Skip to main content
SpringerLink
Log in

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

International Journal of Primatology Aims and scope Submit manuscript

Cite this article

Abstract

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Aldrich-Blake, F. P. G. (1968). A fertile hybrid between two Cercopithecus species in the Budongo Forest, Uganda. Folia Primatologica, 9, 15–21.

    Article  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Allen, W. L., Stevens, M., & Higham, J. P. (2014). Character displacement of Cercopithecini primate visual signals. Nature Communications, 5, 4266.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Arnold, M. L., & Meyer, A. (2006). Natural hybridization in primates: One evolutionary mechanism. Zoology, 109(4), 261–276.

    Article  PubMed  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Avise, J. C. (2004). Molecular markers, natural history, and evolution. Sunderland: Sinauer Associates.

    Google Scholar 

  • Barton, N. H., & Hewitt, G. M. (1985). Analysis of hybrid zones. Annual Review of Ecology and Systematics, 16, 113–148.

    Article  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Bergman, T. J. (2000). Mating behavior and reproductive success of hybrid male baboons (Papio hamadryas hamadryas × Papio hamadryas anubis). Ph.D. thesis, Washington University.

  • Berlocher, S. H., & Howard, D. J. (1998). Endless forms: Species and speciation. New York: Oxford University Press.

    Google Scholar 

  • 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.

    Article  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Butynski, T. M., Kingdon, J., & Kalina, J. (2013). Mammals of Africa. In Primates (Vol. Vol. II). London: Bloomsbury.

    Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Coleman, B. T., & Hill, R. A. (2014). Biogeographic variation in the diet and behavior of Cercopithecus mitis. Folia Primatologica, 85, 319–334.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Cords, M. (1987a). Mixed species association of Cercopithecus monkeys in the Kakamega forest. University of California Publications in. Zoology, 117, 1–109.

    Google Scholar 

  • 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 

  • 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 

  • Cords, M. (2002). Friendship among adult female blue monkeys (Cercopithecus mitis). Behaviour, 139, 291–314.

    Article  Google Scholar 

  • 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.

  • 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.

    Article  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • Darriba, D., Taboada, G. L., Doallo, R., & Posada, D. (2012). jModel test 2: More models new heuristics and parallel computing. Nature Methods, 9, 772.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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 

  • Detwiler, K. M. (2010). Natural hybridization between Cercopithecus mitis × C. ascanius in Gombe National Park. Doctoral dissertation, New York University.

  • 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.

    Article  Google Scholar 

  • 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 

  • 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.

    Article  Google Scholar 

  • 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 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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 

  • 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 

  • 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.

    Article  PubMed  CAS  Google Scholar 

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

    Google Scholar 

  • Groves, C. P. (2001). Primate taxonomy. Washington, DC: Smithsonian Institute Press.

    Google Scholar 

  • 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.

    Article  Google Scholar 

  • Guindon, S., & Gascuel, O. (2003). A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Systematic Biology, 52(5), 696–704.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 

  • 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.

    PubMed  CAS  Google Scholar 

  • Harrison, R. G. (1993). Hybrid zones and the evolutionary process. New York: Oxford University Press.

    Google Scholar 

  • Harrison, R. G., & Larson, E. L. (2014). Hybridization, introgression, and the nature of species boundaries. Journal of Heredity, 105(S1), 795–809.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

  • 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.

  • Hewitt, G. M. (2011). Quaternary phylogeography: The roots of hybrid zones. Genetica, 139, 617–638.

    Article  PubMed  Google Scholar 

  • Hubbs, C. L. (1955). Hybridization between fish species in nature. Systematic Zoology, 4(1), 1.

    Article  Google Scholar 

  • Hubbs, C. L., & Laritz, C. M. (1961). Natural hybridization between Hadropterus scierus and Percina caprodes. The Southwestern Naturalist, 6(3/4), 188.

    Article  Google Scholar 

  • Huelsenbeck, J. P., & Ronquist, F. (2001). MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics, 17(8), 754–755.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Kano, T. (1971). The chimpanzee of Filabanga, western Tanzania. Primates, 12(3–4), 229–246.

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Kingdon, J. S. (1989). Island Africa: The evolution of Africa's rare animals and plants. Princeton, NJ: University Press.

    Google Scholar 

  • 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.

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

  • Lo Bianco, S., Masters, J. C., & Sineo, L. (2017). The evolution of the Cercopithecini: A (post)modern synthesis. Evolutionary Anthropology, 26, 336–349.

    Article  PubMed  Google Scholar 

  • Mallet, J. (2005). Hybridization as an invasion of the genome. Trends in Ecology & Evolution, 2, 229–237.

    Article  Google Scholar 

  • Mallet, J., Besansky, N., & Hahn, M. W. (2015). How reticulated are species? Bioessays, 38, 140–149.

    Article  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

  • 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.

  • 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 

  • 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 

  • Mendelson, T., & Shaw, K. (2012). The (mis)concept of species recognition. Trends in Ecology & Evolution, 27(8), 421–427.

