International Journal of Primatology

, Volume 40, Issue 1, pp 28–52 | Cite as

Mitochondrial DNA Analyses of Cercopithecus Monkeys Reveal a Localized Hybrid Origin for C. mitis doggetti in Gombe National Park, Tanzania

  • Kate M. DetwilerEmail author


In recent years, hybridization has gained recognition as an important creative force in primate evolution. The exchange of genetic material between species provides genetic novelty on which evolutionary forces, such as natural selection, may act. The guenon radiation (Tribe Cercopithecini) is known for numerous cases of contemporary hybridization—in the wild and captivity—between broadly sympatric species. Interspecific hybrids are viable, and field studies report fertile hybrid females. Despite being a well-documented phenomenon, hybridization among wild guenons is relatively rare and sporadic. An exception is the long-standing hybridization between Cercopithecus mitis doggetti and C. ascanius schmidti in Gombe National Park, Tanzania, where hybrids comprise a significant proportion of the breeding population. Here, I used mitochondrial loci to conduct a genetic survey of the Gombe population and examine the extent and direction of gene flow between the parental species. I extracted DNA from noninvasive fecal samples of unhabituated individuals (N = 144 individuals) with known phenotype and provenance. All parental phenotypes and hybrid individuals were identified in the field based on species specific pelage colors and patterns. Phylogenetic analyses of DNA sequences from inside and outside the hybrid zone show Gombe’s population of C. mitis doggetti is distinct from neighboring conspecific populations in having mitochondrial DNA of C. ascanius schmidti. All animals surveyed from the hybrid zone have one of two haplotypes of C. ascanius schmidti unique to Gombe. These results provide evidence of asymmetric introgressive hybridization between sympatric guenon species, a likely consequence of colonization patterns of the parental species during range expansions. The spatial distribution patterns of the two haplotypes imply that Gombe is a site of both historic and contemporary hybridization between sympatric guenons. The discovery of gene flow and ongoing hybridization between clearly defined species, ecologically distinct enough to coexist in broad sympatry, provides an ideal system to investigate speciation mechanisms in primate adaptive radiations.


Ecotone Guenon evolution Introgression Mosaic hybrid zone Natural hybridization 



I would like to thank Dr. Liliana Cortés-Ortiz for her invitation to participate in the IPS/ASP 2016 Primate Hybridization Symposium in Chicago, and for her continued support, and Drs. Christian Roos and Dietmar Zinner as editors for this special issue of International Journal of Primatology. I also thank two anonymous reviewers and Dr. Joanna M. Setchell for their comments and suggestions. I dedicate this article to my PhD advisor, Dr. Cliff Jolly; I think he anticipated the results long before I ran my first sample. This work was funded by a Faculty Research Seed Grant from the Division of Research, Florida Atlantic University (FAU), FAU’s Department of Anthropology, and doctoral dissertation research grants from the National Science Foundation (0424444), Leakey Foundation, and Wenner-Gren Foundation. I am grateful for research permissions to work in Gombe, Mahale, and Nyungwe National Parks from the governments of Tanzania (COSTECH, TAWIRI, TANAPA) and Rwanda (Rwanda Development Board, formerly ORTPN). I thank the wonderful field assistants who contributed to the field work at Gombe, Nyungwe, and Mahale National Parks, with special thanks to long-term field assistants James Gray, Mary Nkoranigwa, and Maneno I. Mpongo. The scientists and staff of the Gombe Stream Research Center (GSRC) have provided generous field support over the years at Gombe, especially Drs. Anthony Collins, Deus Mjungu, and Michael Wilson. I thank Dr. Beth Kaplin for assistance with research at Nyungwe NP. I also thank Sandra Almanza from the FAU Primatology Lab for her assistance with phylogenetic analysis and tree figures. Dr. Itzel Sifuentes-Romero provided assistance in the FAU Primatology Lab with the mtDNA cyt b locus. Maneno I. Mpongo, Elizabeth Tapanes, and Craig Ruaux contributed photographs. Jonas Borkholder and Rayan Alhawiti provided assistance with the map figures. L. Pintea provided ArcGIS shapefiles of the vegetation base map and Gombe National Park boundary for Fig. 7. Drs. A. Burrell, T. Disotell, N. Ting, and A. Tosi provided assistance with molecular protocols while I worked at the NYU Molecular Anthropology Lab.

