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Conservation Implications of Hybridization in African Cercopithecine Monkeys

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Abstract

Numerous field reports of hybrid monkeys and documented cases of persistent hybrid zones suggest that natural hybridization is common among African cercopithecines. Both theoretical considerations and a review of cases lead us to conclude that parapatric hybridization among closely related allotaxa is a widespread, usually natural process whose incidence may be modified by human influence. Sympatric hybridization, between species ecologically distinct enough to have overlapping ranges, is rarer, and in monkeys tends to occur in settings where natural or anthropogenic habitat edges restrict migration and hence access to unrelated conspecific mates. Although sympatric hybridization occurs in the absence of human disturbance, and may even have been a creative force in cercopithecine evolution, anthropogenic habitat fragmentation may increase its incidence. Hybridization with a more abundant form may increase the level of threat faced by a species whose numbers and range have been severely restricted, either naturally or artificially.

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References

  • Alberts, S. C., and Altmann, J. (2001). Immigration and hybridization patterns of yellow and anubis baboons in and around Amboseli, Kenya. Am. J. Primatol. 53: 139–154.

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Aldrich-Blake, F. P. G. (1970). The Ecology and Behaviour of the Blue Monkey, Ph.D. Thesis, University of Bristol, Bristol.

  • Allendorf, F. W., Leary, R. F., Spruell, P., and Wenburg, J. K. (2001). The problems with hybrids: setting conservation guidelines. Trends Ecol. Evol. 16(11): 613–622.

    Google Scholar 

  • Arnold, M. L. (1997). Natural Hybridization and Evolution, Oxford University Press, Oxford.

    Google Scholar 

  • Arntzen, J. W., and Wallis, G. P. (1991). Restricted gene flow in a moving hybrid zone of the newts Triturus cristatus and T. marmoratus in western France. Evolution 45(4): 805–826.

    Google Scholar 

  • Avise, J. C. (1994). Molecular Markers, Natural History and Evolution. Kluwer Academic, London.

    Google Scholar 

  • Baker, L. R., and Tooze, Z. J. (2003). Status of the Sclater’s guenon (Cercopithecus sclateri) in southeastern Nigeria. Am. J. Primatol. 60: 88–89.

    Google Scholar 

  • Barton, N. H. (2001). The role of hybridization in evolution. Mol. Ecol. 10: 551–568.

    CAS  PubMed  Google Scholar 

  • Barton, N. H., and Hewitt, G. M. (1985). Analysis of hybrid zones. Annu. Rev. Ecol. Syst. 16: 113–148.

    Google Scholar 

  • Bergman, T. J. (2000). Mating Behavior and Reproductive Success of Hybrid Male Baboons (Papio hamadryas hamadryas x Papio hamadryas anubis), Ph.D. Thesis, Washington University, Missouri.

  • Bernstein, I. S. (1966). Naturally occurring primate hybrid. Science 154: 1559–1560.

    CAS  PubMed  Google Scholar 

  • Beyene, S. G. (1998). The Role of Female Mating Behavior in Hybridization Between Anubis and Hamadryas Baboons in Awash, Ethiopia, Ph.D. Thesis, Washington University, Missouri.

  • Booth, A. (1955). Speciation in the Mona monkeys. J. Mammol. 36: 434–449.

    Google Scholar 

  • Booth, A. (1956). The Cercopithecidae of the Gold and Ivory Coasts: Geographic and systematic observations. Ann. Mag. Nat. Hist. 12(9): 476–480.

    Google Scholar 

  • Booth, C. (1968). Taxonomic studies of Cercopithecus mitis Wolf (East Africa). Nat. Geogr. Soc. Res. Reports (1963 projects): 37–51.

    Google Scholar 

  • Bourlière, F., Hunkeler, C., and Bertrand, M. (1970). Ecology and behavior of Lowe’s guenon (Cercopithecus campbelli lowei) in the Ivory Coast. In Napier, J. R., and Napier, P. H. (eds.), Old World Monkeys, Academic Press, New York, pp. 297–350.

