Haploid Selection Favors Suppressed Recombination Between Sex Chromosomes Despite Causing Biased Sex Ratios

Abstract

Abstract To date, research on the evolution of sex chromosomes has focused on sexually antagonistic selection among diploids, which has been shown to be a potent driver of the strata and reduced recombination that characterize many sex chromosomes. However, significant selection can also occur on haploid genotypes during less conspicuous life cycle stages, e.g., competition among sperm/pollen or meiotic drive during gamete/spore production. These haploid selective processes are typically sex-specific, e.g., gametic/gametophytic competition typically occurs among sperm/pollen, and meiotic drive typically occurs during either spermatogenesis or oogenesis. We use models to investigate whether sex-specific selection on haploids could drive the evolution of recombination suppression on the sex chromosomes, as has been demonstrated for sex-specific selection among diploids. A potential complication is that zygotic sex-ratios become biased when haploid selected loci become linked to the sex-determining region because the zygotic sex ratio is determined by the relative number and fitness of X- vs. Y-bearing sperm. Despite causing biased zygotic sex-ratios, we find that a period of sex-specific haploid selection generally favors recombination suppression on the sex chromosomes. Suppressed recombination is favored because it allows associations to build up between haploid-beneficial alleles and the sex that experiences haploid selection most often (e.g., pollen beneficial alleles become strongly associated with the male determining region, Y or Z). Haploid selected loci can favor recombination suppression even in the absence of selective differences between male and female diploids. Overall, we expand our view of the sex-specific life cycle stages that can drive sex chromosome evolution to include gametic competition and meiotic drive. Based on our models, sex chromosomes should become enriched for genes that experience haploid selection, as is expected for genes that experience sexually antagonistic selection. Thus, we generate a number of predictions that can be evaluated in emerging sex chromosome systems.