New Genetic Evidence on the Evolution of Chimpanzee Populations and Implications for Taxonomy

  • Mary Katherine Gonder
  • Todd R. Disotell
  • John F. Oates
Article

Primatologists widely recognize chimpanzees as belonging to a single species, Pan troglodytes, which they traditionally have further divided into 3 subspecies: west African P. t. verus, central African P. t. troglodytes, and east African P. t. schweinfurthii. Previously, we suggested that the phylogeographic history of chimpanzees may be different from that implied by the widely used taxonomy of the species. We based the suggestion on only a limited sample of haplotypes from the first hypervariable region (HVRI) of mitochondrial (mt)DNA from chimpanzees in Nigeria. We have now compiled a more geographically comprehensive genetic database for chimpanzees, including samples obtained near the Niger and Sanaga Rivers. Our database is composed of 254 HVRI haplotypes from chimpanzees of known geographic origin, including 79 unique HVRI haplotypes from chimpanzees living in Nigeria and Cameroon. The genetic data provide clear evidence that a major phylogeographic break between chimpanzee lineages occurs near the Sanaga River in central Cameroon and suggest the need for a reclassification of chimpanzees.

Key words:

chimpanzees chimpanzee subspecies mtDNA phylogeography population structure 

REFERENCES

  1. Agbelusi, E. A. (1994). Wildlife conservation in Ondo State. The Nigerian Field. 59: 73–83.Google Scholar
  2. Andrews, R., Kubacka, I., Chinnery, P., Lightowlers, R., Turnbull, D., and Howell, N. (1999). Reanalysis and revision of the Cambridge reference sequence for human mitochondrial DNA. Nat. Genet. 2: 149.Google Scholar
  3. Barnwell, R. (1991). Gashaka-Gumti Game Reserve Gongola State Nigeria: An Indicative Proposal for Developing Gashaka-Gumti as a National Park. WWF, U.K.Google Scholar
  4. Braga, J. (1998). Chimpanzee variation facilitates the interpretation of the incisive suture closure in South African Plio-Pleistocene hominids. Am. J. Phys. Anthropol. 105(2): 121–135.PubMedCrossRefGoogle Scholar
  5. Chen, F. C., and Li, W. H. (2001). Genomic divergences between humans and other hominoids and the effective population size of the common ancestor of humans and chimpanzees. Am. J. Hum. Genet. 68(2): 444–456.PubMedCrossRefGoogle Scholar
  6. Collura, R. V., and Stewart, C. B. (1995). Insertions and duplications of mtDNA in the nuclear genome of old world monkeys and hominoids. Nature 378: 485–489.PubMedCrossRefGoogle Scholar
  7. Dowsett, R. J., and Dowsett-Lemaire, F. (1989). Larger mammals in the Gotel Mts and on the Mambilla Plateau, eastern Nigeria. In Dowsett, R. J. (ed.), A Preliminary Natural History Survey of Mambilla Plateau and Some Lowland Forests of Eastern Nigeria. Tauraco Research Report No. 1, 56 pp., Tauraco Press.Google Scholar
  8. Felsenstein, J. (1981). Evolutionary trees from DNA sequences: A maximum likelihood approach. J. Mol. Evol. 17(6): 368–376.PubMedCrossRefGoogle Scholar
  9. Fischer, A., Wiebe, V., Paabo, S., and Przeworski, M. (2004). Evidence for a complex demographic history of chimpanzees. Mol. Biol. Evol. 21(5): 799–808.PubMedCrossRefGoogle Scholar
  10. Gadsby, E. L., and Jenkins, P. D. (1992). Report on Wildlife and Hunting in the Proposed Etinde Forest Reserve. Limbe Botanic Garden & Rainforest Genetic Conservation Project, Limbe.Google Scholar
  11. Gagneux, P., Wills, C., Gerloff, U., Tautz, D., Morin, P. A., Boesch, C., Fruth, B., Hohmann, G., Ryder, O. A., and Woodruff, D. S. (1999). Mitochondrial sequences show diverse evolutionary histories of African hominoids. Proc. Natl. Acad. Sci. U S A 96(9): 5077–5082.PubMedCrossRefGoogle Scholar
  12. Gartlan, J. S., and Struhsaker, T. T. (1972). Polyspecific associations and niche separation of rain-forest anthropoids in Cameroon, West Africa. J. Zool. Soc. Lond. 168: 221–266.CrossRefGoogle Scholar
  13. Goldberg, T. L., and Ruvolo, M. (1997). The geographic apportionment of mitochondrial genetic diversity in east African chimpanzees, Pan troglodytes schweinfurthii. Mol. Biol. Evol. 14(9): 976–984.PubMedGoogle Scholar
