Divergence and introgression in small apes, the genus Hylobates, revealed by reduced representation sequencing

Abstract

Gibbons in the genus Hylobates, which live in Southeast Asia, show great diversity, comprising seven to nine species. Natural hybridisation has been observed in the species contact zones, although the roles played by hybridisation and introgression in the evolution of these species remain unclear. To uncover the divergence history and the contributions of hybridisation and introgression to the evolution of Hylobates, random amplicon sequencing-direct (GRAS-Di) analysis was employed to genotype 47 gibbons, representing eight species from three genera. After quality filtering, over 300,000 autosomal single-nucleotide variant (SNV) sites were identified. The SNV-based autosomal phylogeny, together with the mitochondrial phylogeny, supported a divergence pattern beginning approximately 4.3 million years ago. First, the mainland species, H. pileatus and H. lar, consecutively diverged from the Sundaic island species. Second, H. moloch, in Java (and likely H. klossii, in the Mentawai Islands) diverged from the other species. Third, H. muelleri, in Borneo, and H. agilis/H. albibarbis, in Sumatra and southwestern Borneo, diverged. Lastly, H. agilis and H. albibarbis diverged from each other. The Pattersons D-statistics indicated significant introgression between H. lar and H. pileatus, between H. lar and H. agilis, and between H. albibarbis and H. muelleri, and weak introgression was identified between H. moloch and H. albibarbis, and between H. moloch and H. muelleri abbotti, suggesting incomplete reproductive barriers among Hylobates species and that hybridisation and introgression occur whenever the distribution ranges contact. Some candidates for introgressed genomic regions were detected, and the functions of these would be revealed by further genome-wide studies.