    Google Scholar 

  • Brett, F., Jolly, C. J., Socha, W., and Wiener, A. S. (1977). Human-like ABO blood groups in wild Ethiopian baboons. Yrbk. Phys. Anth. 20: 276–289.

    Google Scholar 

  • Butynski, T. M. (1990). Comparative ecology of blue monkeys (Cercopithecus mitis) in high- and low-density subpopulations. Ecol. Monogr. 60: 1–26.

    Google Scholar 

  • Butynski, T. M. (2002). The guenons: an overview of diversity and taxonomy. In Glenn, M. E., and Cords, M. (eds.), The Guenons: Diversity and Adaptation in African Monkeys, Kluwer Academic/Plenum, New York, pp. 3–13.

    Google Scholar 

  • Chapman, C. A., and Chapman, L. J. (1996). Mid-elevation forests: a history of disturbance and regeneration. In McClanahan, T. R., and Young, T. P. (eds.), East African Ecosystems and Their Conservation, Oxford University Press, Oxford, pp. 385–400.

    Google Scholar 

  • Chapman, C. A., and Chapman, L. J. (2000). Interdemic variation in mixed-species association patterns: common diurnal primates of Kibale National Park, Uganda. Behav. Ecol. Sociobiol. 47: 129–139.

    Google Scholar 

  • Clarke, B., Johnson, M. S., and Murray, J. (1998). How ‘molecular leakage’ can mislead us about island speciation. In Grant P. R. (ed.), Evolution on Islands, Oxford University Press, Oxford, pp. 181–195.

    Google Scholar 

  • Clutton-Brock, T. H. (1972). Feeding and Ranging Behavior in the Red Colobus. Ph.D. Thesis, Cambridge University, Cambridge.

  • Coe, M. (1985). Islands in the Bush: A Natural History of the Kora National Reserve, Kenya, George Phillip, New York.

    Google Scholar 

  • Colyn, M., and Deleporte, P. (2002). Biogeographic analysis of central African forest guenons. In Glenn, M. E., and Cords, M. (eds.), The Guenons: Diversity and Adaptation in African Monkeys, Kluwer Academic/Plenum, New York, pp. 61–78.

    Google Scholar 

  • Cords, M. (2000). The number of males in guenon groups. In Kappeler, P. (ed.), Primate Males, Cambridge University Press, Cambridge, pp. 84–96.

    Google Scholar 

  • Dandelot, P. (1959). Note sur la classification des cercopitheques du groupe aethiops. Mammalia 23: 357–368.

    Google Scholar 

  • Dandelot, P., and Prevost, J. (1972). Contribution a l’etude des primates d’Ethiopie (Simiens). Mammalia 36: 607–633.

    Google Scholar 

  • Detwiler, K. M. (2002). Hybridization between red-tailed monkeys (Cercopithecus ascanius) and blue monkeys (C. mitis) in East African forests. In Glenn, M. E., and Cords, M. (eds.), The Guenons: Diversity and Adaptation in African Monkeys, Kluwer Academic/Plenum, New York, pp. 79–97.

    Google Scholar 

  • Dowling, T. E., and Secor, C. L. (1997). The role of hybridization and introgression in the diversification of animals. Annu. Rev. Ecol. Syst. 28: 593–619.

    Google Scholar 

  • Dunbar, R. I. M., and Dunbar, P. (1974). On hybridization between Theropithecus gelada and Papio anubis in the wild. J. Hum. Evol. 3: 187–192.

    Google Scholar 

  • Fairgrieve, C., and Muhumuza, G. (2003). Feeding ecology and dietary differences between blue monkey (Cercopithecus mitis stuhlmanni Matschie) groups in logged and unlogged forest, Budongo Forest Reserve, Uganda. Afr. J. Ecol. 41: 141–149.

    Google Scholar 

  • Federal Register (1996). Endangered and threatened wildlife and plants; proposed policy and proposed rule on the treatment of intercrosses and intercross progeny (the issue of ‘hybridization’); Request for public comment. Federal Register 61(26): 4710– 4713.

