Book contents
- The Chimpanzees of the Taï Forest
- The Chimpanzees of the Taï Forest
- Copyright page
- Dedication
- Contents
- Contributors
- Preface
- Acknowledgements
- 1 War and peace in the Taï chimpanzee forest: running a long-term chimpanzee research project
- 2 Developments in statistical methods applied over four decades of research in the Taï Chimpanzee Project
- 3 Observation protocol and long-term data collection in Taï
- 4 The Wild Chimpanzee Foundation (WCF) and the Taï Chimpanzee Project (TCP)
- 5 Insights from genetic analyses of the Taï chimpanzees
- 6 Endocrinological analyses at Taï
- 7 Chimpanzee behavioural diversity and the contribution of the Taï Chimpanzee Project
- 8 An energetic model of foraging optimization: wild chimpanzee hammer selection for nut-cracking
- 9 Demography and life history of five chimpanzee communities in Taï National Park
- 10 Adoption in the Taï chimpanzees: costs, benefits and strong social relationships
- 11 Spatial integration of unusually high numbers of immigrant females into the South Group: further support for the bisexually bonded model in Taï chimpanzees
- 12 Forty years striving to capture culture among the Taï chimpanzees
- 13 Cultural diversity of nut-cracking behaviour between two populations of wild chimpanzees (Pan troglodytes verus) in the Côte d’Ivoire
- 14 Ecological and social influences on rates of social play in immature wild chimpanzees (Pan troglodytes verus)
- 15 Long-term diet of the chimpanzees (Pan troglodytes verus) in Taï National Park: interannual variations in consumption
- 16 Why Taï mangabeys do not use tools to crack nuts like sympatric-living chimpanzees: a cognitive limitation on monkey feeding ecology
- 17 Providing research for conservation from long-term field sites
- 18 Rank changes in female chimpanzees in Taï National Park
- 19 Effects of large-scale knockouts on chimpanzee association networks
- 20 Why do the chimpanzees of the Taï Forest share meat? The value of bartering, begging and hunting
- 21 Group-specific social dynamics affect urinary oxytocin levels in Taï male chimpanzees
- 22 The chimpanzees of the Taï Forest as models for hominine microorganism ecology and evolution
- 23 Acute infectious diseases occurring in the Taï chimpanzee population: a review
- 24 Why does the chimpanzee vocal repertoire remain poorly understood and what can be done about it?
- 25 Evidence for sexual dimorphism in chimpanzee vocalizations: a comparison of male and female call production and acoustic parameters
- 26 Gestural usage and development in two chimpanzee groups of different subspecies (Pan troglodytes verus/P.t. schweinfurthii)
- 27 Spatial cognitive abilities in foraging chimpanzees
- 28 Temporal cognition in Taï chimpanzees
- Index
- References
22 - The chimpanzees of the Taï Forest as models for hominine microorganism ecology and evolution
Published online by Cambridge University Press: 25 November 2019
Book contents
- The Chimpanzees of the Taï Forest
- The Chimpanzees of the Taï Forest
- Copyright page
- Dedication
- Contents
- Contributors
- Preface
- Acknowledgements
- 1 War and peace in the Taï chimpanzee forest: running a long-term chimpanzee research project
- 2 Developments in statistical methods applied over four decades of research in the Taï Chimpanzee Project
- 3 Observation protocol and long-term data collection in Taï
- 4 The Wild Chimpanzee Foundation (WCF) and the Taï Chimpanzee Project (TCP)
- 5 Insights from genetic analyses of the Taï chimpanzees
- 6 Endocrinological analyses at Taï
- 7 Chimpanzee behavioural diversity and the contribution of the Taï Chimpanzee Project
- 8 An energetic model of foraging optimization: wild chimpanzee hammer selection for nut-cracking
- 9 Demography and life history of five chimpanzee communities in Taï National Park
- 10 Adoption in the Taï chimpanzees: costs, benefits and strong social relationships
- 11 Spatial integration of unusually high numbers of immigrant females into the South Group: further support for the bisexually bonded model in Taï chimpanzees
- 12 Forty years striving to capture culture among the Taï chimpanzees
- 13 Cultural diversity of nut-cracking behaviour between two populations of wild chimpanzees (Pan troglodytes verus) in the Côte d’Ivoire
- 14 Ecological and social influences on rates of social play in immature wild chimpanzees (Pan troglodytes verus)
- 15 Long-term diet of the chimpanzees (Pan troglodytes verus) in Taï National Park: interannual variations in consumption
- 16 Why Taï mangabeys do not use tools to crack nuts like sympatric-living chimpanzees: a cognitive limitation on monkey feeding ecology
- 17 Providing research for conservation from long-term field sites
- 18 Rank changes in female chimpanzees in Taï National Park
- 19 Effects of large-scale knockouts on chimpanzee association networks
- 20 Why do the chimpanzees of the Taï Forest share meat? The value of bartering, begging and hunting
- 21 Group-specific social dynamics affect urinary oxytocin levels in Taï male chimpanzees
- 22 The chimpanzees of the Taï Forest as models for hominine microorganism ecology and evolution
- 23 Acute infectious diseases occurring in the Taï chimpanzee population: a review
- 24 Why does the chimpanzee vocal repertoire remain poorly understood and what can be done about it?
