolve under conditions of sex-specific or X-linked dominance for the trait, particularly under weak selection, such that several alleles coexist in a single population through balancing selection. Our analysis furthermore shows that sex-specific dominance and X-linked dominance evolve when permitted, thus polyallelic polymorphism is a likely evolutionary outcome. We conclude that SA selection can drive the co-evolution of differences in dominance between the sexes and polyallelic polymorphism, particularly under weak selection, an outcome reducing the gender load. To assess these findings, we analyse segregating variation in three populations of an insect model system and find that (1) loci with the strongest signal of polyallelic polymorphism are enriched with functions associated with known SA phenotypes and (2) both candidate SA loci and loci exhibiting sex-specific dominance show a stronger signal of polyallelic polymorphism. Competing Interest Statement The authors have declared no competing interest. Footnotes ↵† These authors share senior authorship Updated empirical results and improved presentation of mathematical analysis