  14. Goloboff, P. (1999). NONA. Version 2.0. Fundacion e Instituto Miguel Lillo: Tucuman, Argentina.Google Scholar
  15. Gonder, M. K. (2000). Evolutionary Genetics of Chimpanzees (Pan troglodytes) in Nigeria and Cameroon, Ph.D. Dissertation. City University of New York: New York. pp. 338.Google Scholar
  16. Gonder, M. K., and Disotell, T. R. (2006). Contrasting phylogeographic histories of chimpanzees in Nigeria and Cameroon: A multilocus analysis. In Lehman, S., and Fleagle, J. (ed.), Primate Biogeography. Springer, New York, pp. 129–161.Google Scholar
  17. Gonder, M. K., Oates, J. F., Disotell, T. R., Forstner, M. R., Morales, J. C., and Melnick, D. J. (1997). A new west African chimpanzee subspecies? Nature. 388(6640): 337.PubMedCrossRefGoogle Scholar
  18. Gray, J. E. (1862). List of mammalia from the Cameroon mountains, collected by Captain Burton, H.M. Consul, Fernado Po. P. Zool. Soc. Lond., pp. 180–181.Google Scholar
  19. Gray, M. W., Burger G., and Lang, B. F. (1999). Mitochondrial evolution. Science 283: 1476–1481.PubMedCrossRefGoogle Scholar
  20. Groves, C. P. (1993). Order Primates. In Wilson, D. E., and Reader, D. M. (ed.), Mammalian Species of the World: A Taxonomic and Geographic Reference. Smithsonian Institution Press, Washington, D.C., pp. 243–277.Google Scholar
  21. Groves, C. P. (2001). Primate Taxonomy. Smithsonian Institution Press, Washington, DC. vol. viii, 350 p.Google Scholar
  22. Groves, C. P. (2005). Geographic variation within eastern chimpanzees (Pan troglodytes c. schweinfrthii Giglioli, 1872). Australas. Primatol. 17: 19–46.Google Scholar
  23. Grubb, P. (1982). Refuges and dispersal in the speciation of African forest mammals. In Prance G. T. (ed.), Biological Diversification in the Tropics. Academic Press, New York, pp. 537–553.Google Scholar
  24. Grubb, P. (1990). Primate geography in the Afro-tropical forest biome. In Peters G., Hutterer R. (eds.), Vertebrates in the Tropics. Museum Alexander Koenig, Bonn, pp. 187–214.Google Scholar
  25. Grubb, P., Butynski, T., Oates, J., Bearder, S., Disotell, T., Groves, C., and Strusaker, T. (2003). Assessment of the diversity of African primates. Intl. J. Primatol. 24(6): 1301–1357.CrossRefGoogle Scholar
  26. Hill, W. C. O. (1967). The taxonomy of the genus Pan. In Stark, D., Schneider, D. and, Kuhn H. (eds.), Progress in Primatology. Fischer, Stutgart, pp. 47–54.Google Scholar
  27. Hill, W. C. O. (1969). The nomenclature, taxonomy and distribution of chimpanzees. In Bourne G. H. (ed.), The Chimpanzee. Karger, Basel, pp. 22–49.Google Scholar
  28. Ingman, M., and Gyllensten, U. (2003). Mitochondrial genome variation and evolutionary history of Australian and New Guinean aborigines. Genome Res. 13(7): 1600–1606.PubMedCrossRefGoogle Scholar
  29. Kaessmann, H., Wiebe, V., and Pääbo, S. (1999). Extensive nuclear DNA sequence diversity among chimpanzees. Science 286(5442): 1159–1162.PubMedCrossRefGoogle Scholar
  30. Kingdon, J. (1989). Island Africa. Princeton University Press, Princeton.Google Scholar
  31. Kitano, T., Schwarz, C., Nickel, B., and Paabo, S. (2003). Gene diversity patterns at 10 X-chromosomal loci in humans and chimpanzees. Mol. Biol. Evol. 20(8): 1281–1289.PubMedCrossRefGoogle Scholar
  32. Kormos. R, IUCN/SSC Primate Specialist Group, World Conservation Union. (2003). West African chimpanzees: Status survey and conservation action plan. IUCN–the World Conservation Union, Gland, Switzerland, vol. x, 219 p.Google Scholar
  33. Maddison W. P., and Maddison, D. R. (2000). MacClade: Analysis of Phylogeny and Character Evolution. Version 4.02. Sinauer Associates, Sunderland, MA.Google Scholar
  34. Meyer S., Weiss, G., and von Haesler, A. (1999). Pattern of nucleotide substitution and rate heterogeneity in the hypervariable regions I and II of human mtDNA. Genetics 152: 1103–1110.PubMedGoogle Scholar
  35. Mitani, M. (1991). A note on the present situation of the primate fauna found from south-eastern Cameroon to northern Congo. Primates 31(4): 625–634.CrossRefGoogle Scholar