Supplementary material

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  1. Abbott, R., Albach, D., Ansell, S., Arntzen, J. W., Baird, S. J., et al (2013). Hybridization and speciation. Journal of Evolutionary Biology, 26, 229–246.PubMedGoogle Scholar
  2. Alberts, S. C., & Altmann, J. (2001). Immigration and hybridization patterns of yellow and anubis baboons in and around Amboseli, Kenya. American Journal of Primatology, 53, 139–154.PubMedGoogle Scholar
  3. Aldrich-Blake, F. P. G. (1968). A fertile hybrid between two Cercopithecus species in the Budongo Forest, Uganda. Folia Primatologica, 9, 15–21.Google Scholar
  4. Alin, S. R., O’Reily, C. M., & Cohen, A. S. (2002). Effects of land-use change on aquatic biodiversity: A view from the paleorecord at Lake Tanganyika, East Africa. Geology, 30(12), 1143–1146.Google Scholar
  5. Allen, W. L., Stevens, M., & Higham, J. P. (2014). Character displacement of Cercopithecini primate visual signals. Nature Communications, 5, 4266.PubMedPubMedCentralGoogle Scholar
  6. Arnold, M. L., & Meyer, A. (2006). Natural hybridization in primates: One evolutionary mechanism. Zoology, 109(4), 261–276.PubMedGoogle Scholar
  7. Arnqvist, G., Dowling, D. K., Eady, P., Gay, L., Tregenza, T., et al (2014). The genetic architecture of metabolic rate: Environment specific epistasis between mitochondrial and nuclear genes in an insect. Evolution, 64, 3354–3363.Google Scholar
  8. Avise, J. C. (2004). Molecular markers, natural history, and evolution. Sunderland: Sinauer Associates.Google Scholar
  9. Barton, N. H., & Hewitt, G. M. (1985). Analysis of hybrid zones. Annual Review of Ecology and Systematics, 16, 113–148.Google Scholar
  10. Bensasson, D., Zhang, D., Hartl, D. L., & Hewitt, G. M. (2001). Mitochondrial pseudogenes: Evolution’s misplaced witnesses. Trends in Ecology & Evolution, 16(3), 314–321.Google Scholar
  11. Bergman, T. J. (2000). Mating behavior and reproductive success of hybrid male baboons (Papio hamadryas hamadryas × Papio hamadryas anubis). Ph.D. thesis, Washington University.Google Scholar
  12. Berlocher, S. H., & Howard, D. J. (1998). Endless forms: Species and speciation. New York: Oxford University Press.Google Scholar
  13. Bronikowski, A. M., Cords, M., Alberts, S. C., Altmann, J., Brockman, D. K., Fedigan, L. M., Pusey, A., Stoinski, T., Strier, K. B., & Morris, W. F. (2016). Female and male life tables for seven wild primate species. Scientific Data, 3, 160006.PubMedPubMedCentralGoogle Scholar
  14. Burrell, A. S., Jolly, C. J., Tosi, A. J., & Disotell, T. R. (2009). Mitochondrial evidence for the hybrid origin of the kipunji, Rungwecebus kipunji (Primates: Papionini). Molecular Phylogenetics and Evolution, 51, 340–348.PubMedGoogle Scholar
  15. Butynski, T. M., Kingdon, J., & Kalina, J. (2013). Mammals of Africa. In Primates (Vol. Vol. II). London: Bloomsbury.Google Scholar
  16. Canestrelli, D., Porretta, D., Lowe, W. H., Bisconti, R., Carere, C., & Nascetti, G. (2016). The tangled evolutionary legacies of range expansion and hybridization. Trends in Ecology & Evolution, 31(9), 677–688.Google Scholar
  17. Chapman, C. A., Chapman, L. J., Cords, M., Gathua, J. M., Gautier-Hion, A., et al (2002). Variation in the diets of Cercopithecus species: Differences within forests, among forests, and across species. In M. E. Glenn & M. Cords (Eds.), The guenons: Diversity and adaptation in African monkeys (pp. 325–350). New York: Kluwer Academic.Google Scholar
