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| Popa langur Trachypithecus popa Roos, Helgen, Miguez, Thant, Lwin, et al., 2020 photo: Thaung Win |
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.
Keywords: Colobinae, Integrative zoology, Mitochondrial genome, Museum specimens, New species
Systematic biology
Order Primates Linnaeus, 1758
Family Cercopithecidae Gray, 1821
Subfamily Colobinae Jerdon, 1867
Genus Trachypithecus Reichenbach, 1862
Trachypithecus phayrei (Blyth, 1847)
English name: Phayre’s langur.
Synonyms: Presbytis barbei Blyth, 1863;
Semnopithecus holotephreus Anderson, 1878.
Distribution: East Bangladesh, Northeast India (Assam, Mizoram, and Tripura), and West Myanmar, west of the Chindwin and Ayeyarwaddy rivers (Figure 5).
Conservation status: Currently listed as Endangered (Bleisch et al., 2008a), but reassessment required.
Trachypithecus melamera (Elliot, 1909)
English name: Shan State langur.
Synonyms: Pithecus shanicus Wroughton, 1917.
Distribution: East Myanmar (Shan States) and Southwest China (West Yunnan), between the Ayeyarwaddy and Thanlwin rivers, with the southwestern limit probably extending into the Kayah-Karen Mountains (Figure 5).
Conservation status: Currently listed as Endangered (Bleisch et al., 2008b), but reassessment required.
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| Popa langur Trachypithecus popa photo: Thaung Win |
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| Popa langur Trachypithecus popa is seen on a tree branch on Mount Popa, Myanmar. Photograph: Thaung Win/GERMAN PRIMATE CENTER |
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| Figure 6. Photos of Trachypithecus phayrei (A, B), Trachypithecus popa sp. nov. (C, D) and Trachypithecus melamera (formerly T. p. shanicus) (E, F) |
Trachypithecus popa sp. nov.
Popa langur
Etymology: The English name for Trachypithecus popa is Popa langur. Mount Popa is a major landmark of the Myingyan District in Myanmar, and the place where the designated holotype was originally collected. The specific name “popa” is used as a noun in apposition.
Diagnosis: Overall, Trachypithecus popa sp. nov. is externally more similar to T. phayrei than to T. melamera. Body coloration in all three species is variable, but generally more fawn in T. melamera and more brownish to gray in Trachypithecus popa sp. nov. and T. phayrei. In Trachypithecus popa sp. nov. and T. phayrei, but not in T. melamera, the pale venter sharply contrasts with the back. The hands and feet are black in all three species. In Trachypithecus popa sp. nov., the arms (dorsal side) gradually darken to the hands from above the elbow, while in T. phayrei, they gradually darken from below the elbow. In T. melamera, the lower arms are not darker than the upper arms. In Trachypithecus popa sp. nov. and T. phayrei, the hairs on the head are raised to a crest or are at least long and irregularly structured, while T. melamera has a whorl or a parting behind the brows. Whiskers are laterally directed in T. phayrei, but forward directed in Trachypithecus popa sp. nov. and T. melamera. The direction of the whiskers in combination with the hairs on the head gives the head of T. phayrei a triangular shape, versus a rhomb-like shape for Trachypithecus popa sp. nov. and a round shape for T. melamera. All three species have a fleshy-white muzzle, which is wider in Trachypithecus popa sp. nov. and T. melamera. In T. melamera, the white around the eyes is restricted to the inner side, while in T. phayrei, the white normally encircles the eyes fully, although it is sometimes restricted to the inner side. In Trachypithecus popa sp. nov., the eyes are always fully encircled with broad white eye-rings. Males of T. phayrei have significantly shorter tails than males of the other two species (Figure 3, Supplementary Tables S5–S6).
