, Volume 43, Issue 4, pp 315–327 | Cite as

Population subdivision and gene flow among wild orangutans

  • Sreetharan Kanthaswamy
  • David Glenn Smith


Genetic variability among populations of orangutans from Borneo and Sumatra was assessed using seven SSR loci. Most SSR loci were highly polymorphic and their allele frequencies exhibited substantial variation across subpopulations. While significant genetic subdivision was observed among the island populations, genetic distance did not increase with geographic distance and sufficient gene flow persists to prevent marked genetic subdivision. Since it is unlikely that the Bornean Orangutans dispersed naturally among locations separated by such formidable geographic barriers, human assistance might already have altered their genetic structure. Our data suggests that there may be at least two subspecific clades of orangutans within Borneo while Central Kalimantan animals may have become more genetically related to animals in Sumatra due to human intervention.

Key Words

Pongo pygmaeus Microsatellite polymorphism Migration Conservation 


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  1. Allendorf, F. W. 1983. Isolation, gene flow and genetic differentiation among populations. In:Genetics and Conservation,Shonewald-Cox,C. M.;Chambers,S. M.;MacBryde,B.;Thomas,L. (eds.), Benjamin-Cummings, London, pp. 51–65.Google Scholar
  2. Andau, P. M.;Hiong, L. K.;Sale, J. B. 1994. Translocations of pocketed orangutans in Sabah.Oryx, 28: 263–268.CrossRefGoogle Scholar
  3. Avise, J. C. 1994.Molecular Markers, Natural History and Evolution. Chapman & Hall, New York.CrossRefGoogle Scholar
  4. Ball, R. M.;Neigel, J. E.;Avise, J. C. 1990. Gene genealogies within the organismal pedigrees of random mating populations.Evolution, 44: 360–370.CrossRefGoogle Scholar
  5. Bosi, E.; Kilbourn, E.; Karesh, W.; Andau, M.; Tambing, E.; Komiji, J. in press. Orangutan nest counts using a helicopter at Tabin and Sepilok, Sabah, Malaysia. In:All Apes Great and Small, Vol. 2: Asian Apes,Galdikas, B.; Briggs, N.; Sheeran, L.; Shapiro, G.; Goodall, J. (eds.), Kluver, New York.Google Scholar
  6. Bruce, E. J.;Ayala, F. J. 1979. Phylogenetic relationships between man and apes: electrophoretic evidence.Evolution, 33: 1040–1056.CrossRefGoogle Scholar
  7. Callen, D. F.;Thompson, A. D.;Shen, Y. 1993. Incidence and origin of ‘null’ alleles in the (AC)n microsatellite markers.Amer. J. Human Genet., 52: 922–927.Google Scholar
  8. Cockerham, C. C. 1973. Analyses of gene frequencies.Genetics, 74: 679–700.PubMedGoogle Scholar
  9. Courtenay, J.;Groves, C.;Andrews, P. 1988. Inter-or intra-island variation? An assessment of the differences between Bornean and Sumatran orang-utans. In:Orang-utan Biology,Schwartz,J. H. (ed.), Oxford, Univ. Press, Oxford, pp. 19–29.Google Scholar
  10. Falconer, D. S. 1981.Introduction to Quantitative Genetics (2nd ed.). Longman, London.Google Scholar
  11. Ferber, D. 2000. Orangutans face extinctions in the wild.Science, 288: 1147–1149.PubMedCrossRefGoogle Scholar
  12. Groves, C. P.;Westwood, C.;Shae, B. T. 1992. Unfinished business: Mahalanobis and a clockwork orang.J. Human Evol., 22: 327–340.CrossRefGoogle Scholar
  13. Grumbine, R. E. 1994. What is ecosystem management?Conserv. Biol., 8: 27–38.CrossRefGoogle Scholar
