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Genetic diversity of two Tibetan macaque (Macaca thibetana) populations from Guizhou and Yunnan in China based on mitochondrial DNA D-loop sequences

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Tibetan macaque (Macaca thibetana), an endangered species endemic to China, is categorized as a Category II species under the Chinese Wild Animal Protection Law and listed in Appendix II of the Convention on International Trade in Endangered Species. To further assess genetic diversity and population structure within this species, we sequenced 477 bp of mitochondrial DNA control region in 30 Tibetan macaques from the Guizhou (GZ) and Yunnan (YN) of China and conducted population genetic analysis, along with 15 previously described haplotype sequences representing 55 individuals from Sichuan (SC) and Anhui (AH). 87 polymorphic sites were detected in the alignment of 45 sequences and defined 22 haplotypes, of which 9 were newly identified. Haplotype diversity (h), nucleotide diversity (π) and average number of nucleotide differences (K) is 0.911 ± 0.015, 0.06090 ± 0.00126 and 28.32, respectively, indicating higher genetic diversity in the whole Tibetan macaque population. Analysis of molecular variance (AMOVA) partitioned the total variation into 83.63 % among populations and 16.37 % within populations, revealing that variations occured among populations mainly. Further analysis demonstrated that significant genetic differentiation (Fst = 0.83628, P < 0.01) and poor gene flow (Nm < 1) had occurred among these four populations. On the phylogenetic tree and haplotype network plot, 22 haplotypes cluster together according to their geographical origins, exhibiting an obvious phylogeographic pattern. We speculate that the significant genetic differentiation among these macaque populations might result from long-term geographic barrier and human activity. In particular, Yangtze River probably play a vital role in population differentiation of Tibetan macaques.

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References

  • Avise JC (2000) Phylogeography: the history and formation of species. Harvard University Press, Cambridge

    Google Scholar 

  • Avise JC, Arnold J, Ball RM, Bermingham E, Lamb T, Neigel JE, Reeb CA, Saunders NC (1987) Intraspecific phylogeography: the mitochondrial DNA bridge between population genetics and systematics. Annu Rev Ecol Sys 18:489–522

    Google Scholar 

  • Bandelt HJ, Forster P, Rohl A (1999) Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol 16:37–48

    Article  PubMed  CAS  Google Scholar 

  • Billington N, Hebert PDN (1991) Mitochondrial DNA diversity in fishes and its implications for introductions. Can J Fish Aquat Sci 48(S1):80–94

    Article  Google Scholar 

  • Bossart J, Pashley Prowell D (1998) Genetic estimates of population structure and gene flow: limitations, lessons and new directions. Trends Ecol Evol 13:202–206

    Article  PubMed  CAS  Google Scholar 

  • Brown WM (1985) The mitochondrial genome of animals. In: MacIntyre RJ (ed) Molecular evolutionary genetics. Plenum, New York, pp 95–130

    Chapter  Google Scholar 

  • Brown WM, George M, Wilson AC (1979) Rapid evolution of animal mitochondrial DNA. Proc Natl Acad Sci USA 76:1967–1971

    Article  PubMed  CAS  Google Scholar 

  • Brown J, Beckenbach A, Smith M (1992) Mitochondrial DNA length variation and heteroplasmy in populations of white sturgeon (Acipenser transmontanus). Genetics 132:221–228

    PubMed  CAS  Google Scholar 

  • Cassens I, Van Waerebeek K, Best PB, Crespo EA, Reyes J, Milinkovitch MC (2003) The phylogeography of dusky dolphins (Lagenorhynchus obscurus): a critical examination of network methods and rooting procedures. Mol Ecol 12:1781–1792

    Article  PubMed  CAS  Google Scholar 

  • De Campos Vaz AR, de Oliveira Borba TC, Brondani C, Rangel PH, de Oliveira Camargo GS, de Campos Telles MP, Filho JA, Brondani RP (2009) Genetic analysis of a local population of Oryza glumaepatula using SSR markers: implications for management and conservation programs. Genetica 137:221–231

    Article  PubMed  Google Scholar 

  • Excoffier L, Smouse PE, Quattro JM (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131:479–491

    PubMed  CAS  Google Scholar 

  • Excoffier L, Laval G, Schneider S (2005) Arlequin (version 3.0): an integrated software package for population genetics data analysis. Evol Bioinform Online 1:47–50

