Haploid and Sexual Selection Shape the Rate of Evolution of Genes across the Honey Bee (Apis mellifera L.) Genome

Many species have separate haploid and diploid phases. Theory predicts that each phase should experience the effects of evolutionary forces (like selection) differently. In the haploid phase, all fitness-affecting alleles are exposed to selection, whereas in the diploid phase, those same alleles can be masked by homologous alleles. This predicts that selection acting on genes expressed in haploids should be more effective than diploid-biased genes. Unfortunately, in arrhenotokous species, this prediction can be confounded with the effects of sex-specific expression, as haploids are usually reproductive males. Theory posits that, when accounting for ploidal- and sex-specific expression, selection should be equally efficient on haploid- and diploid-biased genes relative to constitutive genes. Here, we used a multiomic approach in honey bees to quantify the evolutionary rates of haploid-biased genes and test the relative effects of sexual- and haploid-expression on molecular evolution. We found that 16% of the honey bee’s protein-coding genome is highly expressed in haploid tissue. When accounting for ploidy and sex, haploid- and diploid-biased genes evolve at a lower rate than expected, indicating that they experience strong negative selection. However, the rate of molecular evolution of haploid-biased genes was higher than diploid-based genes. Genes associated with sperm storage are a clear exception to this trend with evidence of strong positive selection. Our results provide an important empirical test of theory outlining how selection acts on genes expressed in arrhenotokous species. We propose the haploid life history stage affects genome-wide patterns of diversity and divergence because of both sexual and haploid selection.