Skip to main content

Advertisement

SpringerLink
Log in

Climate and Land Cover Analysis Suggest No Strong Ecological Barriers to Gene Flow in a Natural Baboon Hybrid Zone

  • Published:
International Journal of Primatology Aims and scope Submit manuscript

Abstract

Admixture between diverging taxa has made, and continues to make, an important contribution to primate diversity and evolution. However, although naturally occurring hybrids have now been documented in all major primate lineages, we still know relatively little about the factors that shape when and where admixture occurs. Baboons (genus Papio), in which multiple natural hybrid zones are well described, provide a valuable system to investigate these factors. Here, we combined Geographic Information Systems and weather station data with information on genetically characterized populations in southern Kenya to investigate if ecological variables present a potential barrier to gene flow between anubis baboons and yellow baboons in the region. Specifically, we asked if altitude, seasonal temperature, or seasonal precipitation differ for weather stations in anubis, yellow, or hybrid ranges in southern Kenya, and if land cover or altitude covary with population ancestry near the hybrid zone. Our analyses suggest that the range of yellow baboons in Kenya is climatically distinct from the range of anubis baboons, with hybrids in intermediate regions. However, we identified no clear pattern of climate or land cover differentiation near the hybrid zone itself. Thus, when yellow baboons and anubis baboons come into contact, our data suggest that the resulting population composition is not consistently predicted by the ecological variables we considered. Our results support the designation of baboons as highly flexible “generalists,” and suggest that more fine-grained analyses (e.g., relative success in ecologically stressful years) may be necessary to detect clear signals of ecological barriers to gene flow.

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

Similar content being viewed by others

References

  • Ackermann, R. R., Rogers, J., & Cheverud, J. M. (2006). Identifying the morphological signatures of hybridization in primate and human evolution. Journal of Human Evolution, 51(6), 632–645.

    Article  PubMed  Google Scholar 

  • Ackermann, R. R., Schroeder, L., Rogers, J., & Cheverud, J. M. (2014). Further evidence for phenotypic signatures of hybridization in descendant baboon populations. Journal of Human Evolution, 76, 54–62.

    Article  PubMed  PubMed Central  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(4), 139–154.

    Article  PubMed  CAS  Google Scholar 

  • Alberts, S. C., Watts, H. E., & Altmann, J. (2003). Queuing and queue-jumping: long-term patterns of reproductive skew in male savannah baboons, Papio cynocephalus. Animal Behaviour, 65(4), 821–840.

    Article  Google Scholar 

  • Altmann, J., & Muruthi, P. (1988). Differences in daily life between semiprovisioned and wild-feeding baboons. American Journal of Primatology, 15(3), 213–221.

    Article  PubMed  Google Scholar 

  • Altmann, J., Combes, S. L., & Alberts, S. C. (2013). Papio cynocephalus, yellow baboon. In T. M. Butynski, J. Kingdon, & J. Kalina (Eds.), Mammals of Africa (Vol. 2). London: Bloomsbury.

    Google Scholar 

  • Anderson, E., & Stebbins, G. L. (1954). Hybridization as an evolutionary stimulus. Evolution, 8(4), 378–388.

    Article  Google Scholar 

  • Arnold, M. L. (1992). Natural hybridization as an evolutionary process. Annual Review of Ecology and Systematics, 23, 237–261.

    Article  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Barton, N. H. (1989). Adaptation, speciation and hybrid zones. Nature, 341, 497–503.

    Article  PubMed  CAS  Google Scholar 

  • Barton, N. H. (2001). The role of hybridization in evolution. Molecular Ecology, 10(3), 551–568.

    Article  PubMed  CAS  Google Scholar 

  • Beehner, J. C., & Bergman, T. J. (2006). Female behavioral strategies of hybrid baboons in the awash National Park, Ethiopia. In L. Swedell & S. Leigh (Eds.), Reproduction and fitness in baboons: behavioral, ecological, and life history perspectives (pp. 53–79). Developments in Primatology: Progress and Prospects. New York: Springer Science+Business Media.

  • Beehner, J. C., Onderdonk, D. A., Alberts, S. C., & Altmann, J. (2006). The ecology of conception and pregnancy failure in wild baboons. Behavioral Ecology, 17(5), 741–750.