  18. Clutton-Brock, T. H., & Gillet, J. B. (1979). A survey of forest composition in the Gombe National Park, Tanzania. African Journal of Ecology, 17, 131–158.Google Scholar
  19. Cohen, A. S., Palacios-Fest, M. R., Msaky, E. S., Alin, S. R., McKee, B., O’Reilly, C. M., Dettman, D. L., Nkotagu, H., & Lezzar, K. E. (2005). Paleolimnological investigations of anthropogenic environmental change in Lake Tanganyika: IX. Summary of paleorecords of environmental change and catchment deforestation at Lake Tanganyika and impacts on the Lake Tanganyika ecosystem. Journal of Paleolimnology, 34(1), 125–145.Google Scholar
  20. Coleman, B. T., & Hill, R. A. (2014). Biogeographic variation in the diet and behavior of Cercopithecus mitis. Folia Primatologica, 85, 319–334.Google Scholar
  21. Collins, D. A., & McGrew, W. C. (1988). Habitats of three groups of chimpanzees (Pan troglodytes) in western Tanzania compared. Journal of Human Evolution, 17, 553–574.Google Scholar
  22. Colyn, M., Gautier-Hion, A., & Verheyen, W. (1991). A re-appraisal of a paleoenvironmental history in central Africa: Evidence for a major fluvial refuge in the Zaire Basin. Journal of Biogeography, 18, 403–407.Google Scholar
  23. Cords, M. (1987a). Mixed species association of Cercopithecus monkeys in the Kakamega forest. University of California Publications in. Zoology, 117, 1–109.Google Scholar
  24. Cords, M. (1987b). Forest guenons and patas monkeys: Male-male competition in one-male groups. In B. B. Smuts, D. L. Cheney, R. M. Seyfarth, R. W. Wrangham, & T. T. Struhsaker (Eds.), Primate societies (pp. 98–111). Chicago: University of Chicago Press.Google Scholar
  25. Cords, M. (1988). Mating systems of forest guenons: A preliminary review. In A. Gautier-Hion, F. Bourliere, J. P. Gautier, & J. Kingdon (Eds.), A primate radiate: Evolutionary biology of the African guenons (pp. 323–329). Cambridge: Cambridge University Press.Google Scholar
  26. Cords, M. (2002). Friendship among adult female blue monkeys (Cercopithecus mitis). Behaviour, 139, 291–314.Google Scholar
  27. Cords, M., & Sarmiento, E. (2013). Cercopithecus ascanius species profile. In T. M. Butynski, J. Kingdon, & J. Kalina (Eds.), The mammals of Africa, Vol. II: Primates. London: Bloomsbury.Google Scholar
  28. Cortés-Oritz, L., Duda, T. F., Canales-Espinosa, D., García-Orduña, F., Rodríguez-Luna, E., & Bermingham, E. (2007). Hybridization in large-bodied new world primates. Genetics, 176, 2421–2425.Google Scholar
  29. Cramer, E. R., Alund, M., McFarlane, S. E., Johnsen, A., & Qvranstrom, A. (2016). Females discriminate against heterospecific sperm in a natural hybrid zone. Evolution, 70(8), 1844–1855.PubMedGoogle Scholar
  30. Darriba, D., Taboada, G. L., Doallo, R., & Posada, D. (2012). jModel test 2: More models new heuristics and parallel computing. Nature Methods, 9, 772.PubMedPubMedCentralGoogle Scholar
  31. de Jong, Y. A., & Butynski, T. M. (2010). Three sykes’s monkey Cercopithecus mitis × vervet monkey Chlorocebus pygerythrus hybrids in Kenya. Primate Conservation, 25, 43–56.Google Scholar
  32. Detwiler, K. M. (2002). Hybridization between red-tailed monkeys (Cercopithecus Ascanius) and blue monkeys (C. mitis) in East African forests. In M. E. Glenn & M. Cords (Eds.), The guenons: Diversity and adaptation in African monkeys (pp. 79–97). New York: Kluwer Academic.Google Scholar
  33. Detwiler, K. M. (2010). Natural hybridization between Cercopithecus mitis × C. ascanius in Gombe National Park. Doctoral dissertation, New York University.Google Scholar