- 25 Evidence for sexual dimorphism in chimpanzee vocalizations: a comparison of male and female call production and acoustic parameters
- 26 Gestural usage and development in two chimpanzee groups of different subspecies (Pan troglodytes verus/P.t. schweinfurthii)
- 27 Spatial cognitive abilities in foraging chimpanzees
- 28 Temporal cognition in Taï chimpanzees
- Index
- References
Summary
Microbial communities impact a variety of processes including a host’s ability to access nutrients and maintain health, but can also include pathogens with a detrimental impact. Since the spread of anatomically modern humans across the planet, we have drastically changed the way we live (e.g. agriculture, antibiotic usage). These changes presumably affected our microbial communities. To examine the microbial communities of our ancestors, researchers use two approaches: first, the study of present-day hunter-gatherer societies, suggesting modern humans lost much of their microbial diversity; second, comparative analyses of our closest relatives in their natural environment. We review studies of the microorganisms in the chimpanzees of Taï National Park (particularly bacteria and retroviruses). We discuss how microorganisms are transmitted between chimpanzees, which microorganisms coevolved with their hosts and which were transmitted between chimpanzees and their prey. We examine how the close evolutionary relationship of primates and humans facilitates the zoonotic transmission of microorganisms and how disease ecology informs assessments of human disease risk.
Keywords
- Type
- Chapter
- Information
- The Chimpanzees of the Taï Forest40 Years of Research, pp. 366 - 384Publisher: Cambridge University PressPrint publication year: 2019
References
Adlhoch, C., Kaiser, M., Loewa, A., Ulrich, M., Forbrig, C., Adjogoua, E. V., et al. (2012). Diversity of parvovirus 4-like viruses in humans, chimpanzees, and monkeys in hunter-prey relationships. Emerging Infectious Diseases, 18, 859–862. https://doi.org/10.3201/eid1805.111849CrossRefGoogle ScholarPubMed
Aivelo, T., Laakkonen, J. & Jernvall, J. (2016). Population- and individual-level dynamics of the intestinal microbiota of a small primate. Applied and Environmental Microbiology, 82, 3537–3545.Google Scholar
Alais, S., Pasquier, A., Jegado, B., Journo, C., Rua, R., Gessain, A., et al. (2018). STLV-1 co-infection is correlated with an increased SFV proviral load in the peripheral blood of SFV/STLV-1 naturally infected non-human primates. PLoS Neglected Tropical Diseases, 12(10), e0006812. https://doi.org/10.1371/journal.pntd.0006812Google Scholar
Ali, M., Taylor, G. P., Pitman, R. J., Parker, D., Rethwilm, A., Cheingsong-Popov, R., et al. (1996). No evidence of antibody to human foamy virus in widespread human populations. AIDS Research and Human Retroviruses, 12, 1473–1483.Google Scholar
Amato, K. R., Yeoman, C. J., Kent, A., Righini, N., Carbonero, F., Estrada, A., et al. (2013). Habitat degradation impacts black howler monkey (Alouatta pigra) gastrointestinal microbiomes. The ISME Journal, 7, 1344–1353.CrossRefGoogle ScholarPubMed
Anoh, A. E., Murthy, S., Akoua-Koffi, C., Couacy-Hymann, E., Leendertz, F. H., Calvignac-Spencer, S., et al. (2017). Cytomegaloviruses in a community of wild nonhuman primates in Taï National Park, Côte d’Ivoire. Viruses, 10, 11.Google Scholar
Anthony, S. J., Islam, A., Johnson, C., Navarrete-Macias, I., Liang, E., Jain, K., et al. (2015). Non-random patterns in viral diversity. Nature Communications, 6, 8147.Google Scholar
Ayouba, A., Akoua-Koffi, C., Calvignac-Spencer, S., Esteban, A., Locatelli, S., Li, H., et al. (2013). Evidence for continuing cross-species transmission of SIVsmm to humans: characterization of a new HIV-2 lineage in rural Côte d’Ivoire. AIDS, 27(15).Google Scholar
Barelli, C., Albanese, D., Donati, C., Pindo, M., Dallago, C., Rovero, F., et al. (2015). Habitat fragmentation is associated to gut microbiota diversity of an endangered primate: implications for conservation. Scientific Reports, 5, 14862.CrossRefGoogle ScholarPubMed
