International Journal of Primatology

, Volume 39, Issue 4, pp 581–601 | Cite as

Male-Driven Differences in Chimpanzee (Pan troglodytes) Population Genetic Structure Across Three Habitats in Cameroon and Nigeria

  • Matthew W. MitchellEmail author
  • Sabrina Locatelli
  • Ekwoge E. Abwe
  • Lora Ghobrial
  • Mary Katherine Gonder


Complex ecological pressures affect the social dynamics of many primate species, but it is unclear how they affect primate speciation. Molecular tools are often used to answer questions about the evolutionary histories and social systems of primates. Mitochondrial DNA (mtDNA), in particular, is frequently used to answer many of these questions, but because it is passed from mothers to offspring it reveals only the histories of females. In many species, including chimpanzees, females generally disperse from their natal groups while males are philopatric, and thus differences in dispersal patterns likely leave different signatures in the genome. We previously analyzed samples from 187 unrelated male and female chimpanzees in Nigeria and Cameroon using 21 autosomal microsatellites and mtDNA sequences. Here, we examine the contributions of males and females in shaping the genetic history of these chimpanzees by genotyping a subset of 56 males at 12 Y-chromosome microsatellites. We found that Y-chromosome population structure differed from the results of analysis of mtDNA haplotypes. The results also revealed that males in rainforest habitats (Guinean and Congolian rainforests) are more closely related to one another than those inhabiting the savanna-woodland mosaic ecotone in central Cameroon. In contrast, the pattern of female relatedness did not differ across habitats. We hypothesize that these differences in population structure and patterns of relatedness among males in different habitat types may be due to differences in the community dynamics of chimpanzees in the ecotone vs. rainforests, and that these factors contribute to making Cameroon an engine of diversification for chimpanzees. Broadly, these results demonstrate the importance of habitat variation in shaping social systems, population genetics, and primate speciation.


Cameroon Chimpanzee Genetics Microsatellites Population structure Y-chromosome 



We thank the governments of Cameroon and Nigeria for permission to conduct this research. We thank the Zoological Society of San Diego, the Ebo Forest Research Project, and the Wildlife Conservation Society for their support in Cameroon. We thank Beatrice Hahn, Martine Peeters, Bethan Morgan, Aaron Nicholas, and Amy Pokempner for contributing samples. We also thank Adam Freedman, Jeremy Kirchman, George Robinson, Paul Sesink Clee, Caro-Beth Stewart, Henri Thomassen, Anthony Di Fiore, the editor, and the anonymous reviewers for assistance with analyses and helpful comments on drafts of the manuscript. National Science Foundation awards 0755823 and 1243524 (to M. K. Gonder) and funding from the University at Albany – State University of New York (to M. K. Gonder) supported this work. M. W. Mitchell and M. K. Gonder designed the research. M. W. Mitchell, S. Locatelli, L. Ghobrial, and M. K. Gonder performed research. M. W. Mitchell analyzed the data. M. W. Mitchell, S. Locatelli, E. E. Abwe, and M. K. Gonder wrote the article. All authors read and approved the final manuscript.

