Volume 42 Issue 1
Jan.  2021
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Laxman Khanal, Mukesh Kumar Chalise, Peng-Fei Fan, Randall C. Kyes, Xue-Long Jiang. Multilocus phylogeny suggests a distinct species status for the Nepal population of Assam macaques (Macaca assamensis): implications for evolution and conservation. Zoological Research, 2021, 42(1): 3-13. doi: 10.24272/j.issn.2095-8137.2020.279
Citation: Laxman Khanal, Mukesh Kumar Chalise, Peng-Fei Fan, Randall C. Kyes, Xue-Long Jiang. Multilocus phylogeny suggests a distinct species status for the Nepal population of Assam macaques (Macaca assamensis): implications for evolution and conservation. Zoological Research, 2021, 42(1): 3-13. doi: 10.24272/j.issn.2095-8137.2020.279

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

doi: 10.24272/j.issn.2095-8137.2020.279
Funds:  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
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  • 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.
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  • [1]
    Biswas J, Borah DK, Das A, Das J, Bhattacharjee PC, Mohnot SM, Horwich RH. 2011. The enigmatic Arunachal macaque: its biogeography, biology and taxonomy in northeastern India. American Journal of Primatology, 73(5): 458−473. doi: 10.1002/ajp.20924
    Boonratana R, Chalise MK, Das J, Htun S, Timmins RJ. 2020(2020-07-12). The IUCN red list of threatened species. https://www.iucn.org/theme/species/our-work/iucn-red-list-threatened-species.
    Bunlungsup S, Imai H, Hamada Y, Gumert MD, San AM, Malaivijitnond S. 2016. Morphological characteristics and genetic diversity of Burmese long-tailed Macaques (Macaca fascicularis aurea). American Journal of Primatology, 78(4): 441−455. doi: 10.1002/ajp.22512
    Chakraborty D, Ramakrishnan U, Panor J, Mishra C, Sinha A. 2007. Phylogenetic relationships and morphometric affinities of the Arunachal macaque Macaca munzala, a newly described primate from Arunachal Pradesh, northeastern India. Molecular Phylogenetics and Evolution, 44(2): 838−849.
    Chakraborty D, Sinha A, Ramakrishnan U. 2014. Mixed fortunes: ancient expansion and recent decline in population size of a subtropical montane primate, the Arunachal macaque Macaca munzala. PLoS One, 9(7): e97061. doi: 10.1371/journal.pone.0097061
    Chalise MK. 2005. Characteristics of the Assamese monkey (Macaca assamensis) of Nepal. American Journal of Primatology, 66: 195.
    Chalise MK. 2008. Primate census in Kathmandu and west parts of Nepal. Journal of natural History Museum, 23: 60−64.
    Chalise MK. 2013. Fragmented primate population of Nepal. In: Marsh LK, Chapman CA. Primates in Fragments: Complexity and Resilience. New York: Springer, 329–356.
    Deinard A, Smith DG. 2001. Phylogenetic relationships among the macaques: evidence from the nuclear locus NRAMP1. Journal of Human Evolution, 41(1): 45−59. doi: 10.1006/jhev.2001.0480
    Delson E. 1980. Fossil macaques, phyletic relationships and a scenario of development. In: Lindburg DG (Eds) The Macaques: Studies in Ecology, Behavior and Evolution. New York: Van Nostrand Reinhold, 10–30.
    Edgar RC. 2004. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research, 32(5): 1792−1797. doi: 10.1093/nar/gkh340
    Evans BJ, Gansauge MT, Tocheri MW, Schillaci MA, Sutikna T, Jatmiko, et al. 2020. Mitogenomics of macaques (Macaca) across Wallace's Line in the context of modern human dispersals. Journal of Human Evolution, 146: 102852. doi: 10.1016/j.jhevol.2020.102852
    Fa JE. 1989. The genus Macaca: a review of taxonomy and evolution. Mammal Review, 19(2): 45−81. doi: 10.1111/j.1365-2907.1989.tb00401.x
    Fan PF, Liu Y, Zhang ZC, Zhao C, Li C, Liu WL, et al. 2017. Phylogenetic position of the white-cheeked macaque (Macaca leucogenys), a newly described primate from southeastern Tibet. Molecular Phylogenetics and Evolution, 107: 80−89. doi: 10.1016/j.ympev.2016.10.012
    Fooden J. 1976. Provisional classification and key to living species of macaques (Primates: Macaca). Folia Primatologica, 25(2–3): 225−236.
    Fooden J. 1979. Taxonomy and evolution of the Sinica group of macaques: I. Species and subspecies accounts of Macaca sinica. Primates, 20(1): 109−140. doi: 10.1007/BF02373832
    Groves CP. 2001. Primate Taxonomy. Washington DC: Smithsonian Institution Press.