    Article  Google Scholar 

  • Bergman, T. J., Phillips-Conroy, J. E., & Jolly, C. J. (2008). Behavioral variation and reproductive success of male baboons (Papio anubis× Papio hamadryas) in a hybrid social group. American Journal of Primatology, 70(2), 136–147.

    Article  PubMed  Google Scholar 

  • Charpentier, M. J. E., Tung, J., Altmann, J., & Alberts, S. C. (2008). Age at maturity in wild baboons: genetic, environmental and demographic influences. Molecular Ecology, 17(8), 2026–2040.

    Article  PubMed  CAS  Google Scholar 

  • Charpentier, M. J., Fontaine, M. C., Cherel, E., Renoult, J. P., Jenkins, T., et al (2012). Genetic structure in a dynamic baboon hybrid zone corroborates behavioural observations in a hybrid population. Molecular Ecology, 21(3), 715–731.

    Article  PubMed  CAS  Google Scholar 

  • de Jong, Y. A., & Butynski, T. M. (2010). Photographic maps of the primates of Kenya and Tanzania: a tool for identification and conservation. Primate Conservation, 25, 27–32.

    Article  Google Scholar 

  • de Manuel, M., Kuhlwilm, M., Frandsen, P., Sousa, V. C., Desai, T., et al (2016). Chimpanzee genomic diversity reveals ancient admixture with bonobos. Science, 354(6311), 477–481.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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 

  • Dunn, J., Cardini, A., & Elton, S. (2013). Biogeographic variation in the baboon: dissecting the cline. Journal of Anatomy, 223(4), 337–352.

    Article  PubMed  PubMed Central  Google Scholar 

  • Eastman, J. (2003). IDRISI Kilimanjaro: guide to GIS and image processing. Worcester: Clark Labs, Clark University.

    Google Scholar 

  • Fischer, J., Kopp, G. H., Dal Pesco, F., Goffe, A., Hammerschmidt, K., et al (2017). Charting the neglected West: the social system of Guinea baboons. American Journal of Physical Anthropology, 162(S63), 15–31.

    Article  PubMed  PubMed Central  Google Scholar 

  • Gesquiere, L. R., Khan, M., Shek, L., Wango, T. L., Wango, E. O., et al (2008). Coping with a challenging environment: effects of seasonal variability and reproductive status on glucocorticoid concentrations of female baboons (Papio cynocephalus). Hormones and Behavior, 54(3), 410–416.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Gesquiere, L. R., Onyango, P. O., Alberts, S. C., & Altmann, J. (2011). Endocrinology of year-round reproduction in a highly seasonal habitat: Environmental variability in testosterone and glucocorticoids in baboon males. American Journal of Physical Anthropology, 144(2), 169–176.

    Article  PubMed  Google Scholar 

  • Green, R. E., Krause, J., Briggs, A. W., Maricic, T., Stenzel, U., et al (2010). A draft sequence of the Neandertal genome. Science, 328(5979), 710–722.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Hatfield, T., & Schluter, D. (1999). Ecological speciation in sticklebacks: Environment-dependent hybrid fitness. Evolution, 53, 866–873.

    Article  PubMed  Google Scholar 

  • Hoekstra, H. (2006). Genetics, development and evolution of adaptive pigmentation in vertebrates. Heredity, 97(3), 222–234.

    Article  PubMed  CAS  Google Scholar 

  • Hubbard, J. K., Uy, J. A. C., Hauber, M. E., Hoekstra, H. E., & Safran, R. J. (2010). Vertebrate pigmentation: From underlying genes to adaptive function. Trends in Genetics, 26(5), 231–239.

    Article  PubMed  CAS  Google Scholar 

  • Hutchinson, G. E. (1957). Concluding remarks. Cold Spring Harbor Symposium on Quantitative Biology, 22, 415–427.

    Article  Google Scholar 

  • Jiggins, C. D., & Mallet, J. (2000). Bimodal hybrid zones and speciation. Trends in Ecology & Evolution, 15(6), 250–255.