Supplementary material

10764_2018_53_MOESM1_ESM.xlsx (39 kb)
ESM 1 (XLSX 39 kb)
10764_2018_53_MOESM2_ESM.docx (8.1 mb)
ESM 2 (DOCX 8298 kb)


  1. Arandjelovic, M., Head, J., Rabanal, L. I., Schubert, G., Mettke, E., et al (2011). Non-invasive genetic monitoring of wild central chimpanzees. PLoS One, 6(3), e14761.PubMedPubMedCentralCrossRefGoogle Scholar
  2. Bandelt, H. J., Forster, P., & Rohl, A. (1999). Median-joining networks for inferring intraspecific phylogenies. Molecular Biology and Evolution, 16, 37–48.PubMedCrossRefGoogle Scholar
  3. Beerli, P. (2006). Comparison of Bayesian and maximum likelihood inference of population genetic parameters. Bioinformatics, 22(3), 341–345.PubMedCrossRefGoogle Scholar
  4. Beerli, P., & Felsenstein, J. (2001). Maximum likelihood estimation of a migration matrix and effective population sizes in n subpopulations by using a coalescent approach. Proceedings of the National Academy of Sciences of the United States of America, 98(8), 4563–4568.PubMedPubMedCentralCrossRefGoogle Scholar
  5. Boesch, C. (1991). The effects of leopard predation on grouping patterns in forest chimpanzees. Behaviour, 117(3), 220–241.CrossRefGoogle Scholar
  6. Boesch, C. (2009). The real chimpanzee: Sex strategies in the forest. Cambridge: Cambridge University Press.CrossRefGoogle Scholar
  7. Boesch, C., & Boesch-Achermann, H. (2000). The chimpanzees of the Taï Forest: Behavioural ecology and evolution. Oxford: Oxford University Press.Google Scholar
  8. Boesch, C., Hohmann, G., & Marchant, L. F. (2002). Behavioural diversity in chimpanzees and bonobos. Cambridge: Cambridge University Press.CrossRefGoogle Scholar
  9. Boesch, C., Kohou, G., Néné, H., & Vigilant, L. (2006). Male competition and paternity in wild chimpanzees of the Taï forest. American Journal of Physical Anthropology, 130(1), 103–115.PubMedCrossRefGoogle Scholar
  10. Boesch, C., Crockford, C., Herbinger, I., Wittig, R., Moebius, Y., & Normand, E. (2008). Intergroup conflicts among chimpanzees in Taï National Park: Lethal violence and the female perspective. American Journal of Primatology, 70(6), 519–532.PubMedCrossRefGoogle Scholar
  11. Bonin, A., Bellemain, E., Bronken Eidesen, P., Pompanon, F., Brochmann, C., & Taberlet, P. (2004). How to track and assess genotyping errors in population genetics studies. Molecular Ecology, 13(11), 3261–3273.PubMedCrossRefGoogle Scholar
  12. Bradley, B. J., Chambers, K. E., & Vigilant, L. (2001). Accurate DNA-based sex identification of apes using non-invasive samples. Conservation Genetics, 2, 179–181.CrossRefGoogle Scholar
  13. Caldecott, J. O., & Miles, L. (2005). World atlas of great apes and their conservation. Berkeley: University of California Press, in association with UNEP-WCMC, Cambridge, UK.Google Scholar
  14. Chapman, C. A., White, F. J., & Wrangham, R. W. (1994). Party size in chimpanzees and bonobos: A reevaluation of theory based on two similarly forested sites. In R. W. Wrangham, W. C. McGrew, F. B. deWaal, & P. G. Heltne (Eds.), Chimpanzee cultures (pp. 41–58). Cambridge: Harvard University Press in cooperation with the Chicago Academy of Sciences.Google Scholar
  15. Chapman, C. A., Wrangham, R. W., & Chapman, L. J. (1995). Ecological constraints on group size: an analysis of spider monkey and chimpanzee subgroups. Behavioral Ecology and Sociobiology, 36(1), 59–70.CrossRefGoogle Scholar
