Molecular Biology Reports

, Volume 40, Issue 4, pp 3033–3041 | Cite as

Genetic diversity and population structure in wild Sichuan rhesus macaques

  • Di Yan Li
  • Huai Liang Xu
  • Jessica Satkoski Trask
  • Qing Zhu
  • An Chun Cheng
  • David Glenn Smith
  • Debbie George
  • Long Zhang


Because wild rhesus macaque (Macaca mulatta) populations have suffered major declines, there is a growing need to characterize their genetic and population structure in order to protect the genetic integrity of this species. In this study, we genotyped a sample comprising 120 wild rhesus macaques from six sites in Sichuan Province for 30 nuclear microsatellite (STR) loci using an ABI 3130xl genetic analyzer. Bayesian analyses and PCA clearly differentiated monkeys from Heishui from those at other sites. The samples from all six sites exhibited high gene diversity suggesting that the Sichuan wild rhesus macaque populations are not threatened by a lack of genetic diversity. Deviation from Hardy–Weinberg equilibrium was more frequent in the Danba and Heishui populations. This may be due to the more fragmented habitat and less disturbance by humans in this area that foster greater subpopulation structuring than occurs in eastern China. We suggest that this population subdivision is the result of both long-term geographic barriers and human activity.


DNA typing Short tandem repeat Rhesus macaques population structure 



This work was supported by the National Natural Science Foundation of China (No. 30970383), National Institutes of Health grants R24RR05090 and R24RR025871 to DGS.

Supplementary material

11033_2012_2377_MOESM1_ESM.xlsx (26 kb)
Supplementary material 1 (XLSX 25 kb)
11033_2012_2377_MOESM2_ESM.xlsx (13 kb)
Supplementary material 2 (XLSX 13 kb)
11033_2012_2377_MOESM3_ESM.xlsx (14 kb)
Supplementary material 3 (XLSX 14 kb)


