Hybrid origin of a primate, the gray snub-nosed monkey

Abstract

Hybridization is widely recognized as promoting both species and phenotypic diversity. However, its role in mammalian evolution is rarely examined. We report historical hybridization among a group of snub-nosed monkeys ( Rhinopithecus ) that resulted in the origin of a hybrid species. The geographically isolated gray snub-nosed monkey Rhinopithecus brelichi shows a stable mixed genomic ancestry derived from the golden snub-nosed monkey ( Rhinopithecus roxellana ) and the ancestor of black-white ( Rhinopithecus bieti ) and black snub-nosed monkeys ( Rhinopithecus strykeri ). We further identified key genes derived from the parental lineages, respectively, that may have contributed to the mosaic coat coloration of R. brelichi , which likely promoted premating reproductive isolation of the hybrid from parental lineages. Our study highlights the underappreciated role of hybridization in generating species and phenotypic diversity in mammals.

INTRODUCTION Hybridization is increasingly recognized as an important evolutionary force for generating species and phenotypic diversity in plants and animals. This is especially common in lineages that can tolerate whole-genome duplication and increased levels of ploidy. However, the role of hybridization in generating species and phenotypic diversity of lineages without polyploidization is underappreciated, especially in nonhominoid mammals. RATIONALE The snub-nosed monkey genus Rhinopithecus comprises five allopatric and morphologically differentiated species, the black-white snub-nosed monkey Rhinopithecus bieti , the black snub-nosed monkey Rhinopithecus strykeri , the golden snub-nosed monkey Rhinopithecus roxellana , the gray snub-nosed monkey Rhinopithecus brelichi , and the Tonkin snub-nosed monkey Rhinopithecus avunculus . They possess the same chromosome number, and it has been speculated that they have hybridized in the past. To examine the speciation histories of these species, we generated a chromosome-level high-quality reference genome assembly for the black-white snub-nosed monkey and analyzed 106 resequenced genomes of individuals from all five species. We conducted multiple population genomic analyses—including ADMIXTURE, D-statistics, phylogenetic reconstruction, and evolutionary scenario simulations—to investigate the genomic admixture of these species. We further applied genomic selective scans and functional assays to reveal the likely genetic basis of mosaic coat coloration of the hybrid species. Possible mechanisms of premating and postmating reproductive isolation barriers between the hybrid species and its parents are briefly discussed. RESULTS We show that historical hybridization directly resulted in the origin of the gray snub-nosed monkey. Population genomic analyses provided evidence for apparent genomic admixture across genomes of all gray snub-nosed monkeys from two parental lineages, the golden snub-nosed monkey and an ancestor of the black-white/black snub-nosed monkeys, with the majority of genome derived from the golden snub-nosed monkey. As a result of hybridization, the hybrid species possesses a mosaic of the color patterns of its parents. Genomic selection scans and functional assays identify several key melanogenesis-related genes ( PAH , APC , SLC45A 2, MYO7A , and ELOVL 4). Alleles of these genes were alternately inherited from each parent, likely producing the mosaic coat coloration of the hybrid monkey and promoting premating reproductive isolation of the hybrid species from both parents. In addition, alternate inheritance of divergent alleles at many loci, especially those involved in genetic incompatibility between the parents, may have contributed to postmating reproductive isolation of the gray snub-nosed monkey. CONCLUSION We report a notable example of hybrid speciation in primates and present a detailed evolutionary scenario from the genomic admixture to the likely reproductive isolation establishment owing to alternate inheritance of divergent alleles from parents. This study highlights the underappreciated role of interspecific hybridization in species and phenotypic diversity in mammals. The hybrid origin and genetic basis of mosaic coat coloration for the gray snub-nosed monkey. Interspecific hybridization between the golden snub-nosed monkey and the ancestor of black-white/black snub-nosed monkeys led to the genomic admixture of the gray snub-nosed monkey. Alleles of positively selected genes related to melanogenesis were alternately inherited from parental lineages A and B and contributed to the mosaic coat coloration of the hybrid species.