    Article  CAS  Google Scholar 

  • Jolly, C. J. (1993). Species, subspecies, and baboon systematics. In W. H. Kimbel & L. B. Martin (Eds.), Species, species concepts, and primate evolution (pp. 67–107). New York: Plenum Press.

    Chapter  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(S33), 177–204.

    Article  Google Scholar 

  • Jolly, C. J., Burrell, A. S., Phillips-Conroy, J. E., Bergey, C., & Rogers, J. (2011). Kinda baboons (Papio kindae) and grayfoot chacma baboons (P. ursinus griseipes) hybridize in the Kafue river valley, Zambia. American Journal of Primatology, 73(3), 291–303.

    Article  PubMed  CAS  Google Scholar 

  • Kahle, D., & Wickham, H. (2013). ggmap: spatial visualization with ggplot2. The R Journal, 5(1), 144–161.

    Article  Google Scholar 

  • Keller, C., Roos, C., Groeneveld, L., Fischer, J., & Zinner, D. (2010). Introgressive hybridization in southern African baboons shapes patterns of mtDNA variation. American Journal of Physical Anthropology, 142(1), 125–136.

    PubMed  CAS  Google Scholar 

  • Kingdon, J. (1997). The Kingdon field guide to African mammals. London: Academic Press.

    Google Scholar 

  • Kuhlwilm, M., Gronau, I., Hubisz, M. J., de Filippo, C., Prado-Martinez, J., et al (2016). Ancient gene flow from early modern humans into Eastern Neanderthals. Nature, 530(7591), 429–433.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Lewontin, R. C., & Birch, L. C. (1966). Hybridization as a source of variation for adaptation to new environments. Evolution, 20(3), 315–336.

    Article  PubMed  CAS  Google Scholar 

  • Malukiewicz, J., Boere, V., Fuzessy, L. F., Grativol, A. D., de Oliveira e Silva, I., et al (2015). Natural and anthropogenic hybridization in two species of eastern Brazilian marmosets (Callithrix jacchus and C. penicillata). PloS ONE, 10(6), e0127268.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Markham, A., & Altmann, J. (2008). Remote monitoring of primates using automated GPS technology in open habitats. American Journal of Primatology, 70(5), 495–499.

    Article  PubMed  Google Scholar 

  • Markham, A. C., Guttal, V., Alberts, S. C., & Altmann, J. (2013). When good neighbors don't need fences: Temporal landscape partitioning among baboon social groups. Behavioral Ecology and Sociobiology, 67(6), 875–884.

    Article  PubMed  PubMed Central  Google Scholar 

  • McKinnon, J. S., & Rundle, H. D. (2002). Speciation in nature: The threespine stickleback model systems. Trends in Ecology & Evolution, 17(10), 480–488.

    Article  Google Scholar 

  • Morris, W. F., Altmann, J., Brockman, D. K., Cords, M., Fedigan, L. M., et al (2010). Low demographic variability in wild primate populations: fitness impacts of variation, covariation, and serial correlation in vital rates. The American Naturalist, 177(1), E14–E28.

    Article  PubMed  PubMed Central  Google Scholar 

  • Nagel, U. (1973). A comparison of anubis baboons, hamadryas baboons and their hybrids at a species border in Ethiopia. Folia Primatologica, 19(2–3), 104–165.

    Article  CAS  Google Scholar 

  • Osada, N., Uno, Y., Mineta, K., Kameoka, Y., Takahashi, I., & Terao, K. (2010). Ancient genome-wide admixture extends beyond the current hybrid zone between Macaca fascicularis and M. mulatta. Molecular Ecology, 19(14), 2884–2895.

    Article  PubMed  CAS  Google Scholar 

  • Palombit, R. A. (2013). Papio anubis, olive baboon (Anubis baboon). In T. M. Butynski, J. Kingdon, & J. Kalina (Eds.), Mammals of Africa (Vol. 2). London: Bloomsbury.

    Google Scholar 

  • Phillips-Conroy, J. E., & Jolly, C. J. (1981). Sexual dimorphism in two subspecies of Ethiopian baboons (Papio hamadryas) and their hybrids. American Journal of Physical Anthropology, 56(2), 115–129.

    Article  PubMed  CAS  Google Scholar 

  • Phillips-Conroy, J. E., & 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(3), 337–350.