Cranially, Trachypithecus popa sp. nov. has a slightly longer skull, especially relative to its width, than in T. phayrei and T. melamera; this is achieved by a slight anterior elongation of the facial region of the skull relative to these taxa, rendering Trachypithecus popa sp. nov. slightly more prognathic in lateral and dorsal views and creating a more rectangular shape of the bony palate in ventral view (vs. a more square palate in T. phayrei and T. melamera). The teeth are, on average, larger in Trachypithecus popa sp. nov. than in T. phayrei and T. melamera, and molar measurements are the clearest means for separating the skulls of this new taxon from its closest relatives (Supplementary Tables S3, S7; Figure 4, Supplementary Figures S2–S3); in particular, the third molar (M3/m3) appears larger overall in Trachypithecus popa sp. nov. when skulls are directly compared. PCAs using molar measurements and combined craniodental measurements separated T. phayrei, T. melamera, and Trachypithecus popa sp. nov., but cranial measurements alone did not separate them (Figure 4, Supplementary Figures S2, S3).
Distribution: Between the Ayeyarwaddy and Thanlwin rivers in the central dry zone of Myanmar and into the western foothills of the Kayah-Karen Mountains (Figure 5). The northeastern limit is undefined (see Discussion), but the species may occur throughout the Kayah-Karen Mountains. This species is endemic to Myanmar.
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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). |
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| 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). |
CONCLUSIONS:
We present a robust mitogenomic species-level phylogeny of the genus Trachypithecus, thus providing new insights into the evolutionary history of the genus and forming a basis for future work. Based on our investigations of T. phayrei, we illuminated the intraspecific taxonomy of the species, resulting in the elevation of two known subspecies to species level, renaming of one subspecies, description of a new species, and largely refined distributional ranges for all three species. Including the proposed taxonomic changes, the genus Trachypithecus now contains 22 species, with Myanmar home to a total of 20 non-human primate species (Trachypithecus popa sp. nov., T. phayrei, T. melamera, T. barbei, T. obscurus, T. crepusculus, T. shortridgei, T. pileatus, Presbytis femoralis, Rhinopithecus strykeri, Macaca mulatta, M. fascicularis, M. arctoides, M. assamensis, M. leonina, Hoolock hoolock, H. leuconedys, H. tianxing, Hylobates lar, and Nycticebus bengalensis; Fan et al., 2017; Mittermeier et al., 2013; Roos et al., 2014; Rowe & Myers, 2016), of which Trachypithecus popa sp. nov. and probably H. leuconedys are endemic to the country. Trachypithecus germaini, commonly listed for Myanmar (e.g., Anandam et al., 2013; Groves, 2001; Roos et al., 2014; Rowe & Myers, 2016), is actually not present in the country. Its putative occurrence in Myanmar is based on the incorrect assignment of Pithecus pyrrhus atrior as a synonym of T. germaini instead of T. barbei (Geissmann et al., 2004; C.R., unpublished data).
Overall, our study reaffirms that museum collections are a valuable source for genetic and taxonomic investigations of primates, particularly as modern high-throughput sequencing technologies allow the analysis of highly damaged DNA, which is typically extracted from such material. Future studies on Trachypithecus should also include nuclear sequence data and multiple individuals per species and should focus on the three polytypic species of the genus, i.e., T. pileatus, T. cristatus, and T. obscurus.
Christian Roos, Kristofer M. Helgen, Roberto Portela Miguez, Naw May Lay Thant, Ngwe Lwin, Aung Ko Lin, Aung Lin, Khin Mar Yi, Paing Soe, Zin Mar Hein, Margaret Nyein Nyein Myint, Tanvir Ahmed, Dilip Chetry, Melina Urh, E. Grace Veatch, Neil Duncan, Pepijn Kamminga, Marcus A. H. Chua, Lu Yao, Christian Matauschek, Dirk Meyer, Zhi-Jin Liu, Ming Li, Tilo Nadler, Peng-Fei Fan, Le Khac Quyet, Michael Hofreiter, Dietmar Zinner and Frank Momberg. 2020. Mitogenomic Phylogeny of the Asian Colobine Genus Trachypithecus with Special Focus on Trachypithecus phayrei (Blyth, 1847) and Description of A New Species. Zoological Research. 41(6), 656-669. DOI:
New species of monkey is already critically endangered
