The bear bones: mosaic ancestry of Macaca arctoides explains divergent baculum morphology
AbstractGenital divergence contributes to reproductive barriers between species. Emergence of a novel accessory structure, the baculum, has independently evolved and been lost throughout mammalian evolution, purportedly driven by sexual selection. In primates, the longest recorded baculum belongs to Macaca arctoides, the bear macaque. This species has been proposed to be of homoploid hybrid origin via ancient hybridization between representatives from the fascicularis and sinica species groups. To investigate the evolutionary origins of the bear macaque and its unique morphology, we used whole genome sequences to quantify gene flow and phylogenetic relationships in 10 individuals from 5 species, including the bear macaque (n=3), and two species each from the sinica (n=3) and fascicularis (n=4) species groups. The results of these analyses were concordant, and identified 608 genes in the bear macaque that supported both clustering between M. arctoides and the sinica group (topo2) and had shared derived alleles between species from the two groups. Similarly, 361 genes supported both clustering between M. arctoides and the fascicularis group (topo3) and had shared derived alleles between both groups. Further, sliding window analysis of phylogenetic relationships revealed 53% of the genomic regions supported placement of M. arctoides in the sinica species group (topo2), 16% supported placement in the fascicularis species group (topo3), and 11% supported M. arctoides in a grouping distinct from the sinica and fascicularis groups (topo1). Genomic regions with topo1 were intersected with previously identified QTL for mouse baculum morphology, and 47 genes were found, including five of sixteen major candidate loci that govern mouse baculum variation (KIF14, KIAA0586, RHOJ, TGM2, and DACT1). Although baculum morphology in the bear macaque is diverged from its parent taxa, it most closely resembles that of the fascicularis group. Outliers of shared ancestry from the fascicularis species group located within these same QTL regions overlap with the gene BMP4, which is an important component of the hedgehog signaling pathway that controls gonadogenesis. Two additional outlier genes (one shared with each species group) outside of the baculum QTL are known to interact with BMP4, suggesting this pathway may be involved in baculum morphology in primates. These results highlight how the mosaic ancestry of the bear macaque could explain its unique baculum evolution and collectively contribute to reproductive isolation.Introductory ParagraphIn mammals, the baculum has extreme morphological variability, a dynamic evolutionary history characterized by repeated gain and loss, and is often used in species identification. The bear macaque has divergent genital morphology, including the longest baculum among all primates, and is proposed to have evolved via ancient hybrid speciation. Here, population genetic and phylogenomic approaches were used to examine how ancient hybridization in the bear macaque may have shaped this important component of genital morphology. Results demonstrate extensive mosaicism across the genome, which is consistent with ancient genetic contributions from both putative parental taxa. Genetic regions associated with baculum morphology also had mosaic ancestry for several genes, including KIF14 and KIAA0586, major candidate genes for baculum morphology in mice, and BMP4, a developmental gene involved in gonadogenesis. These results have important implications for how hybridization may have shaped the evolution of reproductive isolation in this unusual species with complex speciation.