Barr, J. J., Auro, R., Furlan, M., Whiteson, K. L., Erb, M. L., Pogliano, J., et al. (2013). Bacteriophage adhering to mucus provide a non–host-derived immunity. Proceedings of the National Academy of Sciences of the United States of America, 110, 10,771–10,776.Google Scholar
Behringer, V., Stevens, J. M., Leendertz, F. H., Hohmann, G. & Deschner, T. (2017). Validation of a method for the assessment of urinary neopterin levels to monitor health status in non-human-primate species. Frontiers in Physiology, 8, 51.CrossRefGoogle ScholarPubMed
Betsem, E., Rua, R., Tortevoye, P., Froment, A. & Gessain, A. (2011). Frequent and recent human acquisition of simian foamy viruses through apes’ bites in central Africa. PLoS Pathogens, 7(10), e1002306.Google Scholar
Blasse, A., Calvignac-Spencer, S., Merkel, K., Goffe, A. S., Boesch, C., Mundry, R., et al. (2013). Mother–offspring transmission and age-dependent accumulation of simian foamy virus in wild chimpanzees. Journal of Virology, 87, 5193–5204.CrossRefGoogle ScholarPubMed
Boesch, C. & Boesch-Achermann, H. (2000). The Chimpanzees of the Taï Forest: Behavioural Ecology and Evolution. Oxford: Oxford University Press.CrossRefGoogle Scholar
Calvignac-Spencer, S., Adjogoua, E. V., Akoua-Koffi, C., Hedemann, C., Schubert, G., Ellerbrok, H., et al. (2012a). Origin of human T-lymphotropic virus type 1 in rural Côte d’Ivoire. Emerging Infectious Diseases, 18, 830–833.Google Scholar
Calvignac-Spencer, S., Leendertz, S. A. J., Gillespie, T. R. & Leendertz, F. H. (2012b). Wild great apes as sentinels and sources of infectious disease. Clinical Microbiology and Infection, 18, 521–527.Google Scholar
Chi, F., Leider, M., Leendertz, F., Bergmann, C., Boesch, C., Schenk, S., et al. (2007). New Streptococcus pneumoniae clones in deceased wild chimpanzees. Journal of Bacteriology, 189, 6085–6088.Google Scholar
Clayton, J. B., Vangay, P., Huang, H., Ward, T., Hillmann, B. M., Al-Ghalith, G. A., et al. (2016). Captivity humanizes the primate microbiome. Proceedings of the National Academy of Sciences of the United States of America, 113, 10,376–10,381.CrossRefGoogle ScholarPubMed
Clemente, J. C., Pehrsson, E. C., Blaser, M. J., Sandhu, K., Gao, Z., Wang, B., et al. (2015). The microbiome of uncontacted Amerindians. Science Advances, 1(3), e1500183.Google Scholar
Compton, A. A. & Emerman, M. (2013). Convergence and divergence in the evolution of the APOBEC3G–Vif interaction reveal ancient origins of simian immunodeficiency viruses. PLoS Pathogens, 9(1), e1003135.Google Scholar
Courgnaud, V., Formenty, P., Akoua-Koffi, C., Noe, R., Boesch, C., Delaporte, E., et al. (2003). Partial molecular characterization of two simian immunodeficiency viruses (SIV) from African colobids: SIVwrc from Western red colobus (Piliocolobus badius) and SIVolc from olive colobus (Procolobus verus). Journal of Virology, 77, 744–748.Google Scholar
Degnan, P. H., Pusey, A. E., Lonsdorf, E. V., Goodall, J., Wroblewski, E. E., Wilson, M. L., et al. (2012). Factors associated with the diversification of the gut microbial communities within chimpanzees from Gombe National Park. Proceedings of the National Academy of Sciences of the United States of America, 109, 13,034–13,039. https://doi.org/10.1073/Proceedings of the National Academy of Sciences of the United States of America.1110994109Google Scholar
Denapaite, D., Rieger, M., Köndgen, S., Brückner, R., Ochigava, I., Kappeler, P., et al. (2016). Highly variable Streptococcus oralis strains are common among viridans streptococci isolated from primates. mSphere, 1(2). https://doi.org/10.1128/mSphere.00041–15Google Scholar
Dominguez-Bello, M. G., Costello, E. K., Contreras, M., Magris, M., Hidalgo, G., Fierer, N., et al. (2010). Delivery mode shapes the acquisition and structure of the initial microbiota across multiple body habitats in newborns. Proceedings of the National Academy of Sciences of the United States of America, 107, 11,971–11,975.Google Scholar
Dutilh, B. E., Cassman, N., McNair, K., Sanchez, S. E., Silva, G. G., Boling, L., et al. (2014). A highly abundant bacteriophage discovered in the unknown sequences of human faecal metagenomes. Nature Communications, 5, 4498.Google Scholar