  1. 1.
    VandeBerg JL, Williams-Blangero S (1997) Advantages and limitations of nonhuman primates as animal models in genetic research on complex diseases. J Med Primatol 26:113–119PubMedCrossRefGoogle Scholar
  2. 2.
    Williams-Blangero S (1993) Research-oriented genetic management of nonhuman primate colonies. Lab Anim Sci 43:535PubMedGoogle Scholar
  3. 3.
    Smith DG (2005) Genetic characterization of Indian-origin and Chinese-origin rhesus macaques (Macaca mulatta). Comp Med 55:227–230PubMedGoogle Scholar
  4. 4.
    Satkoski JA, Malhi R, Kanthaswamy S, Tito R, Malladi V, Smith DG (2008) Pyrosequencing as a method for SNP identification in the rhesus macaque (Macaca mulatta). BMC Genomics 9:256PubMedCrossRefGoogle Scholar
  5. 5.
    Trask JS, Garnica WT, Kanthaswamy S, Malhi RS, Smith DG (2011) 4040 SNPs for genomic analysis in the rhesus macaque (Macaca mulatta). Genomics 98:352–358PubMedCrossRefGoogle Scholar
  6. 6.
    Goodwin WJ, Augustine J (1975) The Primate Research Centers Program of the National Institutes of Health. Fed Proc 34:1641–1642PubMedGoogle Scholar
  7. 7.
    Xu HL, Wang YT, Cheng AC, Yao YF, Ni QY, Zeng W, Bi FJ, Yang ZX, Chen XY (2010) Polymorphism of MHC-DPB1 gene exon 2 in rhesus macaques (Macaca mulatta). Yi Chuan 32:588–598PubMedCrossRefGoogle Scholar
  8. 8.
    Joag SV, Stephens EB, Adams RJ, Foresman L, Narayan O (1994) Pathogenesis of SIVmac infection in Chinese and Indian rhesus macaques: effects of splenectomy on virus burden. Virology 200:436–446PubMedCrossRefGoogle Scholar
  9. 9.
    Ling B, Veazey RS, Penedo C, Xu K, Lifson JD, Marx PA (2002) Longitudinal follow up of SIVmac pathogenesis in rhesus macaques of Chinese origin: emergence of B cell lymphoma. J Med Primatol 31:154–163PubMedCrossRefGoogle Scholar
  10. 10.
    Melnick DJ, Hoelzer GA, Absher R, Ashley MV (1993) mtDNA diversity in rhesus monkeys reveals overestimates of divergence time and paraphyly with neighboring species. Mol Biol Evol 10:282–295PubMedGoogle Scholar
  11. 11.
    Fooden J (2000) Systematic review of the rhesus macaque, Macaca mulatta (Zimmermann, 1780). Fieldiana Zool 96:1–180Google Scholar
  12. 12.
    Smith DG, McDonough J (2005) Mitochondrial DNA variation in Chinese and Indian rhesus macaques (Macaca mulatta). Am J Primatol 65:1–25PubMedCrossRefGoogle Scholar
  13. 13.
    Smith DG, McDonough JW, George DA (2007) Mitochondrial DNA variation within and among regional populations of longtail macaques (Macaca fascicularis) in relation to other species of the fascicularis group of macaques. Am J Primatol 69:182–198PubMedCrossRefGoogle Scholar
  14. 14.
    Ferguson B, Street SL, Wright H, Pearson C, Jia Y, Thompson SL, Allibone P, Dubay CJ, Spindel E, Norgren RB Jr (2007) Single nucleotide polymorphisms (SNPs) distinguish Indian-origin and Chinese-origin rhesus macaques (Macaca mulatta). BMC Genomics 8:43PubMedCrossRefGoogle Scholar
  15. 15.
    Zhang Y, Chen L, Qu W, Coggins C (2002) The primates of China: biogeography and conservation status. Asian Primates 8:20–22Google Scholar
  16. 16.
    Li DY, Xu HL, Smith DG, Cheng 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 73:883–895PubMedCrossRefGoogle Scholar
  17. 17.
    Li DY, Yao YF, Cheng AC, Xu HL, Ni QY, Zeng W, Bi FJ, Yang ZX, Chen XY (2012) Genetic differentiation and systematic evolution of Sichuan rhesus macaques. Adv Mater Res 343:683–689CrossRefGoogle Scholar
  18. 18.
    Doxiadis GGM, Otting N, Groot NG, Groot N, Rouweler AJM, Noort R, Verschoor EJ, Bontjer I, Bontrop RE (2003) Evolutionary stability of MHC class II haplotypes in diverse rhesus macaque populations. Immunogenetics 55:540–551PubMedCrossRefGoogle Scholar
  19. 19.
    Southwood S, Solomon C, Hoof I, Rudersdorf R, Sidney J, Peters B, Wahl A, Hawkins O, Hildebrand W, Mothe BR, Sette A (2011) Functional analysis of frequently expressed Chinese rhesus macaque MHC class I molecules Mamu-A1*02601 and Mamu-B*08301 reveals HLA-A2 and HLA-A3 supertypic specificities. Immunogenetics 63:275–290PubMedCrossRefGoogle Scholar
  20. 20.
    Viray J, Rolfs B, Smith DG (2001) Comparison of the frequencies of major histocompatibility (MHC) class-II DQA1 and DQB1 alleles in Indian and Chinese rhesus macaques (Macaca mulatta). Comp Med 51:555–561PubMedGoogle Scholar
  21. 21.
    Trask JS, Malhi RS, Kanthaswamy S, Johnson J, Garnica WT, Malladi VS, Smith DG (2011) The effect of SNP discovery method and sample size on estimation of population genetic data for Chinese and Indian rhesus macaques (Macaca mulatta). Primates 52:129–138PubMedCrossRefGoogle Scholar
  22. 22.
    Smith DG (1994) Genetic heterogeneity in five captive specific pathogen-free groups of rhesus macaques. Lab Anim Sci 44:200–210PubMedGoogle Scholar
  23. 23.
    Butler JM, Buel E, Crivellente F, McCord BR (2004) Forensic DNA typing by capillary electrophoresis using the ABI Prism 310 and 3100 genetic analyzers for STR analysis. Electrophoresis 25:1397–1412PubMedCrossRefGoogle Scholar
  24. 24.