  36. Morin, P. A., Chambers, K. E., Boesch, C., and Vigilant, L. (2001). Quantitative polymerase chain reaction analysis of DNA from noninvasive samples for accurate microsatellite genotyping of wild chimpanzees (Pan troglodytes verus). Mol. Ecol. 10(7): 1835–1844.PubMedCrossRefGoogle Scholar
  37. Morin, P. A., Moore, J. J., Chakraborty, R., Jin, L., Goodall, J., and Woodruff, D. S. (1994). Kin selection, social structure, gene flow, and the evolution of chimpanzees. Science 265(5176): 1193–1201.PubMedCrossRefGoogle Scholar
  38. Oates, J. F. (1988). The distribution of Cercopithecus monkeys in West African forests. In Gautier-Hion, A., Boulière, F., Gautier, J. P., and Kingdon, J. (eds.), A Primate Radiation: Evolutionary Biology of the African Guenons. Cambridge University Press, Cambridge, pp. 79–103.Google Scholar
  39. Oates, J. F., White, D., Gadsby, E. L., and Bisong, P. O. (1990). Cross River National Park (Okwangwo Division), Feasibility Study: Appendix 1. WWF, U.K.Google Scholar
  40. Olsen, G., Matsuda, J., Hagstrom, R., and Overbeek, R. (1994). FastDNAml: A tool for construction of phylogenetic trees of DNA sequences using maximum likelihood. Comput. Appl. Biosci. 10: 41–48.PubMedGoogle Scholar
  41. Prescott, J., Rapley, W. A., and Joseph, M. M. (1996). Status and conservation of chimpanzee and gorilla in Cameroon. Primate Cons. 14–15: 7–12.Google Scholar
  42. Shea, B. T., and Coolidge, H. J. (1988). Craniometric differentiation and systematics in the genus. Pan. J. Hum. Evol. 17: 671–685.CrossRefGoogle Scholar
  43. Stone, A. C., Griffiths, R. C., Zegura, S. L., and Hammer, M. F. (2002). High levels of Y-chromosome nucleotide diversity in the genus. Pan. Proc. Natl. Acad. Sci. USA 99(1): 43–48.CrossRefGoogle Scholar
  44. Swofford, D. L. (2002). PAUP*: Phylogenetic Analysis Using Parsimony. Version 4.0b10. Sinaeur Associates, Sunderland, MA.Google Scholar
  45. Tamura, K., and Nei, M. (1993). Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol. Biol. Evol. 10(3): 512–526.PubMedGoogle Scholar
  46. Taylor, A. B., and Groves, C. P. (2003). Patterns of mandibular variation in Pan and Gorilla and implications for African ape taxonomy. J. Hum. Evol. 44(5): 529–561.PubMedCrossRefGoogle Scholar
  47. Teleki, G. (1989). Population status of wild chimpanzees (Pan troglodytes) and threats to survival. In Heltne, P. G., and Marquardt L. A. (eds.), Understanding Chimpanzees. Harvard University Press, Cambridge, MA, pp. 312–353.Google Scholar
  48. Thalmann, O., Hebler, J., Poinar, H. N., Paabo, S., and Vigilant, L. (2004). Unreliable mtDNA data due to nuclear insertions: A cautionary tale from analysis of humans and other great apes. Mol. Ecol. 13(2): 321–335.PubMedCrossRefGoogle Scholar
  49. Tourmen, Y., Baris, O., Dessen, P., Jacques, C., Malthiery, Y., and Reynier, P. (2002). Structure and chromosomal distribution of human mitochondrial pseudogenes. Genomics 80(1): 71–77.PubMedCrossRefGoogle Scholar
  50. Vignaud, P., Duringer, P., Mackaye, H. T., Likius, A., Blondel, C., Boisserie, J. R., De Bonis, L., Eisenmann, V., Etienne, M. E., Geraads, D., et al. (2002). Geology and palaeontology of the Upper Miocene Toros-Menalla hominid locality, Chad. Nature 418(6894): 152–155.Google Scholar
  51. Wildman, D. E., Uddin, M., Liu, G., Grossman, L. I., and Goodman, M. (2003). Implications of natural selection in shaping 99.4% nonsynonymous DNA identity between humans and chimpanzees: enlarging genus Homo. Proc. Natl. Acad. Sci. USA 100(12): 7181–7188.Google Scholar

Copyright information

© Springer Science+Business Media, Inc. 2006

Authors and Affiliations

  • Mary Katherine Gonder
    • 1
    • 2
  • Todd R. Disotell
    • 3
  • John F. Oates
    • 2
  1. 1.Department of BiologyUniversity of MarylandCollege ParkUSA
  2. 2.Department of Anthropology, Hunter College and Graduate CenterCity University of New YorkNew YorkUSA
  3. 3.Department of AnthropologyNew York UniversityNew YorkUSA

Personalised recommendations