    Google Scholar 

  • Gartlan, J. S., and Struhsaker, T. T. (1972). Polyspecific associations and niche separation of rain-forest anthropoids in Cameroon, West Africa. J. Zool. 168: 221–266.

    Google Scholar 

  • Gautier, J. P. (1988). Interspecific affinities among guenons as deduced from vocalizations. In Gautier-Hion, A., Bourliere, F., Gautier, J.-P., and Kingdon, J. (eds.) A Primate Radiation: Evolutionary Biology of the African Guenons, Cambridge University Press, Cambridge, pp. 194–226.

    Google Scholar 

  • Gautier-Hion, A. (1988). Polyspecific associations among forest guenons: ecological, behavioural and evolutionary aspects. In Gautier-Hion, A., Bourliere, F., Gautier, J.-P., and Kingdon, J. (eds.), A Primate Radiation: Evolutionary Biology of the African Guenons, Cambridge University Press, Cambridge, pp. 452–476.

    Google Scholar 

  • Gautier-Hion, A., Colyn, M., and Gautier, J.-P. (1999). Histoire Naturelle des Primates d’Afrique Centrale, ECOFAC, Libreville.

    Google Scholar 

  • Goodall, J. (1986). The Chimpanzees of Gombe: Patterns of Behavior, Harvard University Press, Cambridge.

    Google Scholar 

  • Goodman, S. J., Barton, N. H., Swanson, G., Abernethy, K., and Pemberton, J. M. (1999). Introgression through rare hybridization: a genetic study of a hybrid zone between red and sika deer (genus Cervus) in Argyll, Scotland. Genetics 152: 355–371.

    CAS  PubMed  Google Scholar 

  • Grant, B. R., and Grant, P. R. (1998). Hybridization and speciation in Darwin’s finches. In Howard, D. J., and Berlocher, S. H. (eds.), Endless Forms: Species and Speciation, Oxford University Press, Oxford, pp. 404–422.

    Google Scholar 

  • Grant, P. R., and Grant, B. R. (1992). Hybridization of bird species. Science 256: 193–197.

    Google Scholar 

  • Groves, C. P. (1978). Phylogenetic and population systematics of the mangabeys (Primates: Cercopithecoidea). Primates 19(1): 1–34.

    Google Scholar 

  • Groves, C. P. (1993). Speciation in living hominoid primates. In W. H. Kimbel, and L. B. Martin (eds.), Species, Species Concepts, and Primate Evolution, Plenum Press, New York, pp. 109–121.

    Google Scholar 

  • Groves, C. P. (2001). Primate Taxonomy. Smithsonian Institution Press, Washington, DC.

    Google Scholar 

  • Grubb, P. (1999). Evolutionary processes implicit in distribution patterns of modern African mammals. In T. G. Bromage, and F. Schrenk (eds.), African Biogeography, Climate Change, and Human Evolution, Oxford University Press, New York, pp. 150– 164.

    Google Scholar 

  • Grubb, P., Butynski, T. M., Oates, J. F., Bearder, S. K., Disotell, T. R., Groves, C. P., and Struhsaker, T. T. (2003). An assessment of the diversity of African primates. Int. J. Primatol. 24: 1301–1357.

    Google Scholar 

  • Hewitt, G. M. (1996). Some genetic consequences of ice age, and their role in divergence and speciation. Biol. J. Linn. Soc. 58: 247–276.

    Google Scholar 

  • Hewitt, G. M. (2001). Speciation, hybrid zones and phylogeography – or seeing genes in space and time. Mol. Ecol. 10: 537–549.

    CAS  PubMed  Google Scholar 

  • Jolly, C. J., Woolley-Barker, T., Beyene, S., Disotell, T. R., Phillips-Conroy, J. E. (1997). Intergeneric hybrid baboons. Int. J. Primatol. 18: 597–627.

    Google Scholar 

  • Jolly, C. J. (1993). Species, subspecies, and baboon systematics. In W. H. Kimbel, and L. B. Martin (eds.), Species, Species Concepts, and Primate Evolution, Plenum Press, New York, pp. 67–107.