Ezenwa, V. O. & Williams, A. E. (2014). Microbes and animal olfactory communication: Where do we go from here? BioEssays, 36, 847–854.Google Scholar
Faith, J. J., Guruge, J. L., Charbonneau, M., Subramanian, S., Seedorf, H., Goodman, A. L., et al. (2013). The long-term stability of the human gut microbiota. Science, 341(6141), 1237439.Google Scholar
Fierer, N. (2017). Embracing the unknown: disentangling the complexities of the soil microbiome. Nature Reviews Microbiology, 15, 579–590.Google Scholar
Gao, F., Bailes, E., Robertson, D. L., Chen, Y., Rodenburg, C. M., Michael, S. F., et al. (1999). Origin of HIV-1 in the chimpanzee Pan troglodytes troglodytes. Nature, 397(6718), 436–441.Google Scholar
Gessain, A., Rua, R., Betsem, E., Turpin, J. & Mahieux, R. (2013). HTLV-3/4 and simian foamy retroviruses in humans: Discovery, epidemiology, cross-species transmission and molecular virology. Virology, 435, 187–199. https://doi.org/10.1016/j.virol.2012.09.035CrossRefGoogle ScholarPubMed
Gillespie, T. R., Nunn, C. L. & Leendertz, F. H. (2008). Integrative approaches to the study of primate infectious disease: Implications for biodiversity conservation and global health. American Journal of Physical Anthropology, 137(S47), 53–69.Google Scholar
Gillings, M. R., Paulsen, I. T. & Tetu, S. G. (2015). Ecology and evolution of the human microbiota: Fire, farming and antibiotics. Genes, 6, 841–857.Google Scholar
Gogarten, J. F., Akoua-Koffi, C., Calvignac-Spencer, S., Leendertz, S. A. J., Weiss, S., Couacy-Hymann, E., et al. (2014a). The ecology of primate retroviruses – An assessment of 12 years of retroviral studies in the Taï National Park area, Côte d’Ivoire. Virology, 460, 147–153.Google Scholar
Gogarten, J. F., Bonnell, T. R., Brown, L. M., Campenni, M., Wasserman, M. D. & Chapman, C. A. (2014b). Increasing group size alters behavior of a folivorous primate. International Journal of Primatology, 35, 590–608. https://doi.org/10.1007/s10764-014–9770–8Google Scholar
Gogarten, J. F., Davies, T. J., Benjamino, J., Gogarten, J. P., Graf, J., Mielke, A., et al. (2018). Factors influencing bacterial microbiome composition in a wild non-human primate community in Taï National Park, Côte d’Ivoire. The ISME Journal, 12, 2559–2574.Google Scholar
Gogarten, J. F., Düx, A., Schuenemann, V. J., Nowak, K., Boesch, C., Wittig, R. M., et al. (2016). Tools for opening new chapters in the book of Treponema pallidum evolutionary history. Clinical Microbiology and Infection, 22, 916–921.Google Scholar
Gogarten, J. F., Jacob, A. L., Ghai, R. R., Rothman, J. M., Twinomugisha, D., Wasserman, M. D., et al. (2015). Group size dynamics over 15+ years in an African forest primate community. Biotropica, 47, 101–112.CrossRefGoogle Scholar
Goldberg, T. L., Gillespie, T. R., Rwego, I. B., Wheeler, E., Estoff, E. L. & Chapman, C. A. (2007). Patterns of gastrointestinal bacterial exchange between chimpanzees and humans involved in research and tourism in western Uganda. Biological Conservation, 135, 511–517.Google Scholar
Goldberg, T. L., Sintasath, D. M., Chapman, C. A., Cameron, K. M., Karesh, W. B., Tang, S., et al. (2009). Coinfection of Ugandan red colobus (Procolobus [Piliocolobus] rufomitratus tephrosceles) with novel, divergent delta-, lenti-, and spumaretroviruses. Journal of Virology, 83, 11,318–11,329.Google Scholar
Grabowski, M. K. & Redd, A. D. (2014). Molecular tools for studying HIV transmission in sexual networks. Current Opinion in HIV and AIDS, 9, 126.Google Scholar
Gritz, E. C. & Bhandari, V. (2015). The human neonatal gut microbiome: A brief review. Frontiers in Pediatrics, 3, 17.Google Scholar
Han, G. Z. & Worobey, M. (2012). An endogenous foamy-like viral element in the coelacanth genome. PLoS Pathogens, 8, e1002790.Google Scholar
Hehemann, J.-H., Kelly, A. G., Pudlo, N. A., Martens, E. C. & Boraston, A. B. (2012). Bacteria of the human gut microbiome catabolize red seaweed glycans with carbohydrate-active enzyme updates from extrinsic microbes. Proceedings of the National Academy of Sciences of the United States of America, 109, 19,786–19,791.Google Scholar
