Ancient hybridization and admixture in macaques (genus Macaca) inferred from whole genome sequences

Mol Phylogenet Evol. 2018 Oct;127:376-386. doi: 10.1016/j.ympev.2018.03.038. Epub 2018 Mar 31.


The evolutionary history of the stump-tailed macaque (Macaca arctoides) and its genetic relationship to other macaques is a subject of continuing controversy. Here, we have reported the first genome sequences of two stump-tailed macaques and one Assamese macaque (M. assamensis). Additionally, we have investigated the genetic diversity between macaque species and analyzed ancient hybridization events. Genome-wide analyses demonstrated that the stump-tailed macaque is more closely related to sinica species than to fascicularis/mulatta species. This topology contradicts the mitochondrial sequence-based phylogeny that places the stump-tailed macaque into the fascicularis/mulatta group. However, our results further show that stump-tailed macaques have genetic backgrounds distinct from sinica species, and present evidence of gene flows with rhesus macaques. We suggest that an ancient introgression occurred after stump-tailed macaques diverged from sinica species. The distinct gene flow between proto-arctoides and proto-mulatta resulted in the transfer of rhesus macaque-type mitochondria into proto-arctoides. The rhesus macaque-type mitochondria remained in populations because of genetic drift during the bottleneck. The PSMC results and morphological and geographic evidence are consistent with the mitochondria capture pattern in the stump-tailed macaque. The molecular clock estimates suggest that the mitochondrial transference into stump-tailed macaques occurred 0.4-1.4 million years ago. Furthermore, we detected extensive admixtures between different macaque species, indicating that gene flow has played an important role in the evolutionary history of the genus Macaca.

Keywords: Genetic diversity; Genome evolution; Hybridization; Primate.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Base Sequence
  • Gene Flow*
  • Genetic Variation
  • Genome*
  • Heterozygote
  • Hybridization, Genetic*
  • Macaca mulatta / genetics*
  • Phylogeny
  • Polymorphism, Single Nucleotide / genetics
  • Principal Component Analysis
  • Whole Genome Sequencing*