    Malhi RS, Trask JS, Shattuck M, Johnson J, Chakraborty D, Kanthaswamy S, Ramakrishnan U, Smith DG (2011) Genotyping single nucleotide polymorphisms (SNPs) across species in Old World Monkeys. Am J Primatol 73:1031–1040PubMedGoogle Scholar
  25. 25.
    Morin PA, Kanthaswamy S, Smith DG (1997) Simple sequence repeat (SSR) polymorphisms for colony management and population genetics in rhesus macaques (Macaca mulatta). Am J Primatol 42:199–213PubMedCrossRefGoogle Scholar
  26. 26.
    Smith DG, George DA, Kanthaswamy S, McDonough JW (2006) Identification of country of origin and admixture between Indian and Chinese rhesus macaques. Int J Primatol 27:881–898CrossRefGoogle Scholar
  27. 27.
    Kanthaswamy S, von Dollen A, Kurushima JD, Alminas O, Rogers J, Ferguson B, Lerche NW, Allen PC, Smith DG (2006) Microsatellite markers for standardized genetic management of captive colonies of rhesus macaques (Macaca mulatta). Am J Primatol 68:73–95PubMedCrossRefGoogle Scholar
  28. 28.
    Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press, New YorkGoogle Scholar
  29. 29.
    Raymond M, Rousset F (1995) GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. J Hered 86:248–249Google Scholar
  30. 30.
    Weir B, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:1358–1370CrossRefGoogle Scholar
  31. 31.
    Slatkin M (1985) Gene flow in natural populations. Annu Rev Ecol Syst 16:393–430CrossRefGoogle Scholar
  32. 32.
    Jombart T, Devillard S, Dufour A, Pontier D (2008) Revealing cryptic spatial patterns in genetic variability by a new multivariate method. Heredity 101:92–103PubMedCrossRefGoogle Scholar
  33. 33.
    Jombart T (2008) adegenet: a R package for the multivariate analysis of genetic markers. Bioinformatics 24:1403–1405PubMedCrossRefGoogle Scholar
  34. 34.
    Team R (2010) R: a language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
  35. 35.
    Cavalli-Sforza LL, Menozzi P, Piazza A (1994) The history and geography of human genes. Princeton University Press, PrincetonGoogle Scholar
  36. 36.
    Rutledge L, Garroway C, Loveless K, Patterson B (2010) Genetic differentiation of eastern wolves in Algonquin Park despite bridging gene flow between coyotes and grey wolves. Heredity 105:520–531PubMedCrossRefGoogle Scholar
  37. 37.
    Cliff AD, Ord JK (1981) Spatial processes: models & applications. Pion, LondonGoogle Scholar
  38. 38.
    Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959PubMedGoogle Scholar
  39. 39.
    Falush D, Stephens M, Pritchard JK (2003) Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics 164:1567–1587PubMedGoogle Scholar
  40. 40.
    Hedrick PW (2005) A standardized genetic differentiation measure. Evolution 59:1633–1638PubMedGoogle Scholar
  41. 41.
    Goodman DSG (1986) Centre and province in the People’s Republic of China: Sichuan and Guizhou, 1955–1965. Cambridge University Press, CambridgeGoogle Scholar
  42. 42.
    Yong L, Allen PA, Densmore AL, Qiang X (2003) Evolution of the Longmen Shan foreland basin (western Sichuan, China) during the Late Triassic Indosinian orogeny. Basin Res 15:117–138CrossRefGoogle Scholar
  43. 43.
    Banuri T, Marglin FA (1993) Who will save the forests? Knowledge, power and environmental destruction. Zed Books, LondonGoogle Scholar
  44. 44.
    Satkoski JS, George D, Smith DG, Kanthaswamy S (2008) Genetic characterization of wild and captive rhesus macaques in China. J Med Primatol 37:67–80PubMedCrossRefGoogle Scholar
  45. 45.
    Davenport A (1877) Report upon the trading capabilities of the country traversed by the Yunnan Mission. Harrison and Sons, LondonGoogle Scholar
  46. 46.
    Communique of the National Bureau of Statistics of Peoples Republic of China on Major Figures of the 2010 Population Census (No. 1). National Bureau of Statistics of China. April 28, 2011Google Scholar
  47. 47.
    Pu FD (2000) The present conditions of ecology and bio-diversity protection at upstreams of Min River. Resour Sci 22:83–85Google Scholar
  48. 48.
    Frankham R, Briscoe DA, Ballou JD (2002) Introduction to conservation genetics. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  49. 49.
    Nei M, Kumar S (2000) Molecular evolution and phylogenetics. Oxford University Press, OxfordGoogle Scholar
  50. 50.
    Xu HL, Li DY, Cheng AC, Yao YF, Ni QY, Zeng W, Bi FJ, Yang ZX, Chen XY (2010) Population genetic diversity and structure of Rhesus macaque (Macaca mulatta) in Sichuan Province based on mtDNA control region sequences. Acta Theriol Sinica 30:247–255Google Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2012

Authors and Affiliations

  • Di Yan Li
    • 1
    • 2
  • Huai Liang Xu
    • 1
  • Jessica Satkoski Trask
    • 2
  • Qing Zhu
    • 1
  • An Chun Cheng
    • 3
  • David Glenn Smith
    • 2
  • Debbie George
    • 2
  • Long Zhang
    • 1
  1. 1.College of Animal Science and Technology, Sichuan Agricultural UniversityYa’anPeople’s Republic of China
  2. 2.Department of Anthropology and California National Primate Research CenterUniversity of California, DavisDavisUSA
  3. 3.Key Laboratory of Animal Disease and Human Health of Sichuan ProvinceSichuan Agricultural UniversityYa’anChina

Personalised recommendations