    Article  Google Scholar 

  • Phillips-Conroy, J. E., 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(3), 353–368.

    Article  PubMed  CAS  Google Scholar 

  • Prüfer, K., Racimo, F., Patterson, N., Jay, F., Sankararaman, S., et al (2014). The complete genome sequence of a Neanderthal from the Altai Mountains. Nature, 505(7481), 43–49.

    Article  PubMed  CAS  Google Scholar 

  • R Core Team (2015). R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing.

    Google Scholar 

  • Rundle, H. D., & Nosil, P. (2005). Ecological speciation. Ecology Letters, 8(3), 336–352.

    Article  Google Scholar 

  • Samuels, A., & Altmann, J. (1986). Immigration of a Papio anubis male into a group of Papio cynocephalus baboons and evidence for an anubis-cynocephalus hybrid zone in Amboseli, Kenya. International Journal of Primatology, 7(2), 131–138.

    Article  Google Scholar 

  • Sankararaman, S., Patterson, N., Li, H., Pääbo, S., & Reich, D. (2012). The date of interbreeding between Neandertals and modern humans. PLoS Genetics, 8(10), e1002947.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Schluter, D. (2009). Evidence for ecological speciation and its alternative. Science, 323(5915), 737–741.

    Article  PubMed  CAS  Google Scholar 

  • Schott, F. A., Xie, S. P., & McCreary, J. P. (2009). Indian Ocean circulation and climate variability. Reviews of Geophysics, 47(1), RG1002.

  • Seehausen, O., Takimoto, G., Roy, D., & Jokela, J. (2008). Speciation reversal and biodiversity dynamics with hybridization in changing environments. Molecular Ecology, 17(1), 30–44.

    Article  PubMed  Google Scholar 

  • Ségurel, L., & Quintana-Murci, L. (2014). Preserving immune diversity through ancient inheritance and admixture. Current Opinion in Immunology, 30, 79–84.

    Article  PubMed  CAS  Google Scholar 

  • Shurtliff, Q. R., Murphy, P. J., & Matocq, M. D. (2014). Ecological segregation in a small mammal hybrid zone: Habitat-specific mating opportunities and selection against hybrids restrict gene flow on a fine spatial scale. Evolution, 68(3), 729–742.

    Article  PubMed  Google Scholar 

  • Strandburg-Peshkin, A., Farine, D. R., Crofoot, M. C., & Couzin, I. D. (2017). Habitat and social factors shape individual decisions and emergent group structure during baboon collective movement. eLife, 6, e19505.

    Article  PubMed  PubMed Central  Google Scholar 

  • Svardal, H., Jasinska, A., Apetrei, C., Coppola, G., Huang, Y., et al. (2016). Ancient hybridization and strong adaptation to viruses across African vervet monkey populations. bioRxiv, 088989.

  • Taylor, S. A., White, T. A., Hochachka, W. M., Ferretti, V., Curry, R. L., & Lovette, I. (2014). Climate-mediated movement of an avian hybrid zone. Current Biology, 24(6), 671–676.

    Article  PubMed  CAS  Google Scholar 

  • Tung, J., Charpentier, M. J. E., Garfield, D. A., Altmann, J., & Alberts, S. C. (2008). Genetic evidence reveals temporal change in hybridization patterns in a wild baboon population. Molecular Ecology, 17(8), 1998–2011.

    Article  PubMed  CAS  Google Scholar 

  • Tung, J., Charpentier, M. J., Mukherjee, S., Altmann, J., & Alberts, S. C. (2012). Genetic effects on mating success and partner choice in a social mammal. American Naturalist, 180(1), 113–129.

    Article  PubMed  Google Scholar 

  • Wall, J. D., & Brandt, D. Y. C. (2016). Archaic admixture in human history. Current Opinion in Genetics & Development, 41, 93–97.

    Article  CAS  Google Scholar 

  • Wall, J. D., Schlebusch, S. A., Alberts, S. C., Cox, L. A., Snyder-Mackler, N., et al (2016). Genomewide ancestry and divergence patterns from low-coverage sequencing data reveal a complex history of admixture in wild baboons. Molecular Ecology, 25(14), 3469–3483.