  14. Hartl, D. L.;Clark, C. G. 1989.Principles of Population Genetics. Sinauer Associates, Massachusetts.Google Scholar
  15. Janczewski, D. N. 1989. Estimate of genetic distance of orang utan (Pongo pygmaeus) subspecies based on isozyme and two-dimensional gel electrophoresis. Ph.D. thesis, George Mason Univ., Fairfax, Virginia.Google Scholar
  16. Janczewski, D. N.;Goldman, D.;O’Brien, S. J. 1990. Molecular genetic divergence of orang-utan (Pongo pygmaeus) subspecies based on isozyme and two dimensional gel electrophoresis.Heredity, 81: 375–397.Google Scholar
  17. Kanthaswamy, S.;Bininda-Emonds, O.;Viray, J.;Warden, C.;Smith, D. G. 2001. Use of simple sequence repeat fragment length homozygotes to study systematics of the Bornean and Sumatran Orangutan.Primates, 42: 35–45.CrossRefGoogle Scholar
  18. Kanthaswamy, S.; Ely, J.; Smith, D. G. in press. Simple sequence repeat polymorphisms for captive and wild orangutan conservation management. In:All Apes Great and Small, Vol. 2: Asian Apes,Galdikas, B.; Briggs, N.; Sheeran, L.; Shapiro, G.; Goodall, J. (eds.), Kluver, New York.Google Scholar
  19. Kanthaswamy, S.;Smith, D. G. 1998. Use of SSR polymorphisms for paternity exclusion in rhesus macaques (Macaca mulatta).Primates, 39: 135–145.CrossRefGoogle Scholar
  20. Kavanagh, M.;Eudley, A. A.;Mack, D. 1987. The effect of live trapping and trade on primate populations. In:Primate Conservation in the Tropical Rain Forest,Marsh,C. W.;Mittermeier,R. A. (eds.), Alan R. Liss, New York, pp. 147–177.Google Scholar
  21. Kawamoto, Y.;Takenaka, O.;Brotoisworo, E. 1982. Preliminary report on genetic variations within and between species of Sulawesi macaques.Kyoto Univ. Res. Inst., 2: 23–37.Google Scholar
  22. Levene, H. 1949. On matching problems in genetics.Ann. Math. Stat., 20: 91–94.CrossRefGoogle Scholar
  23. Mackinnon, J. R. 1974. The behaviour and ecology of wild orangutans (Pongo pygmaeus).Anim. Behav., 22: 3–74.CrossRefGoogle Scholar
  24. Melnick, D. J.;Hoelzer, G. A. 1992. Differences in male and female macaque dispersal lead to contrasting distributions of nuclear and mitochondrial DNA variation.Int. J. Primatol., 13: 379–393.CrossRefGoogle Scholar
  25. Morin, P. A.;Kanthaswamy, S.;Smith, D. G. 1997. Simple sequence repeat (SSR) polymorphism for colony management and population genetics in rhesus macaques (Macaca mulatta).Amer. J. Primatol., 42: 199–213.CrossRefGoogle Scholar
  26. Morin, P. A.;Moore, J. J.;Chakraborty, R.;Jin, L.;Goodall, J.;Woodruff, D. S. 1994. Kin selection, social structure, gene flow and the evolution of chimpanzees.Science, 265: 1193–1201.PubMedCrossRefGoogle Scholar
  27. Morin, P. A.;Smith, D. G. 1995. Non-radioactive detection of hypervariable simple sequence repeats in short polyacrylamide gels.Bio Techniques, 19: 227–237.Google Scholar
  28. Morin, P. A.;Woodruff, D. S. 1992. Paternity exclusion using multiple hypervariable SSR loci amplified from nuclear DNA of hair cells. In:Paternity in Primates: Genetic Tests and Theories: Implications of Human DNA Fingerprinting,Martin,R. D.;Dixson,A. F.;Wickings,E. J. (eds.), Karger, New York, pp. 63–81.Google Scholar
  29. Moritz, C. 1994. Defining evolutionarily significant units for conservation.Tree, 9: 373–375.PubMedGoogle Scholar