  34. Detwiler, K. M., Burrell, A. S., & Jolly, C. J. (2005). Conservation implications of hybridization in African cercopithecine monkeys. International Journal of Primatology, 26(3), 661–684.Google Scholar
  35. Disotell, T. R., & Raaum, R. L. (2002). Molecular timescale and gene tree incongruence in the guenons. In M. E. Glenn & M. Cords (Eds.), The guenons: Diversity and adaptation in African monkeys (pp. 27–36). New York: Kluwer Academic/Plenum.Google Scholar
  36. Dowling, T. E., & Secor, C. L. (1997). The role of hybridization and introgression in the diversification of animals. Annual Review of Ecology and Systematics, 28, 593–619.Google Scholar
  37. Dutrillaux, B., Muleris, M., & Conturier, J. (1988). Chromosomal evolution of Cercopithecinae. In A. Gautier-Hion, F. Bourlière, J.-P. Gautier, & J. Kingdon (Eds.), A primate radiation: Evolutionary biology of the African guenons (pp. 151–159). Cambridge: Cambridge University Press.Google Scholar
  38. Funk, D. J., & Omland, K. E. (2003). Species-level paraphyly and polyphyly: Frequency, causes, and consequences, with insights from animal mitochondrial DNA. Annual Review of Ecology and Systematics, 34, 397–423.Google Scholar
  39. Fuzessy, L. F., Silva, I. D., Malukiewicz, J., Silva, F. F. R., Ponzio, M. D., et al (2014). Morphological variation in wild marmosets (Callithrix penicillata and C. geoffroyi) and their hybrids. Evolutionary Biology, 41(3), 480–493.Google Scholar
  40. Gaubert, P., Njiokou, F., Ayodeji, O., Pagani, P., Dufour, S., et al (2014). Bushmeat genetics: Setting up a reference framework for the DNA typing of African forest bushmeat. Molecular Ecology Resources, 15, 633–651.PubMedGoogle Scholar
  41. Gautier, J. P. (1988). Interspecific affinities among guenons as deduced rom vocalizations. In A. Gautier-Hion, F. Bourlière, J.-P. Gautier, & J. Kingdon (Eds.), A primate radiation: Evolutionary biology of the African guenons (pp. 194–226). Cambridge: Cambridge University Press.Google Scholar
  42. Gautier-Hion, A. (1988). The diet and dietary habits of forest guenons. In A. Gautier-Hion, F. Bourlière, J.-P. Gautier, & J. Kingdon (Eds.), A primate radiation: Evolutionary biology of the African guenons (pp. 257–283). Cambridge: Cambridge University Press.Google Scholar
  43. Glenn, M. E. (1997). Group size and group composition of the mona monkey (Cercopithecus mona) on the island of Grenada, West Indies. American Journal of Primatology, 43, 167–173.PubMedGoogle Scholar
  44. Goodall, J. (1986). The chimpanzees of Gombe: Patterns of behavior. Cambridge, MA: Belknap Press.Google Scholar
  45. Groves, C. P. (2001). Primate taxonomy. Washington, DC: Smithsonian Institute Press.Google Scholar
  46. Grubb, P., Butynski, T. M., Oates, J. F., Bearders, S. K., Disotell, T. R., et al (2003). An assessment of the diversity of African primates. International Journal of Primatology, 24, 1301–1357.Google Scholar
  47. Guindon, S., & Gascuel, O. (2003). A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Systematic Biology, 52(5), 696–704.PubMedGoogle Scholar
  48. Guschanski, K., Krause, J., Sawyer, S., Valente, L. M., Bailey, S., Finstermeier, K., Sabin, R., Gilissen, E., Sonet, G., Nagy, Z. T., Lenglet, G., Mayer, F., & Savolainen, V. (2013). Next generation museomics disentangles one of the largest primate radiations. Systematic Biology, 62(4), 539–554.PubMedPubMedCentralGoogle Scholar
  49. Hamilton, A. C. (1988). Guenon evolution and forest history. In A. Gautier-Hion, F. Bourliere, J.-P. Gautier, & J. Kingdon (Eds.), A primate radiation: Evolutionary biology of the African guenons (pp. 13–34). Cambridge: Cambridge University Press.Google Scholar