    CAS  Google Scholar 

  • Fu YX (1997) Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147:915–925

    PubMed  CAS  Google Scholar 

  • Giles RE, Blanc H, Cann HM, Wallace DC (1980) Maternal inheritance of human mitochondrial DNA. Proc Natl Acad Sci USA 77:6715

    Article  PubMed  CAS  Google Scholar 

  • Groves CP, Wilson DE, Reeder DM (2005) Order Primates. Mammal species of the world: a taxonomic and geographic reference, vol 1, 3rd edn. Johns Hopkins University Press, Maryland, pp 111–184

    Google Scholar 

  • Hayaishi S, Kawamoto Y (2006) Low genetic diversity and biased distribution of mitochondrial DNA haplotypes in the Japanese macaque (Macaca fuscata yakui) on Yakushima Island. Primates 47:158–164

    Article  PubMed  Google Scholar 

  • Hayasaka K, Horai S, Shotake T, Nozawa K, Matsunaga E (1986) Mitochondrial DNA polymorphism in Japanese monkeys, Macaca fuscata. Jpn J Genet 61:345–359

    Article  Google Scholar 

  • 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. Mol Biol Evol 8:399–415

    PubMed  CAS  Google Scholar 

  • Hutchison CA, Newbold JE, Potter SS, Edgell MH (1974) Maternal inheritance of mammalian mitochondrial DNA. Nature 251:536–538

    Article  PubMed  CAS  Google Scholar 

  • Jensen-seaman M, Kidd K (2001) Mitochondrial DNA variation and biogeography of eastern gorillas. Mol Ecol 10:2241–2247

    Article  PubMed  CAS  Google Scholar 

  • Jiang X, Wang Y (1996) Taxonomy and distribution of Tibetan macaque. Zool Res 17:361–369

    Google Scholar 

  • Kawamoto Y, Shotake T, Nozawa K, Kawamoto S, Tomari K, Kawai S, Shirai K, Morimitsu Y, Takagi N, Akaza H (2007) Postglacial population expansion of Japanese macaques (Macaca fuscata) inferred from mitochondrial DNA phylogeography. Primates 48:27–40

    Article  PubMed  Google Scholar 

  • Li QQ, Zhang YP (2004) A molecular phylogeny of Macaca based on mitochondrial control region sequences. Zool Res 25:385–390

    Google Scholar 

  • Li DM, Fan LQ, Ran JH, Yin HL, Wang HX, Wu SB, Yue BS (2008) Genetic diversity analysis of Macaca thibetana based on mitochondrial DNA control region sequences. Mitochon DNA 19:446–452

    CAS  Google Scholar 

  • Li DY, Xu HL, Smith DG, Chen AC, Trask JS, Zhu Q, Yao YF, Du DD, Ni QY (2011) Phylogenetic analysis of Chinese rhesus macaques (Macaca mulatta) based on mitochondrial control region sequences. Am J Primatol 73:883–895

    Article  PubMed  Google Scholar 

  • Liu Y, Li JH, Zhao JY (2006) Sequence variation of mitochondrial DNA control region and population genetic diversity of Tibetan macaques Macaca thibetana in the Huangshan Mountain. Acta Zool Sin 52:724–730

    CAS  Google Scholar 

  • Melnick DJ, Hoelzer GA (1993) What is mtDNA good for in the study of primate evolution? Evol Anthropol 2:2–10

    Article  Google Scholar 

  • Millar C, Libby W (1991) Strategies for conserving clinal, ccotypic, and disjunct population diversity in widespread species. In: Fald DA, Holsinger KE (eds) Genetics and Conservation of Rare Plants. Oxford University Press, New York, pp 149–170

    Google Scholar 

  • Modolo L, Salzburger W, Martin RD (2005) Phylogeography of Barbary macaques (Macaca sylvanus) and the origin of the Gibraltar colony. Proc Natl Acad Sci USA 102:7392–7397

    Article  PubMed  CAS  Google Scholar 

  • Nei M, Maruyama T, Chakraborty R (1975) The bottleneck effect and genetic variability. Evolution 29:1–10

    Article  Google Scholar 

  • Pan HJ, Shi FL, Chang ZF, Xiang ZF, Sun TT, Liu ZJ, Li M (2011) Mitochondrial DNA variation analysis suggests extreme low genetic diversity in Guizhou snub-nosed monkeys (Rhinopithecus brelichi). Chin Sci Bull 56:2541–2544