  16. Di Fiore, A. (2009). Genetic approaches to the study of dispersal and kinship in new world primates. In P. A. Garber, A. Estrada, J. C. Bicca-Marques, E. W. Heymann, & K. B. Strier (Eds.), South American primates: Comparative perspectives in the study of behavior, ecology, and conservation (pp. 211–250). New York: Springer Science+Business Media.CrossRefGoogle Scholar
  17. Di Fiore, A. (2012). Genetic consequences of primate social organization. In J. C. Mitani, J. Call, P. M. Kappeler, R. A. Palombit, & J. B. Silk (Eds.), The evolution of primate societies (pp. 269–292). Chicago and London: University of Chicago Press.Google Scholar
  18. Emery Thompson, M., Newton-Fisher, N. E., & Reynolds, V. (2006). Probable community transfer of parous adult female chimpanzees in the Budongo Forest, Uganda. International Journal of Primatology, 27(6), 1601–1617.CrossRefGoogle Scholar
  19. Endler, J. A. (1982). Pleistocene forest refuges: Fact or fancy? In G. T. Prance (Ed.), Biological diversification in the tropics (pp. 641–657). New York: Columbia Univeristy Press.Google Scholar
  20. Eriksson, J., Siedel, H., Lukas, D., Kayser, M., Erler, A., et al (2006). Y-chromosome analysis confirms highly sex-biased dispersal and suggests a low male effective population size in bonobos (Pan paniscus). Molecular Ecology, 15(4), 939–949.PubMedCrossRefGoogle Scholar
  21. Erler, A., Stoneking, M., & Kayser, M. (2004). Development of Y-chromosomal microsatellite markers for nonhuman primates. Molecular Ecology, 13(10), 2921–2930.PubMedCrossRefGoogle Scholar
  22. Excoffier, L., & Lischer, H. E. L. (2010). Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Molecular Ecology Resources, 10(3), 564–567.PubMedCrossRefGoogle Scholar
  23. Farr, T. G., Rosen, P. A., Caro, E., Crippen, R., Duren, R., et al (2007). The shuttle radar topography mission. Reviews of Geophysics, 45(2), RG2004.Google Scholar
  24. Freedman, A. H., Thomassen, H. A., Buermann, W., & Smith, T. B. (2010). Genomic signals of diversification along ecological gradients in a tropical lizard. Molecular Ecology, 19(17), 3773–3788.PubMedCrossRefGoogle Scholar
  25. Gerloff, U., Hartung, B., Fruth, B., Hohmann, G., & Tautz, D. (1999). Intracommunity relationships, dispersal pattern and paternity success in a wild living community of Bonobos (Pan paniscus) determined from DNA analysis of faecal samples. Proceedings of the Royal Society of London B: Biological Sciences, 266(1424), 1189–1195.CrossRefGoogle Scholar
  26. Goldstein, D. B., Ruiz Linares, A., Cavalli-Sforza, L. L., & Feldman, M. W. (1995). Genetic absolute dating based on microsatellites and the origin of modern humans. Proceedings of the National Academy of Sciences of the United States of America, 92(15), 6723–6727.PubMedPubMedCentralCrossRefGoogle Scholar
  27. Gonder, M. K., Oates, J. F., Disotell, T. R., Forstner, M. R., Morales, J. C., & Melnick, D. J. (1997). A new west African chimpanzee subspecies? Nature, 388(6640), 337.PubMedCrossRefGoogle Scholar
  28. Gonder, M. K., Disotell, T. R., & Oates, J. F. (2006). New genetic evidence on the evolution of chimpanzee populations, and implications for taxonomy. International Journal of Primatology, 27(4), 1103–1127.CrossRefGoogle Scholar
  29. Gonder, M. K., Locatelli, S., Ghobrial, L., Mitchell, M. W., Kujawski, J. T., et al (2011). Evidence from Cameroon reveals differences in the genetic structure and histories of chimpanzee populations. Proceedings of the National Academy of Sciences of the United States of America, 108(12), 4766–4771.PubMedPubMedCentralCrossRefGoogle Scholar