  50. Hanke, M., & Wink, M. (1994). Direct DNA-sequencing of PCR-amplified vector inserts following enzymatic degradation of primer and DNTPS. BioTechniques, 17(5), 858–860.PubMedGoogle Scholar
  51. Harrison, R. G. (1993). Hybrid zones and the evolutionary process. New York: Oxford University Press.Google Scholar
  52. Harrison, R. G., & Larson, E. L. (2014). Hybridization, introgression, and the nature of species boundaries. Journal of Heredity, 105(S1), 795–809.PubMedGoogle Scholar
  53. Hart, J. A., Detwiler, K. M., Gilbert, C. C., Burrell, A. S., Fuller, J. L., Emetshu, M., Hart, T. B., Vosper, A., Sargis, E. J., & Tosi, A. J. (2012). Lesula: A new species of Cercopithecus monkey endemic to the Democratic Republic of Congo and implications for conservation of Congo’s Central Basin. PLoS ONE, 7(9), e44271.PubMedPubMedCentralGoogle Scholar
  54. Hazkani-Covo, E., Zeller, R. M., & Martin, W. (2010). Molecular poltergeists: Mitochondrial DNA copies (numts) in sequenced nuclear genomes. PLoS Genetics, 6(2), 1–11.Google Scholar
  55. Healy, A. (2013). Species profile of Cercopithecus mitis. In: R. A. Mittermeier, A. B. Rylands, & D. E. Wilson (Eds.), Handbook of the mammals of the world: Volume 3 primates. Lynx Edicions, Barcelona.Google Scholar
  56. Healy, A., & Detwiler, K. M. (2013). Species profile of Cercopithecus ascanius. In: R. A. Mittermeier, A. B. Rylands, D. E. Wilson (Eds.), Handbook of the mammals of the world: Volume 3 primates. Lynx Edicions, Barcelona.Google Scholar
  57. Hewitt, G. M. (2011). Quaternary phylogeography: The roots of hybrid zones. Genetica, 139, 617–638.PubMedGoogle Scholar
  58. Hubbs, C. L. (1955). Hybridization between fish species in nature. Systematic Zoology, 4(1), 1.Google Scholar
  59. Hubbs, C. L., & Laritz, C. M. (1961). Natural hybridization between Hadropterus scierus and Percina caprodes. The Southwestern Naturalist, 6(3/4), 188.Google Scholar
  60. Huelsenbeck, J. P., & Ronquist, F. (2001). MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics, 17(8), 754–755.PubMedGoogle Scholar
  61. Huhndorf, M. H., Kerbis Peterhans, J. C., & Loew, S. S. (2007). Comparative phylogeography of three endemic rodents from the Albertine Rift, east central Africa. Molecular Ecology, 16(3), 663–674.PubMedGoogle Scholar
  62. Jolly, C. J. (2001). A proper study for mankind: Analogies from the Papionin monkeys and their implications for human evolution. American Journal of Physical Anthropology, 116(33), 177–204.Google Scholar
  63. Jolly, D., Taylor, D., Marchant, R., Hamilton, A., Bonnefille, R., et al (1997). Vegetation dynamics in Central Africa since 18,000 yr BP: Pollen records from the interlacustrine highlands of Burundi, Rwanda and Western Uganda. Journal of Biogeography, 24(4), 495–512.Google Scholar
  64. Kahindo, C. M., Bates, J. M., & Bowie, R. K. (2017). Population genetic structure of Grauer’s swamp warbler Bradypterus graueri, an Albertine Rift endemic. Ibis, 159(2), 415–429.Google Scholar
  65. Kamilar, J. M., Martin, S. K., & Tosi, A. J. (2009). Combining biogeographic and phylogenetic data to examine primate speciation: An example using Cercopithecin monkeys. Biotropica, 41(4), 514–519.Google Scholar
  66. Kano, T. (1971). The chimpanzee of Filabanga, western Tanzania. Primates, 12(3–4), 229–246.Google Scholar
  67. Kaplin, B. A. (2001). Ranging behavior of two species of guenons (Cercopithecus lhoesti and C. mitis mitis) in the Nyungwe Forest Reserve, Rwanda. International Journal of Primatology, 22(4), 521–548.Google Scholar