    Article  CAS  Google Scholar 

  • Parsons TJ, Muniec DS, Sullivan K, Woodyatt N, Alliston-Greiner R, Wilson MR, Berry DL, Holland KA, Weedn VW, Gill P (1997) A high observed substitution rate in the human mitochondrial DNA control region. Nat Genet 15:363–368

    Article  PubMed  CAS  Google Scholar 

  • Posada D, Buckley TR (2004) Model selection and model averaging in phylogenetics: advantages of Akaike information criterion and Bayesian approaches over likelihood ratio tests. Syst Biol 53:793–808

    Article  PubMed  Google Scholar 

  • Rogers AR, Harpending H (1992) Population growth makes waves in the distribution of pair wise genetic differences. Mol Biol Evol 9:552–569

    PubMed  CAS  Google Scholar 

  • Rozas J, Sanchez-DelBarrio JC, Messeguer X, Rozas R (2003) DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19:2496–2497

    Article  PubMed  CAS  Google Scholar 

  • Shiina T, Tanaka K, Katsuyama Y, Otabe K, Sakamoto K, Kurata M, Nomura M, Yamanaka H, Nakagawa H, Inoko H (2010) Mitochondrial DNA Diversity among Three Subpopulations of Cynomolgus Macaques (Macaca fascicularis) Originating from the Indochinese Region. Exp Anim 59:567–578

    Article  PubMed  Google Scholar 

  • Slatkin M (1987) Gene flow and the geographic structure of natural populations. Science 236(4803):787

    Article  PubMed  CAS  Google Scholar 

  • Smith DG, McDonough JW (2005) Mitochondrial DNA variation in Chinese and Indian rhesus macaques (Macaca mulatta). Am J Primatol 65:1–25

    Article  PubMed  CAS  Google Scholar 

  • Swofford DL (2002) PAUP*: Phylogenetic analysis using parsimony (and other methods). Version 4.0b10. Sinauer, Sunderland

    Google Scholar 

  • Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585–595

    PubMed  CAS  Google Scholar 

  • Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739

    Article  PubMed  CAS  Google Scholar 

  • Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882

    Article  PubMed  CAS  Google Scholar 

  • Wang S (1998) China red data book of endangered animals. In: Wang S (ed) Mammalia. Science, Beijing, pp 48–50

    Google Scholar 

  • Wright S (1949) The genetical structure of populations. Ann Hum Genet 15:323–354

    Article  Google Scholar 

  • Wright S (1965) The interpretation of population structure by F-statistics with special regard to systems of mating. Evolution 19:395–420

    Article  Google Scholar 

  • Yasukochi Y, Nishida S, Han SH, Kurosaki T, Yoneda M, Koike H (2009) Genetic structure of the Asiatic black bear in Japan using mitochondrial DNA analysis. J Hered 100:297–308

    Article  PubMed  CAS  Google Scholar 

  • Zhu L, Zhang S, Gu X, Wei F (2011) Significant genetic boundaries and spatial dynamics of giant pandas occupying fragmented habitat across southwest China. Mol Ecol 20:1122–1132

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

We thank the Forestry Bureau of Yongshan County in Yunnan Province and Sichuan Mamize Nature Reserve for their suppports, and Anjun Luo, Xifa Chen and Binbin Sun for their field assistance. This work was supported by the National Natural Science Foundation of China (No. 30970383), Natural Science Foundation of Educational Commission of Sichuan Province of China (No. 08ZA076) and Program for Changjiang Scholars and Innovative Research Team in University (No. IRTO848).

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Authors and Affiliations

  1. College of Animal Science and Technology, Sichuan Agricultural University, Ya’an, 625014, China

    Li-Jing Zhong, Ming-Wang Zhang, Yong-Fang Yao, Qing-Yong Ni & Huai-Liang Xu

  2. Xishui National Nature Reserve, Xishui, 564600, China

    Jun Mu & Chong-Qing Li

  3. Key Laboratory of Animal Disease and Human Health of Sichuan Province, Sichuan Agricultural University, Ya’an, 625014, China

    Huai-Liang Xu

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  1. Li-Jing Zhong
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Correspondence to Huai-Liang Xu.

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L.-J. Zhong, M.-W. Zhang and Y.-F. Yao contributed equally to this study.

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Zhong, LJ., Zhang, MW., Yao, YF. et al. Genetic diversity of two Tibetan macaque (Macaca thibetana) populations from Guizhou and Yunnan in China based on mitochondrial DNA D-loop sequences. Genes Genom 35, 205–214 (2013). https://doi.org/10.1007/s13258-012-0048-2

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