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

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.

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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.

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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

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Keywords

  • Ecotone
  • Guenon evolution
  • Introgression
  • Mosaic hybrid zone
  • Natural hybridization