Testing Sex-Biased Admixture Origin of Macaque Species Using Autosomal and X-Chromosomal Genomic Sequences

The role of sex-specific demography in hybridization and admixture of genetically diverged species and populations is essential to understand the origins of the genomic diversity of sexually reproducing organisms. In order to infer how sex-linked loci have been differentiated undergoing frequent hybridization and admixture, we examined 17 whole-genome sequences of seven species representing the genus Macaca, which shows frequent inter-specific hybridization and predominantly female philopatry. We found that hybridization and admixture were prevalent within these species. For three cases of suggested hybrid origin of species/subspecies, Macaca arctoides, Macaca fascicularis ssp. aurea, and Chinese Macaca mulatta, we examined the level of admixture of X chromosomes, which is less affected by male-biased migration than that of autosomes. In one case, we found that Macaca cyclopis and Macaca fuscata was genetically closer to Chinese M. mulatta than to the Indian M. mulatta, and the admixture level of Chinese M. mulatta and M. fuscata/cyclopis was more pronounced on the X chromosome than on autosomes. Since the mitochondrial genomes of Chinese M. mulatta, M. cyclopis, and M. fuscata were found to cluster together, and the mitochondrial genome of Indian M. mulatta is more distantly related, the observed pattern of genetic differentiation on X-chromosomal loci is consistent with the nuclear swamping hypothesis, in which strong, continuous male-biased introgression from the ancestral Chinese M. mulatta population to a population related to M. fuscata and M. cyclopis generated incongruencies between the genealogies of the mitochondrial and nuclear genomes.