  30. Goodall, J. (1986). The chimpanzees of Gombe: Patterns of behavior. Cambridge: Belknap Press of Harvard University Press.Google Scholar
  31. Goodall, J., Bandora, A., Bergmann, E., Busse, C., Matama, H., et al (1979). Intercommunity interactions in the chimpanzee population of the Gombe National Park. The Great Apes, 5, 13–53.Google Scholar
  32. Haffer, J. (1969). Speciation in Amazon forest birds. Science, 165, 131–137.PubMedCrossRefGoogle Scholar
  33. Haffer, J. (2008). Hypotheses to explain the origin of species in Amazonia. Brazilian Journal of Biology, 68(4), 917–947.CrossRefGoogle Scholar
  34. Hammond, R. L., Lawson Handley, L. J., Winney, B. J., Bruford, M. W., & Perrin, N. (2006). Genetic evidence for female-biased dispersal and gene flow in a polygynous primate. Proceedings of the Royal Society of London B: Biological Sciences, 273(1585), 479–484.CrossRefGoogle Scholar
  35. Hansen, M. C., Defries, R. S., Townshend, J. R. G., & Sohlberg, R. (2000). Global land cover classification at 1 km spatial resolution using a classification tree approach. International Journal of Remote Sensing, 21(6–7), 1331–1364.CrossRefGoogle Scholar
  36. Hapke, A., Zinner, D., & Zischler, H. (2001). Mitochondrial DNA variation in Eritrean hamadryas baboons (Papio hamadryas hamadryas): Life history influences population genetic structure. Behavioral Ecology and Sociobiology, 50(6), 483–492.CrossRefGoogle Scholar
  37. Herbinger, I., Boesch, C., & Rothe, H. (2001). Territory characteristics among three neighboring chimpanzee communities in the Taï National Park, Côte d'Ivoire. International Journal of Primatology, 22(2), 143–167.CrossRefGoogle Scholar
  38. Hernandez-Aguilar, R. A. (2009). Chimpanzee nest distribution and site reuse in a dry habitat: Implications for early hominin ranging. Journal of Human Evolution, 57(4), 350–364.PubMedCrossRefGoogle Scholar
  39. Hijmans, R. J., Cameron, S. E., Parra, J. L., Jones, P. G., & Jarvis, A. (2005). Very high resolution interpolated climate surfaces for global land areas. International Journal of Climatology, 25(15), 1965–1978.CrossRefGoogle Scholar
  40. Kalinowski, S. T. (2004). Do polymorphic loci require large sample sizes to estimate genetic distances? Heredity, 94(1), 33–36.CrossRefGoogle Scholar
  41. Kummer, H. (1971). Primate societies: Group techniques of ecological adaptation. Chicago and New York: Aldine and Atherton.Google Scholar
  42. Langergraber, K. E., Siedel, H., Mitani, J. C., Wrangham, R. W., Reynolds, V., et al (2007). The genetic signature of sex-biased migration in patrilocal chimpanzees and humans. PLoS One, 2(10), e973.PubMedPubMedCentralCrossRefGoogle Scholar
  43. Langergraber, K. E., Rowney, C., Crockford, C., Wittig, R., Zuberbühler, K., & Vigilant, L. (2014a). Genetic analyses suggest no immigration of adult females and their offspring into the Sonso community of chimpanzees in the Budongo Forest reserve, Uganda. American Journal of Primatology, 76(7), 640–648.PubMedCrossRefGoogle Scholar
  44. Langergraber, K. E., Rowney, C., Schubert, G., Crockford, C., Hobaiter, C., et al (2014b). How old are chimpanzee communities? Time to the most recent common ancestor of the Y-chromosome in highly patrilocal societies. Journal of Human Evolution, 69, 1–7.PubMedCrossRefGoogle Scholar
  45. Lawson Handley, L. J., & Perrin, N. (2007). Advances in our understanding of mammalian sex-biased dispersal. Molecular Ecology, 16(8), 1559–1578.PubMedCrossRefGoogle Scholar
