Population Genetics of Reproductive Genes in Haplodiploid Species

Abstract

Abstract Many animal species are haplodiploid: their fertilized eggs develop into diploid females and their unfertilized eggs develop into haploid males. The unique genetic features of haplodiploidy raise the prospect that these systems can be used to disentangle the population genetic consequences of haploid and diploid selection. To this end, sex-specific reproductive genes are of particular interest because, while they are shared within the same genome, they consistently experience selection in different ploidal environments. However, other features of these genes, including sex-specific expression and putative involvement in postcopulatory sexual selection, are potentially confounding factors because they may also impact the efficacy of selection asymmetrically between the sexes. Thus, to properly interpret evolutionary genomic patterns, it is necessary to generate a null expectation for the relative amount of polymorphism and divergence we expect to observe among sex-specific genes in haplodiploid species, given differences in ploidal environment, sex-limited expression, and their potential role in sexual selection. Here, we derive the theoretical expectation for the rate of evolution of sex-specific genes in haplodiploid species, under the assumption that they experience the same selective environment as genes expressed in both sexes. We find that the null expectation is that reproductive genes evolve more rapidly than constitutively expressed genes in haplodiploid genomes. However, despite the aforementioned differences, the null expectation does not differ between male- and female-specific reproductive genes, when assuming additivity. Our theoretical results provide an important baseline expectation that should be used in molecular evolution studies comparing rates of evolution among classes of genes in haplodiploid species.