Hooper, L. V., Littman, D. R. & Macpherson, A. J. (2012). Interactions between the microbiota and the immune system. Science, 336(6086), 1268–1273.Google Scholar
Jirků, M., Votýpka, J., Petrželková, K. J., Jirků-Pomajbíková, K., Kriegová, E., Vodička, R., et al. (2015). Wild chimpanzees are infected by Trypanosoma brucei. International Journal for Parasitology: Parasites and Wildlife, 4, 277–282.Google ScholarPubMed
Junglen, S., Hedemann, C., Ellerbrok, H., Pauli, G., Boesch, C. & Leendertz, F. H. (2010). Diversity of STLV-1 strains in wild chimpanzees (Pan troglodytes verus) from Côte d’Ivoire. Virus Research, 150, 143–147.CrossRefGoogle ScholarPubMed
Kaur, T., Singh, J., Tong, S., Humphrey, C., Clevenger, D., Tan, W., et al. (2008). Descriptive epidemiology of fatal respiratory outbreaks and detection of a human‐related metapneumovirus in wild chimpanzees (Pan troglodytes) at Mahale Mountains National Park, Western Tanzania. American Journal of Primatology, 70, 755–765.Google Scholar
Kembel, S. W., O’Connor, T. K., Arnold, H. K., Hubbell, S. P., Wright, S. J. & Green, J. L. (2014). Relationships between phyllosphere bacterial communities and plant functional traits in a neotropical forest. Proceedings of the National Academy of Sciences of the United States of America, 111, 13,715–13,720. https://doi.org/10.1073/Proceedings of the National Academy of Sciences of the United States of America.1216057111Google Scholar
Kirchhoff, F. (2010). Immune evasion and counteraction of restriction factors by HIV-1 and other primate lentiviruses. Cell Host & Microbe, 8, 55–67.Google Scholar
Köndgen, S., Kühl, H. S., N’Goran, P. K., Walsh, P. D., Schenk, S., Ernst, N., et al. (2008). Pandemic human viruses cause decline of endangered great apes. Current Biology, 18, 260–264.Google Scholar
Korpela, K., Costea, P., Coelho, L. P., Kandels-Lewis, S., Willemsen, G., Boomsma, D. I., et al. (2018). Selective maternal seeding and environment shape the human gut microbiome. Genome Research, 28, 561–568.Google Scholar
Langergraber, K. E., Rowney, C., Schubert, G., Crockford, C., Hobaiter, C., Wittig, R. M., et al. (2014). How old are chimpanzee communities? Time to the most recent common ancestor of the Y-chromosome in highly patrilocal societies. Journal of Human Evolution, 69, 1–7.Google Scholar
Leendertz, F. H., Boesch, C., Ellerbrok, H., Rietschel, W., Couacy-Hymann, E. & Pauli, G. (2004). Non-invasive testing reveals a high prevalence of simian T-lymphotropic virus type 1 antibodies in wild adult chimpanzees of the Taï National Park, Côte d’Ivoire. Journal of General Virology, 85, 3305–3312.Google Scholar
Leendertz, F. H., Boesch, C., Junglen, S., Pauli, G. & Ellerbrok, H. (2003). Characterization of a new simian T-lymphotropic virus type 1 (STLV-1) in a wild living chimpanzee (Pan troglodytes verus) from Ivory Coast: evidence of a new STLV-1 group? AIDS Research and Human Retroviruses, 19, 255–258.Google Scholar
Leendertz, F. H., Deckers, M., Schempp, W., Lankester, F., Boesch, C., Mugisha, L., et al. (2009). Novel cytomegaloviruses in free-ranging and captive great apes: phylogenetic evidence for bidirectional horizontal transmission. Journal of General Virology, 90, 2386–2394.CrossRefGoogle ScholarPubMed
Leendertz, F. H., Scuda, N., Cameron, K. N., Kidega, T., Zuberbühler, K., Leendertz, S. A. J., et al. (2011a). African great apes are naturally infected with polyomaviruses closely related to Merkel cell polyomavirus. Journal of Virology, 85, 916–924.Google Scholar
Leendertz, F. H., Zirkel, F., Couacy-Hymann, E., Ellerbrok, H., Morozov, V. A., Pauli, G., et al. (2008). Interspecies transmission of simian foamy virus in a natural predator–prey system. Journal of Virology, 82, 7741–7744.Google Scholar
Leendertz, S. A. J., Junglen, S., Hedemann, C., Goffe, A., Calvignac, S., Boesch, C., et al.(2010). High prevalence, coinfection rate, and genetic diversity of retroviruses in wild red colobus monkeys (Piliocolobus badius badius) in Tai National Park, Cote d’Ivoire. Journal of Virology, 84, 7427–7436.CrossRefGoogle ScholarPubMed