    Article  Google Scholar 

  • 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 

  • Moulin, S., Gerbault-Seureau, M., & Dutrillaux, B. R. F. (2008). Phylogenomics of African guenons. Chromosome Research, 16, 783–799.

    Article  PubMed  CAS  Google Scholar 

  • Nagel, U. (1973). A comparison of anubis baboons, hamadryas baboons, and their hybrids at a species border in Ethiopia. Folia Primatologica, 19, 104–165.

    Article  CAS  Google Scholar 

  • Oates, J. F., & Groves, C. P. (2008). Cercopithecus nictitans. The IUCN Red List of Threatened Species 2008, e.T4224A10682370.

  • Oates, J. F., Baker, L. R., & Tooze, Z. J. (2008a). Cercopithecus sclateri. The IUCN Red List of Threatened Species 2008, e.T4229A10678392.

  • Oates, J. F., Gippoliti, S., & Bearder, S. (2008b). Cercopithecus erythrogaster. The IUCN Red List of Threatened Species 2008, e.T4217A10672698.

  • Oates, J. F., Gippoliti, S. & Bearder, S. (2008c). Cercopithecus cephus. The IUCN Red List of Threatened Species 2008, e.T4214A10664683.

  • Oates, J. F., Gippoliti, S., & Groves, C. P. (2008d). Cercopithecus erythrotis. The IUCN Red List of Threatened Species 2008, e.T4218A10651543.

  • Oates, J. F., Gippoliti, S. & Groves, C. P. (2008e). Cercopithecus petaurista. The IUCN Red List of Threatened Species 2008, e.T4225A10683942.

  • Oates, J. F., Hart, J., Groves, C. P., & Butynski, T. M. (2008f). Cercopithecus ascanius. The IUCN Red List of Threatened Species 2008, e.T4212A10654844.

  • Perry, G. (2014). The promise and practicality of population genomics research with endangered species. International Journal of Primatology, 35(1), 55–70.

    Article  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Pintea, L. (2007). Applying remote sensing and GIS for chimpanzee habitat change detection, behavior and conservation. Ph.D. thesis, University of Minnesota.

  • 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. http://www.wcs.org/science/.

  • 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.

    Article  Google Scholar 

  • 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.

  • 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.

    Article  PubMed  Google Scholar 

  • Rambaut A. (2016). FigTree v.1.4.3. Edinburgh, UK. http://tree.bio.ed.ac.uk/software/figtree/

  • 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.

    Article  Google Scholar 

  • Ronquist, F., & Huelsenbeck (2003). MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics, 19(12), 1572–1574.

    Article  PubMed  CAS  Google Scholar 

  • Schmidt, P. R. (1997). Iron technology in East Africa: Symbolism, science, and archaeology. Bloomington: Indiana University Press.

    Google Scholar 

  • Shaw, K. L., & Lambert, J. M. (2014). Dissecting post-mating prezygotic speciation phenotypes. Bioessays, 36(11), 1050–1053.

    Article  PubMed  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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 

  • 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.

    Article  Google Scholar 

  • 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 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Swofford, D. L. (2003). PAUP*. Phylogenetic analysis using parsimony (* and other methods). Version 4. Sunderland, MA: Sinauer Associates.

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Tung, J., & Barreiro, L. B. (2017). The contribution of admixture to primate evolution. Current Opinion in Genetics & Development, 47, 61–68.

    Article  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Willis, P. M. (2013). Why do animals hybridize? Acta Ethologica, 16(3), 127–134.

    Article  Google Scholar 

  • Wirtz, P. (1999). Mother species-father species: Unidirectional hybridization in animals with female choice. Journal of Animal Behavior, 58, 1–12.

    Article  CAS  Google Scholar 

  • Woodruff, D. S. (1973). Natural hybridization and hybrid zones. Systematic Zoology, 22, 213–217.

    Article  Google Scholar 

  • Zinner, D., Arnold, M. L., & Roos, C. (2009). Is the new primate genus Rungwecebus a baboon? PLoS ONE, 4, e4859. https://doi.org/10.1371/journal.pone.0004859.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Zinner, D., Arnold, M. L., & Roos, C. (2011). The strange blood: Natural hybridization in primates. Evolutionary Anthropology, 20(3), 96–103.

    Article  PubMed  Google Scholar 

  • 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.

Download references

Acknowledgments

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.

Author information

Authors and Affiliations

  1. Departments of Anthropology and Biological Sciences, Florida Atlantic University, Boca Raton, FL, 33431, USA

    Kate M. Detwiler

Authors
  1. Kate M. Detwiler
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Kate M. Detwiler.

Additional information

Handling Editor: Joanna M. Setchell

Electronic supplementary material

ESM 1

(DOC 32 kb)

ESM 2

(XLS 60.5 kb)

ESM 3

(DOCX 192 kb)

Rights and permissions

Reprints and Permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Detwiler, K.M. Mitochondrial DNA Analyses of Cercopithecus Monkeys Reveal a Localized Hybrid Origin for C. mitis doggetti in Gombe National Park, Tanzania. Int J Primatol 40, 28–52 (2019). https://doi.org/10.1007/s10764-018-0029-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10764-018-0029-7

Keywords

search

Navigation