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Non-invasive sampling and DNA amplification for paternity exclusion, community structure, and phylogeography in wild chimpanzees

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  • Part 1: Molecular Ecology — The Present And The Future
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Abstract

Genetic studies of free-ranging primates have been seriously impeded by difficulties of sampling tissues, including the undesirability of bleeding habituated animals, of transporting frozen samples to the laboratory, and of the inherent inadequacies of accessible variation including allozymes, mtDNA RFLP patterns and DNA fingerprints. We have developed methods of non-invasive DNA sampling and DNA-level genoty** which, when combined with a hierarchical analysis of mtDNA sequences and hypervariable nDNA simple sequence repeat (microsatellite) loci size length polymorphisms, facilitate the resolution of most questions at the individual, social group (community), population, and species (phylogenetic) levels. This approach, based on DNA amplified from shed hair, represents an important new tool for the acquisition of genetic information and will facilitate the study and management of both captive and free-ranging chimpanzees (Pan troglodytes). Our hierarchical analysis of population genetics of chimpanzees has revealed high historical levels of gene flow and large effective population sizes, as well as substantial divergence between the West African subspecies and chimpanzees from central and East Africa. At the community level, closer relatedness among philopatric males than among females supports the view that kin selection has been an evolutionary force sha** male-male cooperation in this species. Results from our study of the now relatively isolated Gombe community suggest that habitat fragmentation affects population genetic structure and possibly population viability.

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References

  • Avise, J. C., 1989. Gene trees and organismal histories: a phylogenetic approach to population biology.Evolution, 43: 1192–1208.

    Google Scholar 

  • Bygott, J. D., 1979. Agonistic behavior, dominance, and social structure in wild chimpanzees of the Gombe National Park. In:The Great Apes,D. A. Hamburg &E. R. McCown (eds.), Benjamin/Cummings Publ. Menlo Park, pp. 405–428.

    Google Scholar 

  • Caley, M. J., 1991. A null model for testing distributions of dispersal distances.Amer. Naturalist, 138: 524–532.

    Article  Google Scholar 

  • Chakraborty, R., T. R. Meagher, &P. E. Smouse, 1988. Parentage analysis with genetic markers in natural populations: I. the expected proportion of offspring with unambiguous paternity.Genetics, 118: 527–536.

    CAS  PubMed  Google Scholar 

  • Chakravarti, A. &C. C. Li, 1983. The effect of linkage on paternity calculations. In:Inclusion Probabilities in Parentage Testing,R. H. Walker,R. J. Duquesnoy,E. R. Jennings,H. D. Krause,C. L. Lee, &H. F. Polesky (eds.), American Association of Blood Banks, Arlington, Virginia, pp. 411–420.

    Google Scholar 

  • di Rienzo, A. &A. C. Wilson, 1991. Branching pattern in the evolutionary tree for human mitochondrial DNA.Proc. Natl. Acad. Sci. U.S.A., 88: 1597–1601.

    PubMed  Google Scholar 

  • Edwards, A., H. A. Hammond, L. **, C. T. Caskey, &R. Chakraborty, 1992. Genetic variation at five trimeric and tetrameric tandem repeat loci in four human population groups.Genomics, 12: 241–253.

    Article  CAS  PubMed  Google Scholar 

  • Ferris, S. D., W. M. Brown, W. S. Davidson, &A. C. Wilson, 1981. Extensive polymorphism in the mitochondrial DNA of apes.Proc. Natl. Acad. Sci. U.S.A., 78: 6319–6323.

    CAS  PubMed  Google Scholar 

  • Foran, D. R., J. E. Hixson, &W. M. Brown, 1988. Comparisons of ape and human sequences that regulate mitochondrial DNA transcription and D-loop DNA synthesis.Nucleic Acids Res., 16: 5841–5861.

    CAS  PubMed  Google Scholar 

  • Ghiglieri, M. P., 1984.The Chimpanzees of Kibale Forest: A Field Study of Ecology and Social Structure. Columbia Univ. Press, New York.

    Google Scholar 

  • Goodall, J., 1986.The Chimpanzees of Gombe: Patterns of Behavior. The Belknap Press of Harvard Univ. Press, Cambridge, Massachusetts.

    Google Scholar 

  • Groves, C. P., 1989.A Theory of Human and Primate Evolution. Clarendon Press, Oxford.

    Google Scholar 

  • ————,C. Westwood, &B. T. Shea, 1992. Unfinished business: Mahalanobis and a clockword orang.J. Human Evol., 22: 327–340.

    Google Scholar 

  • Hasegawa, M., H. Kishino, K. Hayasaka, &S. Horai, 1990. Mitochondrial DNA evolution in primates.J. Mol. Evol., 31: 113–121.

    Article  CAS  PubMed  Google Scholar 

  • Hasegawa, T., 1990. Sex differences in ranging patterns. In:The Chimpanzees of the Mahale Mountains: Sexual and Life History Strategies,T. Nishida (ed.), Univ. of Tokyo Press, Tokyo, pp. 99–114.

