Primates

, Volume 37, Issue 3, pp 305–318

Matrilineal kin relationship and social behavior of wild bonobos (Pan paniscus): Sequencing the D-loop region of mitochondrial DNA

  • Chie Hashimoto
  • Osamu Takenaka
  • Takeshi Furuichi
Article

Abstract

Matrilineal kin-relations among wild bonobos (Pan paniscus) were studied by DNA analysis. Subject individuals were the members of E1 group, living at Wamba, Zaire, which has been studied since 1974. DNA samples were extracted from wadges that bonobos spat out when feeding on sugar cane. The D-loop region of mitochondrial DNA was amplified by the PCR method, and a nucleotide sequence of 350 base pairs was determined for 17 individuals. Nucleotide variations were found at 44 positions of the sequence. Based on these variations, 13 matrilineal units were divided into seven groups, and the mother of an orphan male was determined among several females. These genetic analyses, together with behavioral observation to date, revealed the following facts. High sequence variation in the target region indicated that females transfer between groups of bonobos, which is in agreement with supposition from long-term field studies. For females, there was no relationship between genetic closeness and social closeness that is represented by frequencies of proximity or grooming. After immigration into a new group, females form social associations with senior females without regard to kin relationship.

Key Words

Pan paniscus D-loop region Mitochondrial DNA PCR direct sequencing Kin relationship Social behavior 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Anderson, S.;Bankier, A. T.;Barrell, B. G.;de Bruijn, M. H. L.;Coulson, A. R.;Drouin, J.;Eperon, I. C.;Nierlich, D. P.;Roe, B. A.;Sanger, F.;Schreier, P. H.;Smith, A. J. H.;Staden, R.;Young, I. G. 1981. Sequence and organization of the human mitochondrial genome.Nature, 290: 457–465.PubMedGoogle Scholar
  2. Elsacker, L. V. 1995. A review of terminology on aggregation patterns in bonobos (Pan paniscus).Int. J. Primatol., 16: 37–52.Google Scholar
  3. Felsenstein, J. 1993. PHYLIP (phylogeny inference package) Version 3.5c. Distributed by the author. Dept. Genet., Univ. of Washington, Seattle.Google Scholar
  4. Furuichi, T. 1987. Sexual swelling, receptivity, and grouping of wild pygmy chimpanzee females at Wamba, Zaire.Primates, 28: 309–318.CrossRefGoogle Scholar
  5. Furuichi, T. 1989. Social interactions and the life history of femalePan paniscus in Wamba, Zaire.Int. J. Primatol., 10: 173–197.Google Scholar
  6. Furuichi, T.; Idani, G.; Ihobe, H.; Kuroda, S.; Kitamura, K.; Mori, A.; Enomoto, T.; Okayasu, N.; Hashimoto, C.; Kano, T. 1995. Population dynamics of wild groups of bonobos at Wamba, Zaire. Paper presented at the 11th Congress of the Primate Society of Japan, Aichi, Japan.Google Scholar
  7. Furuichi, T.;Ihobe, H. 1995. Variation in male relationships in bonobos and chimpanzees.Behaviour, 130: 212–228.Google Scholar
  8. Goodall, J. 1986.The Chimpanzees of Gombe: Patterns of Behavior. Harvard Univ. Press, Cambridge, Massachusetts.Google Scholar
  9. Hashimoto, C.;Furuchi, T. 1994. Social role and development of noncopulatory sexual behavior of wild bonobos. In:Chimpanzee Cultures,Wrangham,R. W.;McGrew,W. C.;de Waal,B. M.;Heltne,P. G. (eds.), Harvard Univ. Press, Cambridge, Massachusetts & London, pp. 155–168.Google Scholar
  10. Higuchi, R.;von Beroldingen, C. H.;Sensabaugh, G. F.;Erlich, H. A. 1988. DNA typing from single hairs.Nature, 332: 543–546.CrossRefPubMedGoogle Scholar
  11. Idani, G. 1990. Relations between unit-groups of bonobos at Wamba, Zaire: encounters and temporary fusions.Afr. St. Monogr., 11: 153–186.Google Scholar
  12. Idani, G. 1991. Social relationships between immigrant and resident bonobo (Pan paniscus) females at Wamba.Folia Primatol., 57: 83–95.PubMedGoogle Scholar
