Breaking the rule: An exceptional Y chromosome introgression between deeply divergent primate species

Abstract

Hybridization between distinct lineages is widespread in nature, with important implications for adaptation and speciation. If hybrids are fertile, alleles can introgress across species boundaries. Hybrid fitness is often sex dependent, with heterogametic hybrids showing lower fitness than homogametic individuals, a phenomenon known as Haldanes rule. Consequently, loci inherited strictly through the heterogametic sex rarely introgress. We focus on the Y-chromosomal history of guenons (tribe Cercopithecini), a group of African primates that hybridized extensively throughout their evolutionary history. Although our inferences suggest that Haldanes rule is generally in place, we uncover a remarkable Y chromosome introgression event from Cercopithecus mitis into C. denti, which occurred ca. six million years after their initial divergence. Only a weak signal of autosomal gene flow is present, suggesting that the introgressing Y chromosome reached fixation in C. denti from a very low initial frequency. We use simulations to explore the evolutionary mechanisms at play, and find that selection is needed to achieve fixation of the novel Y chromosome. We identify a number of fixed protein differences between the introgressed and ancestral Y, with meiotic drive being an alternative mechanism to adaptive introgression. Our results show that the ability to produce viable and fertile heterogametic hybrids persisted for six million years in guenons, providing a remarkable exception to Haldanes rule.