Evolution of genes involved in the unusual genitals of the bear macaque, Macaca arctoides

Abstract Genital divergence is thought to contribute to reproductive barriers by establishing a “lock- and-key” mechanism for reproductive compatibility. One such example, Macaca arctoides , the bear macaque, has compensatory changes in both male and female genital morphology as compared to close relatives. Macaca arctoides also has a complex evolutionary history, having extensive introgression between the fascicularis and sinica macaque species groups. Here, phylogenetic relationships were analyzed via whole genome sequences from five species, including M. arctoides , and two species each from the putative parental species groups. This analysis revealed ∼3x more genomic regions supported placement in the sinica species group as compared to the fascicularis species group. Additionally, introgression analysis of the M. arctoides genome revealed it is a mosaic of recent polymorphisms shared with both species groups. To examine the evolution of their unique genital morphology further, the prevalence of candidate genes involved in genital morphology were compared against genome-wide outliers in various population genetic metrics, while accounting for background variation in recombination rate. This analysis identified 66 outlier genes, including several genes that influence baculum morphology in mice, which were of interest since the bear macaque has the longest primate baculum. The mean of several metrics was statistically different in the candidate genes as compared to the rest of the genome, suggesting that genes involved in genital morphology have increased divergence and decreased diversity beyond expectations. These results highlight how extensive introgression may have contributed to reproductive isolation and shaped the unique genital morphology in the bear macaque.