    Google Scholar 

  • Jolly, C. J. (2001). A proper study for mankind: analogies from the papionin monkeys and their implications for human evolution. Yrbk. Phys. Anth. 44: 177–204.

    Google Scholar 

  • Kaplin, B. A. (1998). Ecology of Two African Forest Monkeys: Temporal and Spatial Patterns of Habitat Use, Foraging Behavior, and Seed Dispersal, Ph.D. Thesis, The University of Wisconsin, Madison.

  • Kingdon, J. (1971). East African Mammals: An Atlas of Evolution in Africa, Academic Press, New York.

    Google Scholar 

  • Kingdon, J. (1980). The role of visual signals and face patterns in African forest monkeys (guenons) of the genus Cercopithecus. Trans. Zool. Soc. Lond. 35: 425–475.

    Google Scholar 

  • Kingdon, J. (1988). What are face patterns and do they contribute to reproductive isolation in guenons? In Gautier-Hion, A., Bourliere, F., Gautier, J.-P., and Kingdon, J. (eds.), A Primate Radiation: Evolutionary Biology of the African Guenons, Cambridge University Press, Cambridge, pp. 227–245.

    Google Scholar 

  • Kingdon, J. (1997). The Kingdon Field Guide to African Mammals, Academic Press, New York.

    Google Scholar 

  • Lehman, N., Eisenhawer, A., Hansen, K., Mech, L. D., Peterson, R. O., Gogan, P. J., and Wayne, R. K. (1991). Introgression of coyote mitochondrial DNA into sympatric North American gray wolf populations. Evolution 45(1): 104–119.

    Google Scholar 

  • Lernould, J.-M. (1988). Classification and geographical distribution of guenons: A review. In Gautier-Hion, A., Bourliere, F., Gautier, J.-P., and Kingdon, J. (eds). A Primate Radiation: Evolutionary Biology of the African Guenons, Cambridge University Press, Cambridge, pp. 54–78.

    Google Scholar 

  • Machado, A. B. (1965). Acerca do achado em Angola de uma forma racial inedita do Cercopithecus ascanius (Audebert, 1799) (Primates, Cercopithecidae). Boletim da Academia das Ciencias de Lisboa. 37: 182–198.

  • Machado, A. B. (1969). Subsidios para o estudo da biologia na lunda. Mamiferos de Angola ainda nao citados ou pouco conhecidos. Publicacoes Culturais da Companhia de Diamantes Angola. 46: 93–231.

    Google Scholar 

  • Maples, W. R., and McKern, T. W. (1967). A preliminary report on the classification of the Kenya baboon. In Vagtborg, H. (ed.), The Baboon in Medical Research. Vol. 2, University of Texas Press, Austin, pp. 13–22.

    Google Scholar 

  • Mori, A., and Belay, G. (1990). The distribution of baboon species and a new population of gelada baboons along the Wabi-Shebeli River, Ethiopia. Primates 31: 495–508.

    Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Napier, P. H. (1981). Catalogue of Primates in the British Museum (Natural History). Part II: Family Cercopithecidae, Subfamily Cercopithecinae, British Museum (Natural History), London.

    Google Scholar 

  • Newman, T. K. (1997). Mitochondrial DNA Analysis of Intraspecific Hybridization in Papio hamadryas anubis and Papio hamadryas hamadryas and Their Hybrids in the Awash National Park, Ethiopia. Ph.D. Thesis, New York University, New York.

  • Oates, J. F. (1988). The distribution of Cercopithecus monkeys in West African forests. In Gautier-Hion, A., Bourliere, F., Gautier, J.-P., and Kingdon, J. (eds.), A Primate Radiation: Evolutionary Biology of the African Guenons, Cambridge University Press, Cambridge, pp. 79–103.

    Google Scholar 

  • Oates, J. F., Anadu, P. A., Gadsby, E. L., and Werre, J. L. (1992). Sclater’s guenon-a rare Nigerian monkey threatened by deforestation. National Geographic Research and Exploration 8(4): 476–491.

