亚洲叶猴属Trachypithecus线粒体系统发育关系－兼记菲氏叶猴Trachypithecus phayrei (Blyth, 1847)分类问题及记该属一新种
doi: 10.24272/j.issn.2095-8137.2020.254
Mitogenomic phylogeny of the Asian colobine genus Trachypithecus with special focus on Trachypithecus phayrei (Blyth, 1847) and description of a new species
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摘要: 叶猴属Trachypithecus在亚洲疣猴中多样性最高、地理分布最广，目前已知20种，其多样性被划分为四大种组。尽管已有部分研究利用形态学和分子系统学证据对该属开展了部分工作，目前对于其演化历史和系统地理学仍知之甚少。其中，菲氏叶猴Trachypithecus phayrei是叶猴属分布最广的物种之一，但目前对于该种的种下分类及不同亚种的具体分布还存在争议。因此，为了更好的探究叶猴属的系统演化关系，同时理清菲氏叶猴的种下分类问题，本研究通过对野外粪便样品及博物馆实体标本的研究分析，获得了包括2分模式标本在内的41份线粒体基因组数据，并以此构建了叶猴属系统演化关系。结果成功解析了叶猴属物种间的演化关系，并指出戴帽叶猴T. pileatus种组的物种首先从其余物种中分化，其次是黑叶猴T. francoisi种组，而银叶猴种组T. cristatus和郁乌叶猴T. obscurus种组分化最晚。四大种组相互分化的时间大约在4.5–3.1个百万年前，而每个种组内物种形成的时间则更晚，约在1.6–0.3个百万年前。就菲氏叶猴而言，结果显示其包含了3个分化时间在1.0–0.9个百万年的支系，暗示了其实际包括了3个独立物种。基于系统演化物种概念，在综合考虑形态、分子和生态学差异后，本研究将原菲氏叶猴的滇西亚种T. p. shanicus提升至种级，并在此将缅甸中部的种群描述为一新种，并更新了厘定后三种的具体分布信息。本研究结果再次表明了博物馆馆藏标本对于科学研究的重要性，同时为整个叶猴属及菲氏叶猴这一物种的系统演化关系提供了更新数据。Abstract: Trachypithecus, which currently contains 20 species divided into four groups, is the most speciose and geographically dispersed genus among Asian colobines. Despite several morphological and molecular studies, however, its evolutionary history and phylogeography remain poorly understood. Phayre’s langur (Trachypithecus phayrei) is one of the most widespread members of the genus, but details on its actual distribution and intraspecific taxonomy are limited and controversial. Thus, to elucidate the evolutionary history of Trachypithecus and to clarify the intraspecific taxonomy and distribution of T. phayrei, we sequenced 41 mitochondrial genomes from georeferenced fecal samples and museum specimens, including two holotypes. Phylogenetic analyses revealed a robustly supported phylogeny of Trachypithecus, suggesting that the T. pileatus group branched first, followed by the T. francoisi group, and the T. cristatus and T. obscurus groups most recently. The four species groups diverged from each other 4.5–3.1 million years ago (Ma), while speciation events within these groups occurred much more recently (1.6–0.3 Ma). Within T. phayrei, we found three clades that diverged 1.0–0.9 Ma, indicating the existence of three rather than two taxa. Following the phylogenetic species concept and based on genetic, morphological, and ecological differences, we elevate the T. phayrei subspecies to species level, describe a new species from central Myanmar, and refine the distribution of the three taxa. Overall, our study highlights the importance of museum specimens and provides new insights not only into the evolutionary history of T. phayrei but the entire Trachypithecus genus as well.
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Key words:
- Colobinae /
- Integrative zoology /
- Mitochondrial genome /
- Museum specimens /
- New species
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Figure 1. Distribution of Trachypithecus phayrei according to IUCN Red List (Bleisch et al., 2020)
Numbers indicate sample locations for genetic analysis: 1: Letsegan, 2: Kin, 3: Dudaw-Taung, 4: Ramree Island, 5: near Mount Arakan, 6: Mount Popa, 7: 30 miles northwest of Toungoo, 8: Bago Yoma, 9: South Zamayi Reserve, 10: Myogyi Monastery, 11: Panlaung-Pyadalin Cave Wildlife Sanctuary, 12: Mount Yathae Pyan, 13: Yado, 14: Ho Mu Shu Pass, 15: Gaoligong Mountains National Park, 16: Cadu Ciaung, 17: Ngapyinin, 18: Lamaing, 19: Nattaung, 20: Gokteik, and 21: Se’en (for additional information see Supplementary Table S1). Underlined sites refer to type localities of examined holotypes (16: Presbytis melamera, 21: Pithecus shanicus).
Figure 2. Mitogenomic tree showing phylogenetic relationships and divergence times among mitochondrial lineages of Trachypithecus (A) and detailed view on T. phayrei (B)
Node bars indicate 95% highest posterior densities (HPDs). Node supports of <100% ML BS and <1.0 BI PP are given at respective nodes. In A, species group assignment is given on the right; *: T. crepusculus, a member of the T. obscurus group according to phenotype and nuclear sequence data. In B, sample labels contain individual ID and sample location number (as in Figures 1, 5, Supplementary Table S1). Clade assignment is given on the right. Complete ultrametric tree including all non-Trachypithecus taxa and details on estimated divergence times are provided in Supplementary Figure S1 and Table S4, respectively.
Figure 5. Geographical distribution of mitochondrial clades found in Trachypithecus phayrei
Sample locations are numbered as in Figures 1, 2 (see also Supplementary Table S1) and colored according to their mitochondrial clade assignment. Limits of the Central clade to the northeast and East clade to the southwest, depicted in light green, are not yet firmly resolved. Samples from locations 6–9 form Central clade A, while those from locations 10–12 cluster in Central clade B. Note, at location 10, haplotypes of the Central and East clades were found. Museum specimen from location 13 cluster unexpectedly with Central clade A (see Results).
Figure 3. Head-body length (A), tail length (B), and tail/head-body length ratio (C) of adult male and female Trachypithecus phayrei representing West, Central, and East clades (median, quartiles, min-max)
Numbers in brackets: sample sizes; post-hoc pair-wise population comparisons of traits; Mann-Whitney U-test, with Bonferroni correction for multiple testing: *: P<0.025, (*): P<0.05; see Supplementary Table S6.
Figure 4. Morphometric comparisons (principal component analysis performed on 12 molar measurements) among Trachypithecus phayrei individuals representing West (red), Central (blue), and East (yellow) clades
Shown is projection of specimen scores of first and second principal components, with variance explained by each component (graphical depictions of third principal component appear in Supplementary Figure S2 and underlying statistics are provided in Supplementary Table S7.)
Figure 6. Photos of Trachypithecus phayrei (A, B), Trachypithecus popa sp. nov. (C, D) and Trachypithecus melamera (formerly T. p. shanicus) (E, F)
A: Adult female T. phayrei at Yangon Zoo, Myanmar (photo by Tilo Nadler); B: Adult male T. phayrei from Lawachara National Park, Bangladesh (photo by Tanvir Ahmed); C, D: Subadult male T. popa from Mount Popa, Myanmar (photo by Lay Win); E: Adult female T. melamera at Mandalay Zoo, Myanmar (photo by Tilo Nadler), F: Adult female T. melamera with offspring from Gaoligong Mountains National Park, China (photo by Chi Ma).
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