Leendertz, S. A. J., Locatelli, S., Boesch, C., Kücherer, C., Formenty, P., Liegeois, F., et al. (2011b). No evidence for transmission of SIVwrc from western red colobus monkeys (Piliocolobus badius badius) to wild West African chimpanzees (Pan troglodytes verus) despite high exposure through hunting. BMC Microbiology, 11, 24.Google Scholar
Leibold, M. A., Holyoak, M., Mouquet, N., Amarasekare, P., Chase, J. M., Hoopes, M. F., et al. (2004). The metacommunity concept: A framework for multi‐scale community ecology. Ecology Letters, 7, 601–613.Google Scholar
Liégeois, F., Lafay, B., Formenty, P., Locatelli, S., Courgnaud, V., Delaporte, E., et al. (2009). Full-length genome characterization of a novel simian immunodeficiency virus lineage (SIVolc) from olive colobus (Procolobus verus) and new SIVwrcPbb strains from Western red colobus (Piliocolobus badius badius) from the Tai Forest in Ivory Coast. Journal of Virology, 83, 428–439.Google Scholar
Liu, W., Worobey, M., Li, Y., Keele, B. F., Bibollet-Ruche, F., Guo, Y., et al. (2008). Molecular ecology and natural history of simian foamy virus infection in wild-living chimpanzees. PLoS Pathogens, 4(7), e1000097.CrossRefGoogle ScholarPubMed
Locatelli, S., Roeder, A. D., Bruford, M. W., Noë, R., Delaporte, E. & Peeters, M. (2011). Lack of evidence of simian immunodeficiency virus infection among nonhuman primates in Tai National Park, Cote d’Ivoire: Limitations of noninvasive methods and SIV diagnostic tools for studies of primate retroviruses. International Journal of Primatology, 32, 288–307.Google Scholar
Logan, A. C., Katzman, M. A. & Balanzá-Martínez, V. (2015). Natural environments, ancestral diets, and microbial ecology: Is there a modern ‘paleo-deficit disorder’? Part II. Journal of Physiological Anthropology, 34, 9.Google Scholar
Madinda, N. F., Ehlers, B., Wertheim, J. O., Akoua-Koffi, C., Bergl, R. A., Boesch, C., et al. (2016). Assessing host-virus co-divergence for close relatives of Merkel cell polyomavirus infecting African great apes. Journal of Virology, 90, 8531–8541.Google Scholar
Malim, M. H. & Bieniasz, P. D. (2012). HIV restriction factors and mechanisms of evasion. Cold Spring Harbor Perspectives in Medicine, 2(5), a006940.Google Scholar
McGraw, W. S., Zuberbühler, K. & Noë, R. (2007). Monkeys of the Taï Forest: An African Primate Community. Cambridge: Cambridge University Press.Google Scholar
Mills, S., Shanahan, F., Stanton, C., Hill, C., Coffey, A. & Ross, R. P. (2013). Movers and shakers: Influence of bacteriophages in shaping the mammalian gut microbiota. Gut Microbes, 4, 4–16.CrossRefGoogle ScholarPubMed
Moeller, A. H., Caro-Quintero, A., Mjungu, D., Georgiev, A. V., Lonsdorf, E. V., Muller, M. N., et al. (2016a). Cospeciation of gut microbiota with hominids. Science, 353(6297), 380–382.Google Scholar
Moeller, A. H., Foerster, S., Wilson, M. L., Pusey, A. E., Hahn, B. H. & Ochman, H. (2016b). Social behavior shapes the chimpanzee pan-microbiome. Science Advances, 2(1), e1500997. https://doi.org/10.1126/sciadv.1500997Google Scholar
Moeller, A. H., Li, Y., Ngole, E. M., Ahuka-Mundeke, S., Lonsdorf, E. V., Pusey, A. E., et al. (2014). Rapid changes in the gut microbiome during human evolution. Proceedings of the National Academy of Sciences of the United States of America, 111, 16,431–16,435.Google Scholar
Moeller, A. H., Peeters, M., Ayouba, A., Ngole, E. M., Esteban, A., Hahn, B. H., et al. (2015). Stability of the gorilla microbiome despite simian immunodeficiency virus infection. Molecular Ecology, 24, 690–697.Google Scholar
Morozov, V. A., Leendertz, F. H., Junglen, S., Boesch, C., Pauli, G. & Ellerbrok, H. (2009). Frequent foamy virus infection in free-living chimpanzees of the Taï National Park (Côte d’Ivoire). Journal of General Virology, 90, 500–506.Google Scholar
Mossoun, A., Calvignac-Spencer, S., Anoh, A. E., Pauly, M. S., Driscoll, D. A., Michel, A. O., et al. (2017). Bushmeat hunting and zoonotic transmission of Simian T-lymphotropic virus 1 in tropical West and Central Africa. Journal of Virology, 91(10). https://doi.org/10.1128/jvi.02479–16Google Scholar