  68. Kingdon, J. S. (1980). The role of visual signals and face patterns in African forest monkeys (guenons) of the genus Cercopithecus. The Transactions of the Zoological Society of London, 35, 425–475.Google Scholar
  69. Kingdon, J. S. (1989). Island Africa: The evolution of Africa's rare animals and plants. Princeton, NJ: University Press.Google Scholar
  70. Kingdon, J. S., Gippoliti, S., Butynksi, T. M., Lawes, M. J., Eeley, H., et al. (2008). Cercopithecus mitis. The IUCN red list of threatened species 2008, e.T4221A10676022.Google Scholar
  71. Kozak, G. M., & Boughman, J. W. (2012). Plastic responses to parents and predators lead to divergent shoaling behaviour in sticklebacks. Journal of Evolutionary Biology, 25, 759–769.PubMedGoogle Scholar
  72. Kumar, A., Bhandari, A., Sarde, S. J., Muppavarapu, S., & Tandon, R. (2015). Understanding V(D)J recombination initiator RAG1 gene using molecular phylogenetic and genetic variant analyses and upgrading missense and non-coding variants of clinical importance. Biochemical and Biophysical Research Communications, 462, 301–313.PubMedGoogle Scholar
  73. Lawes, M.J., Cords, M., & Lehn, C. (2013). Cercopithecus mitis species profile. In T. M. Butynski, J. Kingdon, & J. Kalina (Eds.), The mammals of Africa, Vol. II: Primates. London: Bloomsbury.Google Scholar
  74. Lo Bianco, S., Masters, J. C., & Sineo, L. (2017). The evolution of the Cercopithecini: A (post)modern synthesis. Evolutionary Anthropology, 26, 336–349.PubMedGoogle Scholar
  75. Mallet, J. (2005). Hybridization as an invasion of the genome. Trends in Ecology & Evolution, 2, 229–237.Google Scholar
  76. Mallet, J., Besansky, N., & Hahn, M. W. (2015). How reticulated are species? Bioessays, 38, 140–149.PubMedPubMedCentralGoogle Scholar
  77. Malukiewicz, J., Boere, V., Fuzessy, L. F., Grativol, A. D., French, J. A., Silva, I. O., Pereira, L. C. M., Ruiz-Miranda, C. R., Valença, Y. M., & Stone, A. C. (2014). Hybridization effects and genetic diversity of the common and black-tufted marmoset (Callithrix jacchus and Callithrux penicillata) mitochondrial control region. American Journal of Physical Anthropology, 155(4), 522–536.PubMedGoogle Scholar
  78. Marler, P. (1973). A comparison of vocalizations of red-tailed monkeys and blue monkeys, Cercopithecus ascanius and C. mitis, in Uganda. Zeitschrift für Tierpsychologie, 33, 223–247.PubMedGoogle Scholar
  79. Marques, J. P., Farelo, L., Vilela, J., Alves, P. C., Melo-Ferreira, J., et al (2017). Range expansion underlies historical introgressive hybridization in the Iberian hare. Scientific Reports, 7, Article number: 40788.Google Scholar
  80. Mastrantonio, V., Porretta, D., Urbanelli, S., Crasta, G., & Nascetti, G. (2016). Dynamics of mtDNA introgression during species range expansion: Insights from an experimental longitudinal study. Scientific Reports, 30355.Google Scholar
  81. McGraw, W. S. (2002). Diversity of guenon positional behavior. In M. E. Glenn & M. Cords (Eds.), The guenons: Diversity and adaptation in African monkeys (pp. 113–131). New York: Kluwer Academic.Google Scholar
  82. McLester, E., Stewart, F. A., & Piel, A. K. (2016). Observation of an encounter between African wild dogs (Lycaon pictus) and a chimpanzee (Pan troglodytes schweinfurthii) in the Issa Valley, Tanzania. African Primates, 11(1), 27–36.Google Scholar
  83. Mendelson, T., & Shaw, K. (2012). The (mis)concept of species recognition. Trends in Ecology & Evolution, 27(8), 421–427.Google Scholar