    Google Scholar 

  • Hill, W. C. O., 1969. The nomenclature, taxonomy and distribution of chimpanzees. In:The Chimpanzees,G. H. Bourne (ed.), Karger, Basel, pp. 22–49.

    Google Scholar 

  • Hoelzel, A. R., J. M. Hancock, &G. A. Dover, 1991. Evolution of the cetation mitochondrial D-loop region.Mol. Biol. Evol., 8: 475–493.

    CAS  PubMed  Google Scholar 

  • Kocher, T. D. &A. C. Wilson, 1991. Sequence evolution of mitochondrial DNA in humans and chimpanzees. In:Evolution of Life,S. Ohsawa &T. Honjo (eds.), Springer-Verlag, Tokyo, pp. 391–413.

    Google Scholar 

  • Lander, E. S., 1989. DNA fingerprinting on trial.Nature, 339: 501–505.

    Article  CAS  PubMed  Google Scholar 

  • ————, 1991. Research on DNA ty** catching up with courtroom application.Amer. J. Human Genet., 48: 819–823.

    CAS  Google Scholar 

  • Lynch, M., 1988. Estimation of relatedness by DNA fingerprinting.Mol. Biol. Evol., 5: 584–599.

    CAS  PubMed  Google Scholar 

  • ———— &W. Gabriel, 1990. Mutation load and the survival of small populations.Evolution, 44: 1725–1737.

    Google Scholar 

  • Morin, P. A., 1992a. Population Genetics of Chimpanzees. Ph.D. thesis, Univ. of California, San Diego.

    Google Scholar 

  • ————, 1992b. Reproductive strategies in chimpanzees. In:Population Genetics of Chimpanzees, Ph.D. thesis, Univ. of California, San Diego, pp. 6–90.

    Google Scholar 

  • ————,J. J. Moore, R. Chakraborty, &D. S. Woodruff, 1992. Levels of simple sequence repeat allelic diversity at community and species levels in the chimpanzee (Pan troglodytes). In:Population Genetics of Chimpanzees, Ph.D. thesis, Univ. of California, San Diego, pp. 136–162.

    Google Scholar 

  • ————, ————,J. Wallis, &D. S. Woodruff, 1992. Paternity exclusion in a wild community of chimpanzees using hypervariable simple sequence repeats. In:Population Genetics of Chimpanzees, Ph.D. thesis. Univ. of California, San Diego, pp. 111–135.

    Google Scholar 

  • ————, ————, &D. S. Woodruff, 1992a. Identification of chimpanzee subspecies with DNA from hair and allele specific probes.Proc. R. Soc. London, B249: 293–297.

    Google Scholar 

  • ————, ————, & ————, 1992b. Mitochondrial DNA sequence variation within and between chimpanzee subspecies. In:Population Genetics of Chimpanzees, Ph.D. thesis, Univ. of California, San Diego, pp. 163–191.

    Google Scholar 

  • ———— &O. A. Ryder, 1991. Founder contribution and pedigree inference in a captive breeding colony of lion-tailed macaques, using mitochondrial DNA and DNA fingerprint analyses.Zoo Biol., 10: 341–352.

    Article  Google Scholar 

  • ———— &D. S. Woodruff, 1992. Paternity exclusion using multiple hypervariable microsatellite loci amplified from nuclear DNA of hair cells. In:Paternity in Primates: Genetic Tests and Theories,R. D. Martin,A. F. Dixson, &E. J. Wickings (eds.), Karger, Basel, pp. 63–81.

    Google Scholar 

  • Nishida, T., 1979. The social structure of chimpanzees of the Mahale Mountains. In:The Great Apes,D. A. Hamburg &E. R. McCown (eds), Benjamin/Cummings Publ., Menlo Park, pp. 73–121.

    Google Scholar 

  • ————, (ed.), 1990. The Chimpanzees of the Mahale Mountains: Sexual and Life History Strategies. Univ. of Tokyo Press, Tokyo.

    Google Scholar 

  • Orrego, C., E. Prager, P. Smith, P. A. Morin, S. Woodward, F. Villablanca, M. Fisher, P. Barber, S. Mack, J. Nielsen, B. Best, W. Rainey, & T. Smith, in prep. Versatility of Chelexmediated DNA extraction for sequence amplification.

  • Pesole, G., E. Sbisa, G. Preparata, &C. Saccone, 1992. The evolution of the mitochondrial D-loop region and the origin of modern man.Mol. Biol. Evol., 9: 587–598.

    CAS  PubMed  Google Scholar 

  • Pusey, A. E., 1979. Intercommunity transfer of chimpanzees in Gombe National Park. In:The Great Apes,D. A. Hamburg &E. R. McCown (eds.), The Benjamin/Cummings Publ., Menlo Park, pp. 465–480.