  13. Ihobe, H. 1992. Male-male relationships among wild bonobos (Pan paniscus) at Wamba, Republic of Zaire.Primates, 33: 163–179.Google Scholar
  14. Inoue, M.;Takenaka, A.;Tanaka, S.;Kominami, R.;Takenaka, O. 1990. Paternity discrimination in a Japanese macaque group by DNA fingerprinting.Primates, 31: 563–570.Google Scholar
  15. Inoue, M.;Takenaka, O. 1993. Japanese macaque microsatellite PCR primers for paternity testing.Primates, 34: 37–45.Google Scholar
  16. Jeffereys, A. J.;Wilson, V.;Thein, S. L. 1985. Hypervariable “microsatellite” regions in human DNA.Nature, 314: 67–73.Google Scholar
  17. Kano, T. 1982. The social group of pygmy chimpanzees (Pan paniscus) of Wamba.Primates, 23: 171–188.Google Scholar
  18. Kano, T. 1992.The Last Ape: Pygmy Chimpanzee Behavior and Ecology. Stanford Univ. Press, Stanford.Google Scholar
  19. Kitamura, K. 1983. Pygmy chimpanzee association patterns in ranging.Primates, 24: 1–12.Google Scholar
  20. Kocher, T. D.;Wilson, A. G. 1991. Sequence evolution of mitochondrial DNA in humans and chimpanzees: control region and a protein-coding region. In:Evolution of Life: Fossils, Molecules, and Culture,Osawa,S.;Honjo,T. (eds.), Springer-Verlag, Tokyo, pp. 391–413.Google Scholar
  21. Kuroda, S. 1980. Social behavior of the pygmy chimpanzees.Primates, 21: 181–197.Google Scholar
  22. Lipman, D. J.;Pearson, W. R. 1985. Rapid and sensitive protein similarity searches.Science, 227: 1435–1441.PubMedGoogle Scholar
  23. Litt, M.;Luty, J. A. 1989. A hypervariable microsatellite revealed byin vitro amplification of a dinucleotide repeat within the cardiac muscle actin gene.Amer. J. Hum. Genet., 44: 397–401.PubMedGoogle Scholar
  24. Morin, P. A.;Moore, J. J.:Chakraborty, R. C.;Jin, L.;Goodall, J.;Woodruff, D. S. 1994. Kin selection, social structure, gene flow, and the evolution of chimpanzees.Science, 265: 1193–1201.PubMedGoogle Scholar
  25. Murray, M. G.;Thompson, W. F. 1980. Rapid isolation of high-molecular-weight plant DNA.Nucl. Acids. Res., 8: 4321–4325.PubMedGoogle Scholar
  26. Sokal, R. R.;Michener, C. D. 1985. A statistical method for evaluating systematic relationships.Univ. of Kansas Sci. Bull., 28: 1409–1438.Google Scholar
  27. Takasaki, H.;Takenaka, O. 1991. Paternity testing in chimpanzees with DNA amplification from hairs and buccal cells in wadges: a preliminary note. In:Primatology Today,Ehara,A.;Kimura,T.;Takenaka,O.;Iwamoto,M. (eds.), Elsevier, Amsterdam, pp. 612–616.Google Scholar
  28. Takenaka, O.;Takasaki, H.;Kawamoto, S.;Arakawa, M.;Takenaka, A. 1993. Polymorphic microsatellite DNA amplification customized for chimpanzee paternity testing.Primates, 34: 27–35.Google Scholar
  29. Tegelström, H. 1986. Mitochondrial DNA in natural populations: an improved routine for the screening of genetic variation based on sensitive silver staining.Electrophoresis, 7: 226–229.Google Scholar
  30. de Waal, F. B. M. 1995. Bonobo sex and society.Sci. Amer., 272: 82–88.PubMedGoogle Scholar
  31. Weber, J. L.;May, P. E. 1989. Abundant class of human DNA polymorphism which can be typed using the polymerase chain reaction.Amer. J. Human Genet., 44: 388–396.Google Scholar
  32. White, F. J. 1988. Party composition and dynamics inPan paniscus.Int. J. Primatol., 9: 179–193.Google Scholar
  33. Wrangham, R. W. 1993. The evolution of sexuality in chimpanzees and bonobos.Human Nature, 4: 47–79.Google Scholar

Copyright information

© Japan Monkey Centre 1996

Authors and Affiliations

  • Chie Hashimoto
    • 1
  • Osamu Takenaka
    • 1
  • Takeshi Furuichi
    • 2
  1. 1.Primate Research InstituteKyoto UniversityKanrin, Inuyama, AichiJapan
  2. 2.Laboratory of BiologyMeiji-Gakuin UniversityYokohama, KanagawaJapan

Personalised recommendations