  46. Lehmann, J., & Boesch, C. (2008). Sexual differences in chimpanzee sociality. International Journal of Primatology, 29(1), 65–81.PubMedPubMedCentralCrossRefGoogle Scholar
  47. Lehmann, J., Korstjens, A. H., & Dunbar, R. I. M. (2007). Fission–fusion social systems as a strategy for coping with ecological constraints: a primate case. Evolutionary Ecology, 21(5), 613–634.CrossRefGoogle Scholar
  48. Lehner, B., Verdin, K., & Jarvis, A. (2008). New global hydrography derived from spaceborne elevation data. Eos, Transactions of the American Geophysical Union, 89(10), 93–94.CrossRefGoogle Scholar
  49. Long, D. G., Drinkwater, M. R., Holt, B., Saatchi, S., & Bertoia, C. (2001). Global ice and land climate studies using scatterometer image data. Eos, Transactions of the American Geophysical Union, 82(43), 503.CrossRefGoogle Scholar
  50. Lukas, D., Reynolds, V., Boesch, C., & Vigilant, L. (2005). To what extent does living in a group mean living with kin? Molecular Ecology, 14(7), 2181–2196.PubMedCrossRefGoogle Scholar
  51. Maisels, F. (2005). Mbam Djerem National Park, Cameroon: at the forest’s edge. Canopee, 27, 2–6.Google Scholar
  52. Manly, B. F. J. (2006). Randomization, bootstrap and Monte Carlo methods in biology (Vol. 70). Boca Raton: Chapman & Hall/CRC Press.Google Scholar
  53. Marshall, A., & Wrangham, R. W. (2007). Evolutionary consequences of fallback foods. International Journal of Primatology, 28(6), 1219–1235.CrossRefGoogle Scholar
  54. Mayr, E., & O'Hara, R. J. (1986). The biogeographic evidence supporting the Pleistocene forest refuge hypothesis. Evolution, 40(1), 55–67.PubMedCrossRefGoogle Scholar
  55. McGrew, W. C., Baldwin, P. J., & Tutin, C. E. G. (1981). Chimpanzees in a hot, dry and open habitat: Mt. Assirik, Senegal, West Africa. Journal of Human Evolution, 10(3), 227–244.CrossRefGoogle Scholar
  56. McGrew, W. C., Marchant, L. F., & Nishida, T. (1996). Great ape societies. Cambridge: Cambridge University Press.CrossRefGoogle Scholar
  57. McGrew, W. C., Ensminger, A. L., Marchant, L. F., Pruetz, J. D., & Vigilant, L. (2004). Genotyping aids field study of unhabituated wild chimpanzees. American Journal of Primatology, 63(2), 87–93.PubMedCrossRefGoogle Scholar
  58. Melnick, D. J., & Hoelzer, G. A. (1992). Differences in male and female macaque dispersal lead to contrasting distributions of nuclear and mitochondrial DNA variation. International Journal of Primatology, 13(4), 379–393.CrossRefGoogle Scholar
  59. Mitchell, M. W., Locatelli, S., Ghobrial, L., Pokempner, A. A., Sesink Clee, P. R., et al (2015a). The population genetics of wild chimpanzees in Cameroon and Nigeria suggests a positive role for selection in the evolution of chimpanzee subspecies. BMC Evolutionary Biology, 15, 3.PubMedPubMedCentralCrossRefGoogle Scholar
  60. Mitchell, M. W., Locatelli, S., Sesink Clee, P. R., Thomassen, H. A., & Gonder, M. K. (2015b). Environmental variation and rivers govern the structure of chimpanzee genetic diversity in a biodiversity hotspot. BMC Evolutionary Biology, 15, 1.PubMedPubMedCentralCrossRefGoogle Scholar
  61. Moore, D. L., Langergraber, K. E., & Vigilant, L. (2015). Genetic analyses suggest male philopatry and territoriality in savanna-woodland chimpanzees (Pan troglodytes schweinfurthii) of Ugalla, Tanzania. International Journal of Primatology, 36(2), 377–397.CrossRefGoogle Scholar