    Google Scholar 

  • Oates, J. F. (1996). African Primates: Status Survey and Conservation Action Plan, Revised Edition. IUCN/SSC Primate Specialist Group, IUCN, Gland, Switzerland.

  • Oates, J. F. (1999). Myth and Reality in the Rain Forest: How Conservation Strategies are Failing in West Africa. University of California Press, Berkeley.

    Google Scholar 

  • Paterson, H. E. H. (1985). The recognition concept of species. In Vrba, E. S. (ed.), Species and Speciation, Transvaal Museum Monograph No. 4 Transvaal Museum, Pretoria, pp. 21– 29.

    Google Scholar 

  • Phillips-Conroy, J., and Jolly, C. J. (1986). Changes in the structure of the baboon hybrid zone in the Awash National Park, Ethiopia. Am. J. Phys. Anth. 71: 337–350.

    Google Scholar 

  • Phillips-Conroy, J., Jolly, C. J., and Brett, F. L. (1991). Characteristics of Hamadryas-like male baboons living in Anubis baboon troops in the Awash hybrid zone, Ethiopia. Am. J. Phys. Anth. 86: 353–368.

    CAS  Google Scholar 

  • Pintea, L., Bauer, M. E., Bolstad, P. V., and Pusey, A. (2002). Matching multiscale remote sensing data to interdisciplinary conservation needs: the case of chimpanzees in western Tanzania. In Morain, S., and Budge, A. (eds.), Pecora 15/Land Satellite Information IV/ISPRS Commission I/FIEOS 2002 Conference Proceedings: Integrated Remote Sensing at the Global, Regional and Local Scale.

  • Plumptre, A. J. (2000). Monitoring mammal populations with line transect techniques in African forests. J. Appl. Ecol. 37: 356–368.

    Google Scholar 

  • Plumptre, A. J., and Reynolds, V. (1994). The effect of selective logging on the primate populations in the Budongo Forest Reserve, Uganda. J. Appl. Ecol. 31: 631–641.

    Google Scholar 

  • Plumptre, A. J., Masozera, M., Fashing, P. J., McNeilage, A., Ewango, C., Kaplin, B., and Liengola, I. (2002). Biodiversity surveys of the Nyungwe Forest Reserve in S. W. Rwanda. WCS Working Papers No. 18.

  • Rahm, U. H. (1970). Ecology, zoogeography, and systematics of some African forest monkeys. In Napier, J. R., and Napier, P. H. (eds.), Old World Monkeys, Academic Press, New York, pp. 589–626.

    Google Scholar 

  • Randler, C. (2002). Avian hybridization, mixed pairing and female choice. Anim. Behav. 63: 103–119.

    Google Scholar 

  • Rhymer, J. M., and Simberloff, D. (1996). Extinction by hybridization and introgression. Annu. Rev. Ecol. Syst. 27: 83–109.

    Google Scholar 

  • Rieseberg, L. H. (1997). Hybrid origins of plant species. Annu. Rev. Ecol. Syst. 28: 359–389.

    Google Scholar 

  • Salzburger, W., Baric, S., and Sturmbauer, C. (2002). Speciation via introgressive hybridization in East African cichlids? Mol. Ecol. 11: 619–625.

    CAS  PubMed  Google Scholar 

  • Samuels, A., and Altmann, J. (1986). Immigration of a Papio anubis male into a group of cynocephalus baboons and evidence for a anubis-cynocephalus hybrid zone in Amboseli, Kenya. Int. J. Primatol. 7: 131–138.

    Google Scholar 

  • Sheppard, D. J. (2000). Ecology of the Budongo Forest Redtail: Patterns of Habitat Use and Population Density in Primary and Regenerating Forest Sites, M.Sc. Thesis, The University of Calgary, Calgary.

  • Shotake, T. (1982). Population genetical study of natural hybridization between Papio anubis and Papio hamadryas. Primates 23: 285–308.