    Article  PubMed  PubMed Central  Google Scholar 

  • Winder, I. C. (2015). The biogeography of the Papio baboons: a GIS-based analysis of range characteristics and variability. Folia Primatologica, 85(5), 292–318.

    Article  Google Scholar 

  • Zinner, D., Groeneveld, L. F., Keller, C., & Roos, C. (2009). Mitochondrial phylogeography of baboons (Papio spp.): indication for introgressive hybridization? BMC Evolutionary Biology, 9(1), 83.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Zinner, D., Buba, U., Nash, S., & Roos, C. (2011b). Pan-African voyagers: the phylogeography of baboons. In Primates of Gashaka (pp. 319–358). Developments in primatology: Progress and prospects. New York: Springer Science+Business Media.

  • Zinner, D., Wertheimer, J., Liedigk, R., Groeneveld, L. F., & Roos, C. (2013). Baboon phylogeny as inferred from complete mitochondrial genomes. American Journal of Physical Anthropology, 150(1), 133–140.

    Article  PubMed  PubMed Central  Google Scholar 

  • Zinner, D., Keller, C., Nyahongo, J. W., Butynski, T. M., de Jong, Y. A., et al (2015). Distribution of mitochondrial clades and morphotypes of baboons Papio spp.(Primates: Cercopithecidae) in Eastern Africa. Journal of East African Natural History, 104(1–2), 143–168.

    Article  Google Scholar 

Download references

Acknowledgements

We thank the Kenya Wildlife Service, Institute of Primate Research, National Museums of Kenya, National Council for Science and Technology, University of Nairobi, members of the Amboseli–Longido pastoralist communities, Tortilis Camp, and Ker and Downey Safaris for their assistance in Kenya. We also thank two anonymous reviewers for constructive comments on an earlier version of the manuscript, Kenneth Chiou for the map of the baboon species distributions modified here, and the editors of this Special Issue (Dietmar Zinner, Liliana Cortes-Ortiz, and Christian Roos) for the opportunity to contribute. T. L. Wango was supported by a grant from the Patricia William Mwangaza Foundation; weather data collection at Amboseli was supported by the National Science Foundation IOS 0919200 and IOS 1456832.

Author information

Author notes

  1. Susan C. Alberts and Jenny Tung contributed equally to this work.

Authors and Affiliations

  1. Department of Geomatic Engineering and Geospatial Information Systems, Jomo Kenyatta University of Agriculture and Technology, Nairobi, Kenya

    Tim L. Wango & Douglas Musiega

  2. Department of Veterinary Anatomy and Physiology, University of Nairobi, Nairobi, Kenya

    Tim L. Wango

  3. Department of Geomatic and Geospatial Information Systems, Dedan Kimathi University of Technology, Nyeri, Kenya

    Charles N. Mundia

  4. Department of Ecology and Evolutionary Biology, Princeton University, Princeton, NJ, 08544, USA

    Jeanne Altmann

  5. Institute of Primate Research, Nairobi, Kenya

    Jeanne Altmann, Susan C. Alberts & Jenny Tung

  6. Department of Evolutionary Anthropology, Duke University, Durham, NC, 27708, USA

    Susan C. Alberts & Jenny Tung

  7. Department of Biology, Duke University, Durham, NC, 27708, USA

    Susan C. Alberts & Jenny Tung

  8. Duke University Population Research Institute, Duke University, Durham, NC, 27710, USA

    Jenny Tung

Authors
  1. Tim L. Wango
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Douglas Musiega
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Charles N. Mundia
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jeanne Altmann
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Susan C. Alberts
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Jenny Tung
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jenny Tung.

Additional information

Handling Editor: Joanna M. Setchell

Electronic supplementary material

ESM 1

(XLSX 80 kb)

ESM 2

(PDF 4122 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wango, T.L., Musiega, D., Mundia, C.N. et al. Climate and Land Cover Analysis Suggest No Strong Ecological Barriers to Gene Flow in a Natural Baboon Hybrid Zone. Int J Primatol 40, 53–70 (2019). https://doi.org/10.1007/s10764-017-9989-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10764-017-9989-2

Keywords

Search

Navigation