  62. Morgan, B., Adeleke, A., Bassey, T., Bergl, R., Dunn, A., et al. (2011). Regional action plan for the conservation of the Nigeria-Cameroon chimpanzee (Pan troglodytes ellioti). Gland, Switzerland and San Diego, CA, USA: IUCN/SSC Primate Specialist Group and Zoological Society of San Diego, CA, USA.Google Scholar
  63. 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(5176), 1193–1201.PubMedCrossRefGoogle Scholar
  64. Myneni, R. B., Hoffman, S., Knyazikhin, Y., Privette, J. L., Glassy, J., et al (2002). Global products of vegetation leaf area and fraction absorbed PAR from year one of MODIS data. Remote Sensing of Environment, 83(1–2), 214–231.CrossRefGoogle Scholar
  65. Nishida, T. (1968). The social group of wild chimpanzees in the Mahale Mountains. Primates, 9(3), 167–224.CrossRefGoogle Scholar
  66. Nishida, T., & Hiraiwa-Hasegawa, M. (1985). Responses to a stranger mother-son pair in the wild chimpanzee: a case report. Primates, 26(1), 1–13.CrossRefGoogle Scholar
  67. Oates, J. F., Groves, C. P., & Jenkins, P. D. (2009). The type locality of Pan troglodytes vellerosus (Gray, 1862), and implications for the nomenclature of West African chimpanzees. Primates, 50(1), 78–80.PubMedCrossRefGoogle Scholar
  68. Ogawa, H., Idani, G., Moore, J., Pintea, L., & Hernandez-Aguilar, A. (2007). Sleeping parties and nest distribution of chimpanzees in the savanna woodland, Ugalla, Tanzania. International Journal of Primatology, 28(6), 1397–1412.CrossRefGoogle Scholar
  69. Potts, K. B., Baken, E., Levang, A., & Watts, D. P. (2016). Ecological factors influencing habitat use by chimpanzees at Ngogo, Kibale National Park, Uganda. American Journal of Primatology, 78(4), 432–440.PubMedCrossRefGoogle Scholar
  70. Pruetz, J. D., & Bertolani, P. (2009). Chimpanzee (Pan troglodytes verus) behavioral responses to stresses associated with living in a savanna-mosaic environment: implications for hominin adaptations to open habitats. PaleoAnthropology, 2009, 252–262.CrossRefGoogle Scholar
  71. Reynolds, J., Weir, B. S., & Cockerham, C. C. (1983). Estimation of the coancestry coefficient: basis for a short-term genetic distance. Genetics, 105(3), 767–779.PubMedPubMedCentralGoogle Scholar
  72. Schubert, G., Stoneking, C. J., Arandjelovic, M., Boesch, C., Eckhardt, N., et al (2011). Male-mediated gene flow in patrilocal primates. PLoS One, 6(7), e21514.PubMedPubMedCentralCrossRefGoogle Scholar
  73. Sesink Clee, P. R., Abwe, E. E., Ambahe, R. D., Anthony, N. M., Fotso, R., et al (2015). Chimpanzee genetic structure in Cameroon and Nigeria is associated with habitat variation that may be lost under climate change. BMC Evolutionary Biology, 15, 2.PubMedPubMedCentralCrossRefGoogle Scholar
  74. Slatkin, M. (1995). A measure of population subdivision based on microsatellite allele frequencies. Genetics, 139(1), 457–462.PubMedPubMedCentralGoogle Scholar
  75. Smith, T. B., Wayne, R. K., Girman, D. J., & Bruford, M. W. (1997). A role for ecotones in generating rainforest biodiversity. Science, 276(5320), 1855–1857.CrossRefGoogle Scholar
  76. Stone, A. C., Griffiths, R. C., Zegura, S. L., & Hammer, M. F. (2002). High levels of Y-chromosome nucleotide diversity in the genus Pan. Proceedings of the National Academy of Sciences of the United States of the America, 99(1), 43–48.CrossRefGoogle Scholar
  77. Stumpf, R. (2007). Chimpanzees and bonobos: Diversity within and between species. In C. J. Campbell, A. Fuentes, K. C. MacKinnon, M. Panger, & S. K. Bearder (Eds.), Primates in perspective (pp. 321–344). New York: Oxford University Press.Google Scholar