    Google Scholar 

  • Stanford, C. (1998). Chimpanzee and Red Colobus: the Ecology of Predator and Prey, Harvard University Press, Cambridge.

    Google Scholar 

  • Struhsaker, T. T. (1970). Phylogenetic implications of some vocalizations of Cercopithecus monkeys. In Napier, J. R., and Napier, P. H. (eds.), Old World Monkeys, Academic Press, New York, pp. 365–444.

    Google Scholar 

  • Struhsaker, T. T., Butynski, T. M., and Lwanga, J. S. (1988). Hybridization between redtail (Cercopithecus ascanius schmidti) and blue (C. mitis stuhlmanni) monkeys in the Kibale Forest, Uganda. In Gautier-Hion, A., Bourliere, F., Gautier, J. -P., Kingdon, J. (eds.), A Primate Radiation: Evolutionary Biology of the African Guenons, Cambridge University Press, Cambridge, pp. 477–497.

    Google Scholar 

  • Suzuki, A. (1979). The variation and adaptation of social groups of chimpanzees and black and white colobus monkeys. In Bernstein, I. S., and Smith, E. O. (eds.), Primate Ecology and Human Origins, Garland STPM Press, New York, pp. 153–174.

    Google Scholar 

  • Tooze, Z. (1995). Update on Sclater’s guenon Cercopithecus sclateri in southern Nigeria. African Primates 1(2): 38–42.

    Google Scholar 

  • Tosi, A. J., Morales, J. C., and Melnick, D. J. (2002). Y-chromosome and mitochondrial markers in Macaca fascicularis indicate introgression with Indochinese M. mulatta and a biogeographic barrier in the Isthmus of Kra. Int. J. Primatol. 23: 161–178.

    Google Scholar 

  • Tosi, A. J., Morales, J. C., and Melnick, D. J. (2003). Paternal, maternal, and biparental molecular markers provide unique windows onto the evolutionary history of macaque monkeys. Evolution 57(6): 1419–1435.

    CAS  PubMed  Google Scholar 

  • Tutin, C. E. G. (1999). Fragmented living: behavioral ecology of primates in a forest fragment in the Lopé Reserve, Gabon. Primates 40(1): 249–265.

    Google Scholar 

  • Tutin, C. E. G., White, L. J. T., and Mackanga-Missandzou, A. (1997). The use by rain forest mammals of natural forest fragments in an equatorial African savanna. Cons. Biol. 11(5): 1190–1203.

    Google Scholar 

  • Tweheyo, M., and Obua, J. (2001). Feeding habits of chimpanzees (Pan troglodytes), red-tail monkeys (Cercopithecus ascanius schmidti) and blue monkeys (Cercopithecus mitis stuhlmanni) on figs in Budongo Forest Reserve, Uganda. Afr. J. Ecol. 39: 133–139.

    Google Scholar 

  • Twinomugisha, D., Basuta, G. I., and Chapman, C. A. (2003). Status and ecology of the golden monkey (Cercopithecus mitis kandti) in Mgahinga Gorilla National Park, Uganda. Afr. J. Ecol. 41: 47–55.

    Google Scholar 

  • Woodruff, D. S. (1973). Natural hybridization and hybrid zones. Syst. Zool. 22: 213–217.

    Google Scholar 

  • Woolley-Barker, T. (1999). Social Organization and Genetic Structure in a Baboon Hybrid Zone, Ph.D. Thesis, New York University, New York.

  • WWF. (2003). Biological Priorities for Conservation in the Guinean-Congolian Forest and Freshwater Region. WWF-US/CARPO, Washington, DC.

  • Zinner, D., Peláez, P., Torkler, F., and Berhane, D. (2003). Primates of Eritrea – current distribution and habitat. African Primates 5: 7–17.

    Google Scholar 

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Detwiler, K.M., Burrell, A.S. & Jolly, C.J. Conservation Implications of Hybridization in African Cercopithecine Monkeys. Int J Primatol 26, 661–684 (2005). https://doi.org/10.1007/s10764-005-4372-0

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