  84. Mittermeier, R. A., Rylands, A. B., & Wilson, D. E. (2013). Handbook of the mammals of the world. In Primates (Vol. Vol. 3). Barcelona: Lynx Edicions.Google Scholar
  85. Moulin, S., Gerbault-Seureau, M., & Dutrillaux, B. R. F. (2008). Phylogenomics of African guenons. Chromosome Research, 16, 783–799.PubMedGoogle Scholar
  86. Nagel, U. (1973). A comparison of anubis baboons, hamadryas baboons, and their hybrids at a species border in Ethiopia. Folia Primatologica, 19, 104–165.Google Scholar
  87. Oates, J. F., & Groves, C. P. (2008). Cercopithecus nictitans. The IUCN Red List of Threatened Species 2008, e.T4224A10682370.Google Scholar
  88. Oates, J. F., Baker, L. R., & Tooze, Z. J. (2008a). Cercopithecus sclateri. The IUCN Red List of Threatened Species 2008, e.T4229A10678392.Google Scholar
  89. Oates, J. F., Gippoliti, S., & Bearder, S. (2008b). Cercopithecus erythrogaster. The IUCN Red List of Threatened Species 2008, e.T4217A10672698.Google Scholar
  90. Oates, J. F., Gippoliti, S. & Bearder, S. (2008c). Cercopithecus cephus. The IUCN Red List of Threatened Species 2008, e.T4214A10664683.Google Scholar
  91. Oates, J. F., Gippoliti, S., & Groves, C. P. (2008d). Cercopithecus erythrotis. The IUCN Red List of Threatened Species 2008, e.T4218A10651543.Google Scholar
  92. Oates, J. F., Gippoliti, S. & Groves, C. P. (2008e). Cercopithecus petaurista. The IUCN Red List of Threatened Species 2008, e.T4225A10683942.Google Scholar
  93. Oates, J. F., Hart, J., Groves, C. P., & Butynski, T. M. (2008f). Cercopithecus ascanius. The IUCN Red List of Threatened Species 2008, e.T4212A10654844.Google Scholar
  94. Perry, G. (2014). The promise and practicality of population genomics research with endangered species. International Journal of Primatology, 35(1), 55–70.Google Scholar
  95. Peterson, M., Larson, E., Brassil, M., Buckingham, K., Juárez, D., et al (2011). Cryptic gametic interactions confer both conspecific and heterospecific advantages in the Chrysochus (Coleoptera: Chrysomelidae) hybrid zone. Genetica, 139(5), 663–676.PubMedGoogle Scholar
  96. Phillips-Conroy, J., & Jolly, C. J. (1986). Changes in the structure of the baboon hybrid zone in the Awash National Park, Ethiopia. American Journal of Physical Anthropology, 71, 337–350.Google Scholar
  97. Phillips-Conroy, J., Jolly, C. J., & Brett, F. L. (1991). Characteristics of Hamadryas-like male baboons living in anubis baboon troops in the Awash hybrid zone, Ethiopia. American Journal of Physical Anthropology, 86, 353–368.PubMedGoogle Scholar
  98. Pintea, L. (2007). Applying remote sensing and GIS for chimpanzee habitat change detection, behavior and conservation. Ph.D. thesis, University of Minnesota.Google Scholar
  99. Plumptre, A. J., Masozera, M., Fashing, P. J., McNeilage, A., Ewango, C., et al. (2002). Biodiversity surveys of the Nyungwe Forest Reserve in S.W. Rwanda. WCS Working Papers No. 18.
  100. Plumptre, A. J., Davenport, T. R. B., Behangana, M., Kityo, R., Eilu, G., et al (2007). The biodiversity of the Albertine rift. Biological Conservation, 134, 178–194.Google Scholar
  101. Pozzi, L., Hodgson, J. A., Burrell, A. S., Sterner, K. N., Raaum, R. L., & Disotell, T. R. (2014). Primate phylogenetic relationships and divergence dates inferred from complete mitochondrial genomes. Molecular Phylogenetics and Evolution, 75, 165–183.Google Scholar
  102. Pusey, A. E., Pintea, L., Wilson, M. L., Kamenya, S., & Goodall, J. (2007). The contribution of long-term research at Gombe National Park to chimpanzee conservation. Conservation Biology, 21(3), 623–634.PubMedGoogle Scholar
