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Primates

, Volume 55, Issue 2, pp 189–197 | Cite as

Preliminary study of the genetic diversity of eastern Assamese macaques (Macaca assamensis assamensis) in Thailand based on mitochondrial DNA and microsatellite markers

  • Manakorn Sukmak
  • Suchinda Malaivijitnond
  • Oliver Schülke
  • Julia Ostner
  • Yuzuru Hamada
  • Worawidh WajjwalkuEmail author
Original Article

Abstract

Human overpopulation, deforestation, invasion of agricultural areas, and livestock are the primary causes for population fragmentation of wildlife. The distribution range of species of the genus Macaca is constantly decreasing and becoming increasingly fragmented due to forest deterioration. Assamese macaques (M. assamensis) are classified as near threatened in the International Union for Conservation of Nature (IUCN) Red List of Threatened Animals (2008) and have been declared a protected wildlife animal according to Wildlife Preservation and Protection Act, B.E.2535 (1992) of Thailand. As studies of the population history and genetic diversity of Assamese macaques in Thailand are currently lacking, we aimed at a first investigation of their genetic diversity based on mitochondrial DNA [hypervariable regions 1 and 2 (HV1, HV2) and cytochrome B (CYTB) regions], as well as 15 microsatellite markers of five sampling sites distributed across Thailand. Our results indicate that Assamese macaques in Thailand are diverse, with eight maternal haplotypes and a low inbreeding coefficient in the Phu Khieo Wildlife Sanctuary (PKWS) population. Moreover, our phylogenetic and median-joining network analysis based on mitochondrial (mt)DNA suggests a population distribution in accordance with the evolutionary scenario proposed for M. sinica. Today, the population of Assamese macaques is fragmented, and conservation strategies are needed to ensure the maintenance of genetic diversity of this primate species.

Keywords

Phylogenetic Median-joining network mtDNA Microsatellites Macaca assamensis 

Notes

Acknowledgments

We thank the National Research Council of Thailand (NRCT) and the Department of National Parks, Wildlife and Plant Conservation (DNP) for the permission to conduct this study and for all the support granted (permit 0004.3/3618, 0002.3/2647, 0907.1/1092). We are grateful to Kitti Kreetiyutanont, Mongkul Kumsuk, Kanjana Nitaya, and Jarupol Prabnasuk (Phu Khieo Wildlife Sanctuary) for their cooperation. We thank all Team Macaque members at Phu Khieo Wildlife Sanctuary for help with sample collection. We thank Supakarn Kaewchot, Khajornpong Nakguea, all staff members from Mae Lao Wildlife Breeding Center and Chaing Rai Provincial Livestock Office for sample collection. We thank all staff from Primate Research Unit, Department of Biology, Faculty of Science, Chulalongkorn University and the 11th protected area regional office. We thank Benchapol Lorsunyaluck from Wildlife Unit, Kasetsart University Veterinary Teaching Hospital, Kampaeng Saen Campus and Private Zoo for helping us with sample collection. We are very grateful to Linda Vigilant and Jojo Bhagavatula who developed the genetic analyses for the samples collected at PKWS. This research was supported by the Max-Planck Society, the National Geographic Society, and the German Initiative of Excellence through funds to University of Göttingen, as well as the Center of Excellence on Agricultural Biotechnology, Science and Technology Postgraduate Education and Research Development Office, Office of Higher Education Commission, Ministry of Education (AG-BIO/PERDO-CHE); and we thank the Faculty of Veterinary Medicine, Kasetsart University, Thailand.