  30. Muir, C. C.;Galdikas, B. M. F.;Beckenbach, A. T. 2000. mtDNA sequence diversity of orangutans from the islands of Borneo and Sumatra.J. Mol. Evol., 51: 471–480.PubMedGoogle Scholar
  31. Nei, M. 1987.Molecular Evolutionary Genetics. Columbia Univ. Press, New York.Google Scholar
  32. Paetkau, D.;Calvert, W.;Stirling, I.;Stroebeck, C. 1995. Microsatellite analysis of population in Canadian polar bears.Mol. Ecol., 4: 347–354.PubMedCrossRefGoogle Scholar
  33. Paetkau, D.;Waits, L. P.;Clarkson, P. L.;Craighead, L.;Strobeck, C. 1997. An empirical evaluation of genetic distance statistics using microsatellite data from bear (Ursidae) populations.Genetics, 147: 1943–1957.PubMedGoogle Scholar
  34. Palumbi, S. R.;Baker, C. S. 1994. Contrasting population structuer from nuclear intron sequences and mtDNA of humpback whales.Mol. Biol. Evol., 11: 426–435.PubMedGoogle Scholar
  35. Raymond, M.;Rousset, F. 1995a. GENEPOP (Version 1.2): population genetics software for exact tests and ecumenicism.Heredity, 86: 248–249.Google Scholar
  36. Raymond, M.;Rousset, F. 1995b. An exact test for population differentiation.Evolution, 49: 1280–1283.CrossRefGoogle Scholar
  37. Richard, M.;Thorpe, R. S. 2001. Can microsatellites be used to infer phylogenies?: evidence from population affinities of the Western Canary Island lizard (Gallotia galloti).Mol. Phylogenet. Evol., 20: 351–360.PubMedCrossRefGoogle Scholar
  38. Rijksen, H. D. 1978.A Field Study of Sumatran Orangutans. H. Veenman & Zonen, Wagenigen.Google Scholar
  39. Rijksen, H. D.;Meijaard, E. 1999.Our Vanishing Relative. Kluwer Academic Publ., Dordrecht.CrossRefGoogle Scholar
  40. Robertson, A.;Hill, W. G. 1984. Deviations from Hardy-Weinberg proportions: sampling variances and use in estimation of inbreeding coefficients.Genetics, 107: 713–718.Google Scholar
  41. Rodman, P. S. 1978. Diets, densities, and distributions of Bornean primates. In:The Ecology of Arboreal Folivores,Montgomerry,G. G. (ed.), Smithsonian Instit. Press, Washington, D. C.Google Scholar
  42. Ruvolo, M.;Pan, D.;Zehr, S.;Goldberg, T.;Dissotell, T. R.;von Dornum, M. 1994. Gene trees and hominoid phylogeny.PNAS, 91: 8900–8904.PubMedCrossRefGoogle Scholar
  43. Ryder, O. A.;Chemnick, L. G. 1993. Chromosomal and mitochondrial DNA variation in orang-utans.Heredity, 84: 405–409.Google Scholar
  44. Scribner, K. T.;Arntzen, J. W.;Burke, T. 1994. Comparative analysis of intra- and inter-population genetic diversity inBufo bufo, using allozyme, single-locus microsatellite, minisatellite, and multilocus minisatellite data.Mol. Biol. Evol., 11: 737–748.PubMedGoogle Scholar
  45. Slatkin, M. 1985. Gene flow in natural populations.Ann. Rev. Ecol. Syst., 16: 393–430.CrossRefGoogle Scholar
  46. Slatkin, M.;Barton, N. H. 1989. A comparison of three indirect methods of estimating gene flow.Evolution, 43: 1347–1368.CrossRefGoogle Scholar
  47. Slatkin, M.;Maddison, W. P. 1989. A cladistic measure of gene flow inferred from the phylogenies of alleles.Genetics, 123: 603–613.PubMedGoogle Scholar
  48. Slatkin, M.;Maddison, W. P. 1990. Detecting isolation by distance using phylogenies of genes.Genetics, 126: 249–260.PubMedGoogle Scholar
  49. Smith, D. G.;Kanthaswamy, S.;Disbrow, M.;Wagner, J. L. 1999. Reconstruction of parentage in a band of captive hamadryas baboons.Int. J. Primatol., 20: 415–429.CrossRefGoogle Scholar
