Abstract
Reproductive isolation is a fundamental step in speciation. While sex chromosomes have been linked to reproductive isolation in many model systems, including hominids, genetic studies of the contribution of sex chromosome loci to speciation for natural populations are relatively sparse. Natural hybrid zones can help identify genomic regions contributing to reproductive isolation, like hybrid incompatibility loci, since these regions exhibit reduced introgression between parental species. Here, we use a primate hybrid zone (Alouatta palliata × Alouatta pigra) to test for reduced introgression of X-linked SNPs compared to autosomal SNPs. To identify X-linked sequence in A. palliata, we used a sex-biased mapping approach with whole-genome re-sequencing data. We then used genomic cline analysis with reduced-representation sequence data for parental A. palliata and A. pigra individuals and hybrids (n = 88) to identify regions with non-neutral introgression. We identified ~26 Mb of non-repetitive, putatively X-linked genomic sequence in A. palliata, most of which mapped collinearly to the marmoset and human X chromosomes. We found that X-linked SNPs had reduced introgression and an excess of ancestry from A. palliata as compared to autosomal SNPs. One outlier region with reduced introgression overlaps a previously described “desert” of archaic hominin ancestry on the human X chromosome. These results are consistent with a large role for the X chromosome in speciation across animal taxa and further, suggest shared features in the genomic basis of the evolution of reproductive isolation in primates.
Highlights
Reproductive isolation is a fundamental step in speciation
Because the genomic signature of ancient genetic exchanges is all that is left of our archaic cousins, it is not possible to directly investigate the mechanisms that may have lead to restricted gene flow in certain genomic regions while allowing exchange in others. We address this here by identifying genomic regions that are consistent with the signature of reproductive isolation (i.e., “barrier loci”) between 2 contemporary primate species that form a natural hybrid zone and ask whether deserts of archaic ancestry on the human X chromosome are unique to hominids or shared with other primates
Contiguous X-chromosomal sequence in A. palliata, with regions exhibiting a high degree of conservation with the human and marmoset X chromosomes, consistent with conservation of the mammalian X chromosome
Summary
Reproductive isolation is a fundamental step in speciation. While sex chromosomes have been linked to reproductive isolation in many model systems, including hominids, genetic studies of the contribution of sex chromosome loci to speciation for natural populations are relatively sparse. One outlier region with reduced introgression overlaps a previously described “desert” of archaic hominin ancestry on the human X chromosome These results are consistent with a large role for the X chromosome in speciation across animal taxa and further, suggest shared features in the genomic basis of the evolution of reproductive isolation in primates. Orr 1989) that sex chromosomes seem to be important drivers of reproductive isolation in many animal taxa (e.g., birds: Sætre et al 2003; Carling and Brumfield 2008; Irwin 2018; Drosophila: Presgraves 2008; Mus: Good et al 2008a, 2008b, 2010; Janoušek et al 2012; fish: Kitano and Peichel 2012), including humans. In hybrid flies and mice, loci underlying hybrid male sterility disproportionately map to the X chromosome, consistent with a large role of the X chromosome in speciation (e.g., Presgraves 2008; Turner and Harr 2014)
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