  78. Szpiech, Z. A., Jakobsson, M., & Rosenberg, N. A. (2008). ADZE: a rarefaction approach for counting alleles private to combinations of populations. Bioinformatics, 24(21), 2498–2504.PubMedPubMedCentralCrossRefGoogle Scholar
  79. Taylor, H. R. (2015). The use and abuse of genetic marker-based estimates of relatedness and inbreeding. Ecology and Evolution, 5(15), 3140–3150.PubMedPubMedCentralCrossRefGoogle Scholar
  80. Tishkoff, S. A., Gonder, M. K., Henn, B. M., Mortensen, H., Knight, A., et al (2007). History of click-speaking populations of Africa inferred from mtDNA and Y chromosome genetic variation. Molecular Biology and Evolution, 24(10), 2180–2195.PubMedCrossRefGoogle Scholar
  81. Tishkoff, S. A., Reed, F. A., Friedlaender, F. R., Ehret, C., Ranciaro, A., et al (2009). The genetic structure and history of Africans and African Americans. Science, 324(5930), 10.CrossRefGoogle Scholar
  82. Tutin, C. E. G., Fernandez, M., Rogers, M. E., Williamson, E. A., McGrew, W. C., et al (1991). Foraging profiles of sympatric lowland gorillas and chimpanzees in the Lope reserve, Gabon [and Discussion]. Philosophical Transactions of the Royal Society of London B: Biological Sciences, 334(1270), 179–186.PubMedCrossRefGoogle Scholar
  83. Tutin, C. E. G., Ham, R. M., White, L. J. T., & Harrison, M. J. S. (1997a). The primate community of the Lope reserve, Gabon: diets, responses to fruit scarcity, and effects on biomass. American Journal of Primatology, 42(1), 1–24.CrossRefPubMedGoogle Scholar
  84. Tutin, C. E. G., White, L. J. T., & Mackanga-Missandzou, A. (1997b). The use by rain forest mammals of natural forest fragments in an equatorial African savanna. Conservation Biology, 11(5), 1190–1203.CrossRefGoogle Scholar
  85. Wang, J. (2007). Triadic IBD coefficients and applications to estimating pairwise relatedness. Genetical Research, 89(3), 135–153.PubMedCrossRefGoogle Scholar
  86. Wang, J. (2011). COANCESTRY: A program for simulating, estimating and analysing relatedness and inbreeding coefficients. Molecular Ecology Resources, 11(1), 141–145.PubMedCrossRefGoogle Scholar
  87. White, F. (1983). The vegetation of Africa. Paris: UNESCO.Google Scholar
  88. Wrangham, R. W., Chapman, C. A., Clark-Acadi, A. P., & Isabirye-Basuta, G. (1996). Social ecology of Kanyawara chimpanzees: Implications for understanding the costs of great ape groups. In W. C. McGrew, L. F. Marchant, & T. Nishida (Eds.), Great ape societies (pp. 81–98). Cambridge: Cambridge University Press.Google Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  • Matthew W. Mitchell
    • 1
    • 2
    • 3
    Email author
  • Sabrina Locatelli
    • 2
    • 4
  • Ekwoge E. Abwe
    • 1
    • 5
    • 6
  • Lora Ghobrial
    • 2
    • 7
  • Mary Katherine Gonder
    • 1
    • 2
  1. 1.Department of BiologyDrexel UniversityPhiladelphiaUSA
  2. 2.Department of Biological SciencesUniversity at Albany – State University of New YorkAlbanyUSA
  3. 3.Department of BiologyUniversity of PennsylvaniaPhiladelphiaUSA
  4. 4.Unité Mixte Internationale 233, Institut de Recherche pour le Développement, INSERM U1175, and University of MontpellierMontpellierFrance
  5. 5.Ebo Forest Research Project, BP 3055YaoundéCameroon
  6. 6.Zoological Society of San DiegoInstitue for Conservation ResearchEscondidoUSA
  7. 7.Forensic Biology SectionNorth Carolina State Crime LaboratoryRaleighUSA

Personalised recommendations