  50. St. George, D.;Witte, S. M.;Turner, T. R.;Weiss, M. L.;Phillips-Conroy, J.;Smith, E. O.;Rogers, J. 1998. Microsatellite variation in two populations of free-ranging yellow baboons (Papio hamadryas cynocephalus).Int. J. Primatol., 19: 273–285.CrossRefGoogle Scholar
  51. Sugardjito, J.;te Boekhorst, I. J. A.;van Hooff, J. A. R. A. M. 1987. Ecological constraints on the grouping of wild orang-utans (Pongo pygmaeus) in the Gunung Leuser National Park, Sumatra, Indonesia.Int. J. Primatol., 8: 17–41.CrossRefGoogle Scholar
  52. Swofford, D. L.;Selander, R. B. 1981. Biosys-1: A FORTRAN program for the comprehensive analysis for electrophoretic data in population genetics and systematics.Heredity, 72: 281–283.Google Scholar
  53. te Boekhorst, I. J. A.;Schürmann, C. L.;Sugardjito, J. 1990. Residential status and seasonal movements of wild orang-utans in the Gunung Leuser Reserve (Sumatra, Indonesia).Anim. Behav., 39: 1098–1109.CrossRefGoogle Scholar
  54. Thorpe, J. P. 1982. The molecular clock hypothesis: biochemical evolution, genetic differentiation, and systematics.Ann. Rev. Ecol. Syst., 13: 139–168.CrossRefGoogle Scholar
  55. Uchida, A. 1998. Variation in tooth morphology ofPongo pygmaeus.J. Human Evol., 34: 71–79.CrossRefGoogle Scholar
  56. Warren, K. S.;Nijman, I. J.;Lenstra, J. A.;Swan, R. A.;Heriyanto;den Boer, M. H. 2000. Microsatellite DNA variation in Bornean orang-utans (Pongo pygmaeus).J. Med. Primatol., 29: 57–62.PubMedCrossRefGoogle Scholar
  57. Warren, K. S.;Verschoor, E. J.;Langenhuijzen, S.;Heriyanto;Swan, R. A.;Vigilant, L.;Heeney, J. 2001. Speciation and intrasubspecific variation of Bornean Orangutans,Pongo pygmaeus pygmaeus.Mol. Biol. Evol., 18: 472–480.PubMedCrossRefGoogle Scholar
  58. Weir, B. S. 1990a. Intraspecific differentiation. In:Molecular Systematics,Hillis,D. M.;Moritz,C. (eds.), Sinauer Associates, Massachusetts, pp. 373–410.Google Scholar
  59. Weir, B. S. 1990b.Genetic Data Analysis. Sinauer Publ., Massachusetts.Google Scholar
  60. Weir, B. S.;Cockerham, C. C. 1984. Estimating F-statistics for the analysis of population structure.Evolution, 38: 1358–1370.CrossRefGoogle Scholar
  61. Winkler, L. 1988. Morphology and relationships of the orangutan fatty cheek pads.Amer. J. Primatol., 17: 305–319.CrossRefGoogle Scholar
  62. Wright, S. 1943. Isolation by distance.Genetics, 28: 114–138.PubMedGoogle Scholar
  63. Wright, S. 1951. The genetical structure of populations.Annals of Eugenics, 15: 323–354.CrossRefGoogle Scholar
  64. Xu, X.;Arnason, U. 1996. The mitochondrial molecule of Sumatran Orangutan and a molecular proposal for two (Bornean and Sumatran) species of orangutans.Mol. Evol., 3: 431–437.CrossRefGoogle Scholar
  65. Zhi, L.;Karesh, W. B.;Janczewski, D. N.;Frazier-Taylor, H.;Dondin Sajuthi;Francis Gombek;Mahedi Andau;Martenson, J. S.;O’Brien, S. J. 1996. Genomic differention among natural populations of orang-utan (Pongo pygmaeus).Curr. Biol., 6: 1326–1336.PubMedCrossRefGoogle Scholar

Copyright information

© Japan Monkey Centre 2002

Authors and Affiliations

  • Sreetharan Kanthaswamy
    • 1
  • David Glenn Smith
    • 2
  1. 1.Department of Internal MedicineUniversity of Iowa College of Medicine, Department of Veteran Affairs Medical CenterIowa CityUSA
  2. 2.Department of AnthropologyUniversity of CaliforniaDavisUSA

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