    Hayasaka K, Fujii K, Horai S. 1996. Molecular phylogeny of Macaques: implications of nucleotide sequences from an 896-base pair region of mitochondrial DNA. Molecular Biology and Evolution, 13(7): 1044−1053. doi: 10.1093/oxfordjournals.molbev.a025655
    Hayasaka K, Ishida T, Horai S. 1991. Heteroplasmy and polymorphism in the major noncoding region of Mitochondrial DNA in Japanese monkeys: association with tandemly repeated sequences. Molecular Biology and Evolution, 8(4): 399−415.
    Hebert PDN, Cywinska A, Ball SL, deWaard JR. 2003. Biological identifications through DNA barcodes. Proceedings of Royal Society Biological Sciences: Biological Sciences, 270(1512): 313−321. doi: 10.1098/rspb.2002.2218
    Hillis DM, Bull JJ. 1993. An empirical test of bootstrapping as a method for assessing confidence in phylogenetic analysis. Systematic Biology, 42(2): 182−192. doi: 10.1093/sysbio/42.2.182
    Khanal L, Chalise MK, He K, Acharya BK, Kawamoto Y, Jiang XL. 2018a. Mitochondrial DNA analyses and ecological niche modeling reveal post-LGM expansion of the Assam macaque (Macaca assamensis) in the foothills of Nepal Himalaya. American Journal of Primatology, 80(3): e22748. doi: 10.1002/ajp.22748
    Khanal L, Chalise MK, Jiang XL. 2018b. Inconsistency in phylogeny of sinica-group of macaques. In: Satellite International Symposium on Asian Primates-2018. Kathmandu: Nepal Biodiveristy Research Society, 48–49.
    Khanal L, Chalise MK, Jiang XL. 2019. Distribution of the threatened Assamese Macaque Macaca assamensis (Mammalia: Primates: Cercopithecidae) population in Nepal. Journal of Threatened Taxa, 11(1): 13047−13057. doi: 10.11609/jott.4623.11.1.13047-13057
    Khanal L, Chalise MK, Wan T, Jiang XL. 2018c. Riverine barrier effects on population genetic structure of the Hanuman langur (Semnopithecus entellus) in the Nepal Himalaya. BMC Evolutionary Biology, 18(1): 159. doi: 10.1186/s12862-018-1280-4
    Kim HS, Hirai H, Takenaka O. 1996. Molecular features of the TSPY gene of gibbons and Old World monkeys. Chromosome Research, 4(7): 500−506. doi: 10.1007/BF02261777
    Kimura M. 1980. A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. Journal of Molecular Evolution, 16(2): 111−120. doi: 10.1007/BF01731581
    Kumar S, Stecher G, Li M, Knyaz C, Tamura K. 2018. MEGA X: molecular Evolutionary Genetics Analysis across computing platforms. Molecular Biology and Evolution, 35(6): 1547−1549.
    Lanfear R, Calcott B, Ho SYW, Guindon S. 2012. Partitionfinder: combined selection of partitioning schemes and substitution models for phylogenetic analyses. Molecular Biology and Evolution, 29(6): 1695−1701. doi: 10.1093/molbev/mss020
    Li BG, He G, Guo ST, Hou R, Huang K, Zhang P, et al. 2020. Macaques in China: evolutionary dispersion and subsequent development. American Journal of Primatology, 82(7): e23142.
    Li C, Zhao C, Fan PF. 2015. White-cheeked macaque (Macaca leucogenys): a new macaque species from Medog, southeastern Tibet. American Journal of Primatology, 77(7): 753−766. doi: 10.1002/ajp.22394
    Li J, Han K, Xing JC, Kim HS, Rogers J, Ryder OA, et al. 2009. Phylogeny of the macaques (Cercopithecidae: Macaca) based on Alu elements. Gene, 448(2): 242−249.
    Li QQ, Zhang YP. 2004. A molecular phylogeny of Macaca based on mitochondrial control region sequences. Zoological Research, 25(5): 385−390.
    Li QQ, Zhang YP. 2005. Phylogenetic relationships of the macaques (Cercopithecidae: Macaca), inferred from mitochondrial DNA sequences. Biochemical Genetics, 43(7–8): 375−386.
    Liedigk R, Kolleck J, Böker KO, Meijaard E, Md-Zain BM, Abdul-Latiff MAB, et al. 2015. Mitogenomic phylogeny of the common long-tailed macaque (Macaca fascicularis fascicularis). BMC Genomics, 16(1): 222.
    Matsudaira K, Hamada Y, Bunlungsup S, Ishida T, San AM, Malaivijitnond S. 2018. Whole mitochondrial genomic and Y-chromosomal phylogenies of Burmese long-tailed macaque (Macaca fascicularis aurea) suggest ancient hybridization between fascicularis and sinica species groups. Journal of Heredity, 109(4): 360−371.