Mouinga-Ondémé, A., Caron, M., Nkoghé, D., Telfer, P., Marx, P., Saïb, A., et al. (2012). Cross-species transmission of simian foamy virus to humans in rural Gabon, Central Africa. Journal of Virology, 86, 1255–1260.Google Scholar
Muegge, B. D., Kuczynski, J., Knights, D., Clemente, J. C., González, A., Fontana, L., et al. (2011). Diet drives convergence in gut microbiome functions across mammalian phylogeny and within humans. Science, 332(6032), 970–974.Google Scholar
Murray, S. & Linial, M. (2006). Foamy virus infection in primates. Journal of Medical Primatology, 35, 225–235.CrossRefGoogle ScholarPubMed
Murthy, S., Couacy-Hymann, E., Metzger, S., Nowak, K., De Nys, H., Boesch, C., et al. (2013). Absence of frequent herpesvirus transmission in a non-human primate predator–prey system in the wild. Journal of Virology, 87(19).CrossRefGoogle Scholar
Ng, M., Ndungo, E., Kaczmarek, M. E., Herbert, A. S., Binger, T., Kuehne, A. I., et al. (2015). Filovirus receptor NPC1 contributes to species-specific patterns of ebolavirus susceptibility in bats. eLife, 4, e11785.Google Scholar
Nguyen, S., Baker, K., Padman, B. S., Patwa, R., Dunstan, R. A., Weston, T. A., et al (2017). Bacteriophage transcytosis provides a mechanism to cross epithelial cell layers. mBio, 8(6), e01874–01817.Google Scholar
Oksanen, J. F., Blanchet, F. G., Friendly, M., Kindt, R., Legendre, P., McGlinn, D., et al. (2016). Vegan: Community Ecology Package. R package version 2.4–0.Google Scholar
Palacios, G., Lowenstine, L. J., Cranfield, M. R., Gilardi, K. V., Spelman, L., Lukasik-Braum, M., et al. (2011). Human metapneumovirus infection in wild mountain gorillas, Rwanda. Emerging Infectious Diseases, 17, 711.Google Scholar
Patrono, L. V., Samuni, L., Corman, V. M., Nourifar, L., Röthemeier, C., Wittig, R. M., et al. (2018). Human coronavirus OC43 outbreak in wild chimpanzees, Côte d´ Ivoire, 2016. Emerging Microbes & Infections, 7, 118.Google Scholar
Prince, A. M., Brotman, B., Lee, D. H., Andrus, L., Valinsky, J. & Marx, P. (2002). Lack of evidence for HIV type 1-related SIVcpz infection in captive and wild chimpanzees (Pan troglodytes verus) in West Africa. AIDS Research and Human Retroviruses, 18, 657–660.Google Scholar
Refisch, J. & Koné, I. (2005). Impact of commercial hunting on monkey populations in the Taï region, Côte d’Ivoire. Biotropica, 37, 136–144.Google Scholar
Ren, T., Grieneisen, L. E., Alberts, S. C., Archie, E. A. & Wu, M. (2015). Development, diet and dynamism: Longitudinal and cross‐sectional predictors of gut microbial communities in wild baboons. Environmental Microbiology, 18, 1312–1325.Google Scholar
Roberts, A. P. & Kreth, J. (2014). The impact of horizontal gene transfer on the adaptive ability of the human oral microbiome. Frontiers in Cellular and Infection Microbiology, 4, 124.Google Scholar
Salem, N. B., Leendertz, F. H. & Ehlers, B. (2016). Genome sequences of polyomaviruses from the wild-living red colobus (Piliocolobus badius) and western chimpanzee (Pan troglodytes verus). Genome Announcements, 4(5), e01101–01116.Google Scholar
Samson, M., Libert, F., Doranz, B. J., Rucker, J., Liesnard, C., Farber, C. M., et al. (1996). Resistance to HIV-1 infection in Caucasian individuals bearing mutant alleles of the CCR-5 chemokine receptor gene. Nature, 382(6593), 722–725.Google Scholar
Santiago, M. L., Range, F., Keele, B. F., Li, Y., Bailes, E., Bibollet-Ruche, F., et al. (2005). Simian immunodeficiency virus infection in free-ranging sooty mangabeys (Cercocebus atys atys) from the Tai Forest, Cote d’Ivoire: Implications for the origin of epidemic human immunodeficiency virus type 2. Journal of Virology, 79, 12,515–12,527.Google Scholar
Santiago, M. L., Rodenburg, C. M., Kamenya, S., Bibollet-Ruche, F., Gao, F., Bailes, E., et al. (2002). SIVcpz in wild chimpanzees. Science, 295(5554), 465. https://doi.org/10.1126/science.295.5554.465Google Scholar
Schnorr, S. L., Candela, M., Rampelli, S., Centanni, M., Consolandi, C., Basaglia, G., et al. (2014). Gut microbiome of the Hadza hunter-gatherers. Nature Communications, 5. https://doi.org/10.1038/ncomms4654CrossRefGoogle ScholarPubMed