    Google Scholar 

  • ————, 1980. Inbreeding avoidance in chimpanzees.Anim. Behav., 28: 543–552.

    Google Scholar 

  • Queller, D. C. &K. F. Goodnight, 1989. Estimating relatedness using genetic markers.Evolution, 43: 258–275.

    Google Scholar 

  • Seal, U. S. &N. R. Flessness, 1986. Captive chimpanzee populations — past, present, and future. In:Primates. The Road to Self-sustaining Populations,K. Benirschke (ed.), Springer-Verlag, New York, pp. 47–55.

    Google Scholar 

  • Smouse, P. E. &R. Chakraborty, 1986. The use of restriction fragment length polymorphisms in paternity analysis.Amer. J. Human Genet., 38: 918–939.

    CAS  Google Scholar 

  • Spiess, E. B., 1989.Genes in Populations. Wiley, New York.

    Google Scholar 

  • Staub, K. C., D. S. Woodruff, E. S. Upatham, &V. Viyanant, 1990. Genetic variation inNeotricula aperta, the intermediate snail host ofSchistosoma mekongi: allozyme differences reveal a group of sibling species.Amer. Malacol Bul., 7: 93–103.

    Google Scholar 

  • Sugiyama, Y. &J. Koman, 1979. Social structure and dynamics of wild chimpanzees at Bossou, Guinea.Primates, 20: 323–339.

    Google Scholar 

  • Tutin, C. E. G., 1979. Mating patterns and reproductive strategies in a community of wild chimpanzees (Pan troglodytes schweinfurthii).Behav. Ecol. Sociobiol., 6: 29–38.

    Article  Google Scholar 

  • ————,W. C. McGrew, &P. J. Baldwin, 1983. Social organization of savanna-dwelling chimpanzees,Pan troglodytes verus, at Mt. Assirik, Senegal.Primates, 24: 154–173.

    Google Scholar 

  • Waser, P. M., 1987. A model predicting dispersal distance distributions. In:Mammalian Dispersal Patterns,B. K. Chepko-Sade &Z. T. Halpin (eds.), Univ. of Chicago Press, Chicago, pp. 251–256.

    Google Scholar 

  • Wilson, A. C., H. Ochman, &E. M. Prager, 1987. Molecular time scale for evolution.Trends Genet., 3: 241–247.

    Article  CAS  Google Scholar 

  • ———— &V. M. Sarich, 1967. Immunological time scale for Hominid evolution. Science, 158: 1200–1203.

    PubMed  Google Scholar 

  • Woodruff, D. S., 1990. Genetics and demography in the conservation of biodiversity.J. Sci. Soc. Thailand, 16: 117–132.

    Google Scholar 

  • ————, 1992. Genetics and the conservation of animals in fragmented habitats. In:In Harmony with Nature: Proceedings of the International Conference on Tropical Biodiversity, June 6–12, 1990, Kuala Lumpur, Malaysia, Malay Nature Society, Kuala Lumpur, pp. 258–272.

    Google Scholar 

  • ————, 1993.Non-invasive genoty** of primates. Primates, 34: 333–346.

    Google Scholar 

  • Wrangham, R. W., 1979. Sex differences in chimpanzee dispersion. In:The Great Apes,D. A. Hamburg &E. R. McCown (eds.), Benjamin/Cummings Publ., Menlo Park, pp. 481–489.

    Google Scholar 

  • ————, 1982. Mutualism, kinship, and social evolution. In:Current Problems in Sociobiology,Kings College Sociobiology Group (eds.), Cambridge Univ. Press, Cambridge, pp. 269–289.

    Google Scholar 

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Author notes

  1. Phillip A. Morin

    Present address: Department of Biology, University of California, 92093, San Diego, La Jolla, California, USA

Authors and Affiliations

  1. University of Oregon, USA

    Phillip A. Morin

  2. Department of Obstetrics and Gynecology, University of Oklahoma, 73190, Oklahoma City, Oklahoma, USA

    Janette Wallis

  3. Department of Anthropology, University of California, 92093, San Diego, La Jolla, California, USA

    James J. Moore

  4. Center for Demographic and Population Genetics, University of Texas Graduate School of Biomedical Sciences, 77225, Houston, Texas, USA

    Ranajit Chakraborty

  5. Department of Biology, University of California, 92093, San Diego, La Jolla, California, USA

    David S. Woodruff

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  1. Phillip A. Morin
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  2. Janette Wallis
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  4. Ranajit Chakraborty
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  5. David S. Woodruff
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Morin, P.A., Wallis, J., Moore, J.J. et al. Non-invasive sampling and DNA amplification for paternity exclusion, community structure, and phylogeography in wild chimpanzees. Primates 34, 347–356 (1993). https://doi.org/10.1007/BF02382630

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  • DOI: https://doi.org/10.1007/BF02382630

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