  103. Rambaut A. (2016). FigTree v.1.4.3. Edinburgh, UK.
  104. Roberts, S., Nikitopoulos, E., & Cords, M. (2014). Factors affecting low resident male siring success in one-male groups of blue monkeys. Behavioral Ecology, 25, 852–861.Google Scholar
  105. Ronquist, F., & Huelsenbeck (2003). MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics, 19(12), 1572–1574.PubMedGoogle Scholar
  106. Schmidt, P. R. (1997). Iron technology in East Africa: Symbolism, science, and archaeology. Bloomington: Indiana University Press.Google Scholar
  107. Shaw, K. L., & Lambert, J. M. (2014). Dissecting post-mating prezygotic speciation phenotypes. Bioessays, 36(11), 1050–1053.PubMedGoogle Scholar
  108. Šíchová, K., Koskela, E., Mappes, T., Lantová, P., & Boratyński, Z. (2014). On personality, energy metabolism and mtDNA introgression in bank voles. Animal Behavior, 92, 229–237.Google Scholar
  109. Struhsaker, T. T. (1970). Phylogenetic implications of some vocalizations of Cercopithecus monkeys. In J. R. Napier & P. H. Napier (Eds.), Old World monkeys: Evolution, systematics, and behavior (pp. 365–444). New York: Academic Press.Google Scholar
  110. Struhsaker, T. T., & Leland, L. (1979). Socioecology of five sympatric monkey species in the Kibale Forest, Uganda. Advances in the Study of Behavior, 9, 159–228.Google Scholar
  111. Struhsaker, T. T., Butynski, T. M., & Lwanga, J. S. (1988). Hybridization between redtail (Cercopithecus ascanius schmidti) and blue (C. mitis stuhlmanni) monkeys in the Kibale Forest, Uganda. In A. Gautier-Hion, F. Bourlière, J.-P. Gautier, & J. Kingdon (Eds.), A primate radiation: Evolutionary biology of the African guenons (pp. 477–497). Cambridge: Cambridge University Press.Google Scholar
  112. Svensson, E. I. (2013). Beyond hybridization: Diversity of interactions with heterospecifics, direct fitness consequences and the effects on mate preferences. Journal of Evolutionary Biology, 26, 270–273.PubMedGoogle Scholar
  113. Swofford, D. L. (2003). PAUP*. Phylogenetic analysis using parsimony (* and other methods). Version 4. Sunderland, MA: Sinauer Associates.Google Scholar
  114. Ting, N. (2008). Mitochondrial relationships and divergence dates of the African colobines: Evidence of Miocene origins for the living colobus monkeys. Journal of Human Evolution, 55, 312–325.PubMedGoogle Scholar
  115. Tosi, A. J. (2008). Forest monkeys and Pleistocene refugia: A phylogeographic window onto the disjunct distribution of the Chlorocebus lhoesti species group. Zoological Journal of the Linnean Society, 154(2), 408–418.Google Scholar
  116. Tung, J., & Barreiro, L. B. (2017). The contribution of admixture to primate evolution. Current Opinion in Genetics & Development, 47, 61–68.Google Scholar
  117. Verzijden, M. N., ten Cate, C., Servedio, M. R., Kozak, G. M., Boughman, J. W., & Svensson, E. I. (2012). The impact of learning on sexual selection and speciation. Trends in Ecology & Evolution, 27(9), 511–519.Google Scholar
  118. Wang, B., Zhou, X., Shi, F., Liu, Z., Roos, C., Garber, P. A., Li, M., & Pan, H. (2015). Full-length numt analysis provides evidence for hybridization between the Asian colobine genera Trachypithecus and Semnopithecus. American Journal of Primatology, 77, 901–910.PubMedGoogle Scholar
  119. Willis, P. M. (2013). Why do animals hybridize? Acta Ethologica, 16(3), 127–134.Google Scholar
  120. Wirtz, P. (1999). Mother species-father species: Unidirectional hybridization in animals with female choice. Journal of Animal Behavior, 58, 1–12.Google Scholar
  121. Woodruff, D. S. (1973). Natural hybridization and hybrid zones. Systematic Zoology, 22, 213–217.Google Scholar
  122. Zinner, D., Arnold, M. L., & Roos, C. (2009). Is the new primate genus Rungwecebus a baboon? PLoS ONE, 4, e4859. Scholar
  123. Zinner, D., Arnold, M. L., & Roos, C. (2011). The strange blood: Natural hybridization in primates. Evolutionary Anthropology, 20(3), 96–103.PubMedGoogle Scholar
  124. Zwickl, D. J. (2006). Genetic algorithm approaches for the phylogenetic analysis of large biological sequence datasets under the maximum likelihood criterion. Ph.D. dissertation, University of Texas at Austin.Google Scholar

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

Authors and Affiliations

  1. 1.Departments of Anthropology and Biological SciencesFlorida Atlantic UniversityBoca RatonUSA

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