Multilocus phylogeny suggests a distinct species status for the Nepal population of Assam macaques ( Macaca assamensis): implications for evolution and conservation

Zool Res. 2021 Jan 18;42(1):3-13. doi: 10.24272/j.issn.2095-8137.2020.279.


Phylogenetic relationships within the sinica-group of macaques based on morphological, behavioral, and molecular characteristics have remained controversial. The Nepal population of Assam macaques ( Macaca assamensis) (NPAM), the westernmost population of the species, is morphologically distinct but has never been used in phylogenetic analyses. Here, the phylogenetic relationship of NPAM with other congeners was tested using multiple mitochondrial and Y-chromosomal loci. The divergence times and evolutionary genetic distances among macaques were also estimated. Results revealed two major mitochondrial DNA clades of macaques under the sinica-group: the first clade included M. thibetana, M. sinica, and eastern subspecies of Assam macaque ( M. assamensis assamensis); the second clade included M. radiata together with species from the eastern and central Himalaya, namely, M. leucogenys, M. munzala, and NPAM. Among the second-clade species, NPAM was the first to diverge from the other members of the clade around 1.9 million years ago. Our results revealed that NPAM is phylogenetically distinct from the eastern Assam macaques and closer to other species and hence may represent a separate species. Because of its phylogenetic distinctiveness, isolated distribution, and small population size, the Nepal population of sinica-group macaques warrants detailed taxonomic revision and high conservation priority.

长期以来,基于形态、行为和分子特征的猕猴属( Macaca)斯里兰卡猴种组( sinica group)系统发育关系一直饱受争议。熊猴( M. assamensis)尼泊尔种群生活在该物种分布范围的最西部,形态特征独特,但其系统发育关系仍未有相关研究。本研究利用多个线粒体和Y染色体基因位点检验熊猴尼泊尔种群与其他猕猴间的系统发育关系,估算其分化时间与遗传距离。结果显示,斯里兰卡猴种组分化为两个主要分支:第一个分支包括藏酋猴( M. thibetana)、斯里兰卡猴( M. sinica)和熊猴指名亚种( M. assamensis assamensis),第二个分支包括帽猴( M. radiata)、喜马拉雅山脉东部和中部的白颊猕猴( M. leucogenys)、达旺猴( M. munzala)和熊猴尼泊尔种群。在第二分支当中,熊猴尼泊尔种群大约于1.9百万年前最先与该分支其他成员分开。研究结果揭示熊猴尼泊尔种群与东部的熊猴指名亚种显著分化,而与白颊猕猴和达旺猴更接近,说明熊猴尼泊尔种群可能是一个独立的物种。由于其系统发育关系特殊、分布区隔离且种群数量少,斯里兰卡猴种组尼泊尔种群亟需详细的分类修订并采取相应优先保护措施。.

Keywords: Himalaya; Macaques; Paraphyletic; Taxonomy; sinica-group.

MeSH terms

  • Animal Distribution*
  • Animals
  • Biological Evolution*
  • Conservation of Natural Resources*
  • DNA, Mitochondrial / genetics
  • Female
  • Macaca / classification
  • Macaca / genetics*
  • Macaca / physiology
  • Male
  • Multilocus Sequence Typing
  • Nepal
  • Phylogeny*
  • RNA, Ribosomal, 16S / genetics
  • Species Specificity
  • Time Factors
  • Y Chromosome


  • DNA, Mitochondrial
  • RNA, Ribosomal, 16S

Grant support

This study was supported by the Chinese Academy of Sciences-World Academy of Sciences (CAS-TWAS) President’s PhD Fellowship Program to L.K., Second Tibetan Plateau Scientific Expedition and Research Program (2019QZKK0501), and National Key Research and Development Plan (#2017YFC0505202) China. R.C.K. was supported in part by the Office of Research Infrastructure Programs (ORIP) of the National Institutes of Health through Grant Number P51OD010425 to the WaNPRC. L.K. was supported by the Rufford Small Grants (17666-1) of Rufford Foundation, UK partly for fieldworks