References

  1. Acevedo-Whitehouse K, Gulland F, Grieg D, Amos W (2003) Inbreeding: disease susceptibility in California sea lions. Nature 422:35CrossRefPubMedGoogle Scholar
  2. Arandjelovic M, Guschanski K, Schubert G, Harris TR, Thalmann O, Siedel H, Vigilant L (2009) Two-step multiplex polymerase chain reaction improves the speed and accuracy of genotyping using DNA from noninvasive and museum samples. Mol Ecol Resour 9:28–36CrossRefPubMedGoogle Scholar
  3. Bandelt HJ, Forster P, Röhl A (1999) Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol 16:37–48CrossRefPubMedGoogle Scholar
  4. Borries C, Larney E, Kreetiyutanont K, Koenig A (2002) The diurnal primate community in a dry evergreen forest in Phu Khieo Wildlife Sanctuary, Northeast Thailand. Nat Hist Bull Siam Soc 50:75–88Google Scholar
  5. 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. Mol Phyl Evol 44:838–849CrossRefGoogle Scholar
  6. Charpentier M, Hossaert-McKey M, Wickings EJ, Peignot P (2005a) Consequences of a one-male harem reproductive system and inbreeding in a captive group of Cercopithecus solatus. Int J Primatol 26:697–710CrossRefGoogle Scholar
  7. Charpentier M, Setchell JM, Prugnolle F, Knapp LA, Wickings EJ, Peignot P, Hossaert-McKey M (2005b) Genetic diversity and reproductive success in mandrills (Mandrillus sphinx). Proc Natl Acad Sci USA 102:16723–16728PubMedCentralCrossRefPubMedGoogle Scholar
  8. Charpentier M, Setchell JM, Prugnolle F, Wickings EJ, Peignot P, Balloux F, Hossaert-McKey M (2006) Life history correlates of inbreeding depression in mandrills (Mandrillus sphinx). Mol Ecol 15:21–28CrossRefPubMedGoogle Scholar
  9. Charpentier MJE, Widdig A, Alberts SC (2007) Inbreeding depression in non-human primates: a historical review of methods used and empirical data. Am J Primatol 69:1–17CrossRefGoogle Scholar
  10. Choudhury A (1998) Pere David’s Macaque discovered in India. The Rhino Foundation for Nat. NE India Newsletter 2:7Google Scholar
  11. Constable JL, Ashley MV, Goodall J, Pusey AE (2001) Noninvasive paternity assignment in Gombe chimpanzees. Mol Ecol 10:1279–1300CrossRefPubMedGoogle Scholar
  12. Delson E (1980) Fossil macaques, phyletic relationships and a scenario of deployment. In: Lindburg DG (ed) Macaques: studies in ecology, behavior and evolution. Van Nostrand Reinhold, New York, pp 10–30Google Scholar
  13. Espoti MD, De Vries S, Crimi M, Ghelli A, Patarnello T, Mayer A (1993) Mitochondrial cytochrome b: evolution and structure of the protein. Biocimica et Biophysica Acta 1143:243–271CrossRefGoogle Scholar
  14. Fa JE, Lindburg R (1996) Population management and viability of the Gibraltar Barbary macaques. In: Fa JE, Lindburg DG (eds) Evolution and ecology of macaques societies. Cambridge University Press, London, pp 235–262Google Scholar
  15. Fooden J (1982) Ecogeographic segregation of macaque species. Primates 23:574–579CrossRefGoogle Scholar
  16. Fooden J (1982a) Taxonomy and evolution of the Sinica group of macaques: 3. Species and subspecies accounts of Macaca assamensis. Fieldiana Zool new ser no. 10 Google Scholar
  17. Fooden J (1988) Taxonomy and evolution of the Sinica group of macaques: 6. Interspecific comparisons and synthesis. Fieldiana Zool new ser 45Google Scholar
  18. Fu YX (1997) Statistical tests of neutrality of mutations against population growth, hitchhiking, and background selection. Genetics 147:915–925PubMedCentralPubMedGoogle Scholar
  19. Goudet J (1995) FSTAT (Version 1.2): a computer program to calculate F-statistics. J Hered 86:485–486Google Scholar
  20. Goudet J (2001) FSTAT, a program to estimate and test gene diversities and fixation indices (Version 2.9.3). Available from http://www.unil.ch/izea/softwares/fstat.html
  21. Groves CP (2001) Primate taxonomy. Smithsonian Institution, Washington DCGoogle Scholar
  22. Kawamoto Y, Aimi M, Wangchuk T, Sherub (2006) Distribution of Assamese macaques (Macaca assamensis) in the inner Himalayan region of Bhutan and their mtDNA diversity. Primates 47:388–392CrossRefPubMedGoogle Scholar
  23. Kocher TD, Wilson AC (1989) Sequence evolution of mitochondrial DNA in humans and chimpanzees: control region and a protein-coding region. In: Osawa S, Honjo T (eds) Evolution of life: fossils, molecules and culture. Springer, Tokyo, pp 391–413Google Scholar
  24. Lawler RR, Richard AF, Riley MA (2003) Genetic population structure of the white sifaka (Propithecus verreauxi verreauxi) at Beza Mahafaly Special Reserve, southwest Madagascar (1992–2001). Mol Ecol 12:2307–2317CrossRefPubMedGoogle Scholar
  25. Li QQ, Zhang YP (2005) Phylogenetic relationships of the macaques (Cercopithecidae: Macaca), inferred from mitochondrial DNA sequences. Biochem Genet 43:375–386CrossRefPubMedGoogle Scholar
  26. Malaivijitnond S, Hamada Y (2008) Current situation and status of long-tailed macaques (Macaca fascicularis) in Thailand. Nat Hist J of Chulalongkorn Univ 8:185–204Google Scholar