    Melnick DJ, Hoelzer GA. 1993. What is mtDNA good for in the study of primate evolution?. Evolutionary Anthropology, 2(1): 2−10.
    Minge C, Berghänel A, Schülke O, Ostner J. 2016. Patterns and consequences of male-infant relationships in wild assamese macaques (Macaca assamensis). International Journal of Primatology, 37(3): 350−370.
    Molur S, Brandon-Jones D, Dittus W, Eudey A, Kumar A, Singh M, et al. 2003. Status of South Asian primates: conservation assessment and management plan (C.A.M. P.). Coimbatore, India: Zoo Outreach Organization /CBSG-South Asia.
    Morales JC, Melnick DJ. 1998. Phylogenetic relationships of the macaques (Cercopithecidae: Macaca), as revealed by high resolution restriction site mapping of mitochondrial ribosomal genes. Journal of Human Evolution, 34(1): 1−23. doi: 10.1006/jhev.1997.0171
    Moritz C. 1994. Defining ‘Evolutionarily Significant Units’ for conservation. Trends in Ecology & Evolution, 9(10): 373−375.
    Nei M, Kumar S. 2000. Molecular Evolution and Phylogenetics. New York: Oxford University Press, 333.
    Page SL, Chiu CH, Goodman M. 1999. Molecular phylogeny of old world monkeys (Cercopithecidae) as inferred from γ-globin DNA sequences. Molecular Phylogenetics and Evolution, 13(2): 348−359. doi: 10.1006/mpev.1999.0653
    Rambaut A, Suchard M, Xie D, Drummond A. 2014(2020-04-25). Tracer v1.6. – Computer program and documentation. https://www.scirp.org/reference/referencespapers.aspx?referenceid=2565011.
    Roos C, Kothe M, Alba DM, Delson E, Zinner D. 2019. The radiation of macaques out of Africa: Evidence from mitogenome divergence times and the fossil record. Journal of Human Evolution, 133: 114−132. doi: 10.1016/j.jhevol.2019.05.017
    Sarania B, Devi A, Kumar A, Sarma K, Gupta AK. 2017. Predictive distribution modeling and population status of the endangered Macaca munzala in Arunachal Pradesh, India. American Journal of Primatology, 79(2): e22592. doi: 10.1002/ajp.22592
    Sinha A, Datta A, Madhusudan MD, Mishra C. 2005. Macaca munzala: a new species from western Arunachal Pradesh, Northeastern India. International Journal of Primatology, 26(4): 977−989. doi: 10.1007/s10764-005-5333-3
    Stamatakis A. 2014. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics, 30(9): 1312−1313. doi: 10.1093/bioinformatics/btu033
    Suchard MA, Lemey P, Baele G, Ayres DL, Drummond AJ, Rambaut A. 2018. Bayesian phylogenetic and phylodynamic data integration using BEAST 1.10. Virus Evolution, 4(1): vey016.
    Thierry B, Singh M, Kaumanns W. 2004. Why macaque societies?. In: Thierry B, Singh M, Kaumanns W. Macaque Societies – A Model for the Study of Social Organization. Cambridge: Cambridge University Press.
    Thompson JD, Higgins DG, Gibson TJ. 1994. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Research, 22(22): 4673−4680.
    Tosi AJ, Morales JC, Melnick DJ. 2000. Comparison of Y chromosome and mtDNA phylogenies leads to unique inferences of macaque evolutionary history. Molecular Phylogenetics and Evolution, 17(2): 133−144. doi: 10.1006/mpev.2000.0834
    Tosi AJ, Morales JC, Melnick DJ. 2003. Paternal, maternal, and biparental molecular markers provide unique windows onto the evolutionary history of macaque monkeys. Evolution, 57(6): 1419−1435. doi: 10.1111/j.0014-3820.2003.tb00349.x
    Wada K. 2005. The distribution pattern of rhesus and Assamese monkeys in Nepal. Primates, 46(2): 115−119.
    Whitfield LS, Lovell-Badge R, Goodfellow PN. 1993. Rapid sequence evolution of the mammalian sex-determining gene SRY. Nature, 364(6439): 713−715.
    Zhou QH, Wei H, Huang ZH, Huang CM. 2011. Diet of the Assamese macaque Macaca assamensis in limestone habitats of Nonggang, China. Current Zoology, 57(1): 18−25.
    Ziegler T, Abegg C, Meijaard E, Perwitasari-Farajallah D, Walter L, Hodges JK, et al. 2007. Molecular phylogeny and evolutionary history of Southeast Asian macaques forming the M. silenus group. Molecular Phylogenetics and Evolution, 42(3): 807−816. doi: 10.1016/j.ympev.2006.11.015
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