Is the X chromosome a hot spot for sexually antagonistic polymorphisms? Biases in current empirical tests of classical theory.

ABSTRACT

Females and males carry nearly identical genomes, which can constrain the evolution of sexual dimorphism and generate conditions that are favourable for maintaining sexually antagonistic (SA) polymorphisms, in which alleles beneficial for one sex are deleterious for the other. An influential theoretical prediction, by Rice (Rice 1984 Evolution38, 735-742), is that the X chromosome should be a 'hot spot' (i.e. enriched) for SA polymorphisms. While important caveats to Rice's theoretical prediction have since been highlighted (e.g. by Fry (2010) Evolution64, 1510-1516), several empirical studies appear to support it. Here, we show that current tests of Rice's theory-most of which are based on quantitative genetic measures of fitness (co)variance-are frequently biased towards detecting X-linked effects. We show that X-linked genes tend to contribute disproportionately to quantitative genetic patterns of SA fitness variation whether or not the X is enriched for SA polymorphisms. Population genomic approaches for detecting SA loci, including genome-wide association study of fitness and analyses of intersexual FST, are similarly biased towards detecting X-linked effects. In the light of our models, we critically re-evaluate empirical evidence for Rice's theory and discuss prospects for empirically testing it.