  27. Malaivijitnond S, Varavudhi P (2002) The last possible troop of semi-wild rhesus macaque (Macaca mulatta) in Thailand. Nat Hist J of Chulalongkorn Univ 2:59–61Google Scholar
  28. Malaivijitnond S, Hamada Y, Varavudhi P, Takenaka O (2005) The current distribution and status of long-tailed macaques in Thailand. Nat Hist J of Chulalongkorn Univ Suppl 1:35–45Google Scholar
  29. Malaivijitnond S, Takenaka O, Kawamoto Y, Urasopon N, Hadi I, Hamada Y (2007) Anthropogenic macaque hybridization and genetic pollution of a threatened population. Nat Hist J of Chulalongkorn Univ 7:11–23Google Scholar
  30. Malaivijitnond S, Arsaithamkul V, Tanaka H, Pomchote P, Jaroenporn S, Suryobroto B, Hamada Y (2012) Boundary zone between northern and southern pig-tailed macaques and their morphological differences. Primates 53:377–389CrossRefPubMedGoogle Scholar
  31. Mandal A, Pant KP, Rout PK, Roy R (2004) Effects of inbreeding on lamb survival in a flock of Muzaffarnagari sheep. Asian Australas J Anim Sci 17:594–597Google Scholar
  32. Marshall TC, Slate J, Kruuk LEB, Pemberton JM (1998) Statistical confidence for likelihood-based paternity inference in natural populations. Mol Ecol 7:639–655CrossRefPubMedGoogle Scholar
  33. Nelson JE, Krawetz SA (1992) Purification of cloned and genomic DNA by guanidinethiocyanate/isobutyl alcohol fractionation. Anal Biochem 207:362–364CrossRefGoogle Scholar
  34. Noble SJ, Chesser RK, Ryder OA (1990) Inbreeding effects in captive populations of ruffed lemurs. Hum Evol 5:283–291CrossRefGoogle Scholar
  35. Nsubuga AM, Robbins MM, Roeder A, Morin PA, Boesch C, Vigilant L (2004) Factors affecting the amount of genomic DNA extracted from ape feces and the identification of an improved sample storage method. Mol Ecol 13:2089–2094CrossRefPubMedGoogle Scholar
  36. Pattanavibool A, Dearden P (2002) Fragmentation and wildlife in montane evergreen forests, northern Thailand. Biol Conserv 107:155–164CrossRefGoogle Scholar
  37. Pocock RI (1939) Primates and Carnivora (in Part), vol. 1. Mammalia. The Fauna of British India, including Ceylon and Burma. Taylor and Francis, London, p 463Google Scholar
  38. Pujolar JM, Maes GE, Vancoillie C, Volckaert FAM (2005) Growth rate correlates to individual heterozygosity in the European eel Anguilla anguilla L. Evolution 59:189–199PubMedGoogle Scholar
  39. Raymond M, Rousset F (1995) Genepop (version 1.2): population genetics software for exact tests and ecumenicism. J Hered 86:248–249Google Scholar
  40. Rozas J, Sánchez-DelBarrio JC, Messeguer X, Rozas R (2003) DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19:2496–2497CrossRefPubMedGoogle Scholar
  41. Schülke O, Bhagavatula J, Vigilant L, Ostner J (2010) Social bonds enhance reproductive success in male macaques. Curr Biol 20:2207–2210CrossRefPubMedGoogle Scholar
  42. Schülke O, Pesek D, Whitman BJ, Ostner J (2011) Ecology of Assamese macaques (Macaca assamensis) at Phu Khieo Wildlife Sanctuary, Thailand. J Wildl Thail 18:1–15Google Scholar
  43. Sinha A, Datta A, Madhusudan MD, Mishra C (2005) Macaca munzala: a new species from western Arunachal Pradesh, northeastern India. Int J Primatol 26:977–989CrossRefGoogle Scholar
  44. Storz JF, Ramakrishnan U, Alberts SC (2002) Genetic effective size of wild primate population: influence of current and historical demography. Evolution 56:817–829PubMedCrossRefGoogle Scholar
  45. Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599CrossRefPubMedGoogle Scholar
  46. Vigilant L, Pennington R, Harpending H, Kocher TD, Wilson AC (1989) Mitochondrial DNA sequences in single hairs from a southern African population. Proc Natl Acad Sci USA 86:9350–9354PubMedCentralCrossRefPubMedGoogle Scholar
  47. Woodruff DS (1990) Genetic and demography in the conservation of biodiversity. J Sci Soc Thailand 16:117–132CrossRefGoogle Scholar

Copyright information

© Japan Monkey Centre and Springer Japan 2013

Authors and Affiliations

  • Manakorn Sukmak
    • 1
    • 2
  • Suchinda Malaivijitnond
    • 3
  • Oliver Schülke
    • 4
  • Julia Ostner
    • 4
  • Yuzuru Hamada
    • 5
  • Worawidh Wajjwalku
    • 6
    Email author
  1. 1.Center for Agricultural BiotechnologyKasetsart UniversityNakhon PathomThailand
  2. 2.Center of Excellence on Agricultural Biotechnology: (AG-BIO/PERDO-CHE)BangkokThailand
  3. 3.Primate Research Unit, Department of Biology, Faculty of ScienceChulalongkorn UniversityBangkokThailand
  4. 4.Courant Research Centre Evolution of Social BehaviourGeorg August UniversityGöttingenGermany
  5. 5.Evolutionary Morphology Section, Primate Research InstituteKyoto UniversityInuyamaJapan
  6. 6.Department of Pathology, Faculty of Veterinary MedicineKasetsart UniversityNakhon PathomThailand

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