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

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Abstract

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.

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References

  • 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bandelt, H. J., Forster, P., & Rohl, A. (1999). Median-joining networks for inferring intraspecific phylogenies. Molecular Biology and Evolution, 16, 37–48.

    Article  CAS  PubMed  Google Scholar 

  • Beerli, P. (2006). Comparison of Bayesian and maximum likelihood inference of population genetic parameters. Bioinformatics, 22(3), 341–345.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Boesch, C. (1991). The effects of leopard predation on grouping patterns in forest chimpanzees. Behaviour, 117(3), 220–241.

    Article  Google Scholar 

  • Boesch, C. (2009). The real chimpanzee: Sex strategies in the forest. Cambridge: Cambridge University Press.

    Book  Google Scholar 

  • Boesch, C., & Boesch-Achermann, H. (2000). The chimpanzees of the Taï Forest: Behavioural ecology and evolution. Oxford: Oxford University Press.

    Google Scholar 

  • Boesch, C., Hohmann, G., & Marchant, L. F. (2002). Behavioural diversity in chimpanzees and bonobos. Cambridge: Cambridge University Press.

    Book  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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 

  • 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 

  • 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.

    Article  Google Scholar 

  • 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.

    Chapter  Google Scholar 

  • 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 

  • 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.

    Article  Google Scholar 

  • 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 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • Erler, A., Stoneking, M., & Kayser, M. (2004). Development of Y-chromosomal microsatellite markers for nonhuman primates. Molecular Ecology, 13(10), 2921–2930.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Goodall, J. (1986). The chimpanzees of Gombe: Patterns of behavior. Cambridge: Belknap Press of Harvard University Press.

    Google Scholar 

  • 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 

  • Haffer, J. (1969). Speciation in Amazon forest birds. Science, 165, 131–137.

    Article  CAS  PubMed  Google Scholar 

  • Haffer, J. (2008). Hypotheses to explain the origin of species in Amazonia. Brazilian Journal of Biology, 68(4), 917–947.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Kalinowski, S. T. (2004). Do polymorphic loci require large sample sizes to estimate genetic distances? Heredity, 94(1), 33–36.

    Article  CAS  Google Scholar 

  • Kummer, H. (1971). Primate societies: Group techniques of ecological adaptation. Chicago and New York: Aldine and Atherton.

    Google Scholar 

  • 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.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • Lawson Handley, L. J., & Perrin, N. (2007). Advances in our understanding of mammalian sex-biased dispersal. Molecular Ecology, 16(8), 1559–1578.

    Article  CAS  PubMed  Google Scholar 

  • Lehmann, J., & Boesch, C. (2008). Sexual differences in chimpanzee sociality. International Journal of Primatology, 29(1), 65–81.

    Article  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • Maisels, F. (2005). Mbam Djerem National Park, Cameroon: at the forest’s edge. Canopee, 27, 2–6.

    Google Scholar 

  • Manly, B. F. J. (2006). Randomization, bootstrap and Monte Carlo methods in biology (Vol. 70). Boca Raton: Chapman & Hall/CRC Press.

    Google Scholar 

  • Marshall, A., & Wrangham, R. W. (2007). Evolutionary consequences of fallback foods. International Journal of Primatology, 28(6), 1219–1235.

    Article  Google Scholar 

  • Mayr, E., & O'Hara, R. J. (1986). The biogeographic evidence supporting the Pleistocene forest refuge hypothesis. Evolution, 40(1), 55–67.

    Article  PubMed  Google Scholar 

  • 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.

    Article  Google Scholar 

  • McGrew, W. C., Marchant, L. F., & Nishida, T. (1996). Great ape societies. Cambridge: Cambridge University Press.

    Book  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Nishida, T. (1968). The social group of wild chimpanzees in the Mahale Mountains. Primates, 9(3), 167–224.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  PubMed  PubMed Central  Google Scholar 

  • Slatkin, M. (1995). A measure of population subdivision based on microsatellite allele frequencies. Genetics, 139(1), 457–462.

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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 

  • 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Taylor, H. R. (2015). The use and abuse of genetic marker-based estimates of relatedness and inbreeding. Ecology and Evolution, 5(15), 3140–3150.

    Article  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Wang, J. (2007). Triadic IBD coefficients and applications to estimating pairwise relatedness. Genetical Research, 89(3), 135–153.

    Article  CAS  PubMed  Google Scholar 

  • Wang, J. (2011). COANCESTRY: A program for simulating, estimating and analysing relatedness and inbreeding coefficients. Molecular Ecology Resources, 11(1), 141–145.

    Article  PubMed  Google Scholar 

  • White, F. (1983). The vegetation of Africa. Paris: UNESCO.

    Google Scholar 

  • 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 

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Acknowledgments

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.

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Mitchell, M.W., Locatelli, S., Abwe, E.E. et al. Male-Driven Differences in Chimpanzee (Pan troglodytes) Population Genetic Structure Across Three Habitats in Cameroon and Nigeria. Int J Primatol 39, 581–601 (2018). https://doi.org/10.1007/s10764-018-0053-7

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