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. While current theory predicts that biallelic polymorphism can be maintained in SA loci, particularly with strong selection or sex-specific dominance, some candidate SA loci harbour more than two segregating alleles. This highlights a gap in our understanding of the origin and maintenance of SA genetic variation. We present a mathematical model to explore the evolution of alleles at either an autosomal or an X-linked locus under SA selection, affecting a quantitative trait with distinct female and male optima. We show that additive allelic effects predict only biallelic polymorphism, and only under symmetric and relatively strong selection. 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) evolves when permitted, thus promoting the evolution of polyallelic polymorphism. We conclude that SA selection can drive the co-evolution of sex-specific dominance and polyallelic polymorphism, particularly under weak selection, which reduces the gender load. To assess these findings, we analyse segregating variation in three populations of a seed beetle model system and find support for our predictions: (i) candidate SA loci show a relatively strong signal of polyallelic polymorphism and (ii) loci with the strongest signal of polyallelic polymorphism are enriched with genes associated with known SA phenotypes.