Scuda, N., Madinda, N. F., Akoua-Koffi, C., Adjogoua, E. V., Wevers, D., Hofmann, J., et al. (2013). Novel polyomaviruses of nonhuman primates: Genetic and serological predictors for the existence of multiple unknown polyomaviruses within the human population. PLoS Pathogens, 9(6), e1003429. https://doi.org/10.1371/journal.ppat.1003429Google Scholar
Sender, R., Fuchs, S. & Milo, R. (2016). Revised estimates for the number of human and bacteria cells in the body. PLoS Biology, 14(8), e1002533. https://doi.org/10.1371/journal.pbio.1002533Google Scholar
Switzer, W. M., Bhullar, V., Shanmugam, V., Cong, M. E., Parekh, B., Lerche, N. W., et al. (2004). Frequent simian foamy virus infection in persons occupationally exposed to nonhuman primates. Journal of Virology, 78, 2780–2789.Google Scholar
Switzer, W. M., Garcia, A. D., Yang, C., Wright, A., Kalish, M. L., Folks, T. M., et al. (2008). Coinfection with HIV-1 and simian foamy virus in West Central Africans. Journal of Infectious Diseases, 197, 1389–1393.Google Scholar
Switzer, W. M., Salemi, M., Shanmugam, V., Gao, F., Cong, M. E., Kuiken, C., et al. (2005). Ancient co-speciation of simian foamy viruses and primates. Nature, 434(7031), 376–380.Google Scholar
Thomas, F., Barbeyron, T., Tonon, T., Génicot, S., Czjzek, M. & Michel, G. (2012). Characterization of the first alginolytic operons in a marine bacterium: From their emergence in marine Flavobacteriia to their independent transfers to marine Proteobacteria and human gut Bacteroides. Environmental Microbiology, 14, 2379–2394.Google Scholar
Traina-Dorge, V. L., Lorino, R., Gormus, B. J., Metzger, M., Telfer, P., Richardson, D., et al. (2005). Molecular epidemiology of simian T-cell lymphotropic virus type 1 in wild and captive sooty mangabeys. Journal of Virology, 79, 2541–2548.Google Scholar
Tremaroli, V. & Bäckhed, F. (2012). Functional interactions between the gut microbiota and host metabolism. Nature, 489(7415), 242–249.Google Scholar
Tung, J., Barreiro, L. B., Burns, M. B., Grenier, J.-C., Lynch, J., Grieneisen, L. E., et al. (2015). Social networks predict gut microbiome composition in wild baboons. eLife, 4, e05224.CrossRefGoogle ScholarPubMed
van Schaik, C. P. & Kappeler, P. M. (1997). Infanticide risk and the evolution of male–female association in primates. Proceedings of the Royal Society of London B, 264(1388), 1687–1694.Google Scholar
Ventura, M., Sozzi, T., Turroni, F., Matteuzzi, D. & Sinderen, D. (2011). The impact of bacteriophages on probiotic bacteria and gut microbiota diversity. Genes & Nutrition, 6, 205.CrossRefGoogle ScholarPubMed
Ventura, M., Turroni, F., Motherway, M. O. C., MacSharry, J. & van Sinderen, D. (2012). Host–microbe interactions that facilitate gut colonization by commensal bifidobacteria. Trends in Microbiology, 20, 467–476.Google Scholar
Wevers, D., Metzger, S., Babweteera, F., Bieberbach, M., Boesch, C., Cameron, K., et al. (2011). Novel adenoviruses in wild primates: High genetic diversity and evidence of zoonotic transmissions. Journal of Virology, 85, 10,774–10,784. https://doi.org/00810–00811.Google Scholar
WHO Ebola Response Team (2014). Ebola virus disease in West Africa – The first 9 months of the epidemic and forward projections. New England Journal of Medicine, 371, 1481–1495.Google Scholar
Wolfe, N. D., Escalante, A. A., Karesh, W. B., Kilbourn, A., Spielman, A. & Lal, A. A. (1998). Wild primate populations in emerging infectious disease research: The missing link? Emerging Infectious Disease, 4, 149–158.Google Scholar
Wolfe, N. D., Switzer, W. M., Carr, J. K., Bhullar, V. B., Shanmugam, V., Tamoufe, U., et al. (2004). Naturally acquired simian retrovirus infections in central African hunters. The Lancet, 363(9413), 932–937.Google Scholar
Wu, D. F., Löhrich, T., Sachse, A., Mundry, R., Wittig, R. M., Calvignac-Spencer, S., et al. (2018). Seasonal and inter-annual variation of malaria parasite detection in wild chimpanzees. Malaria Journal, 17, 38.Google Scholar
Zilber-Rosenberg, I. & Rosenberg, E. (2008). Role of microorganisms in the evolution of animals and plants: The hologenome theory of evolution. FEMS Microbiology Reviews, 32, 723–735.CrossRefGoogle ScholarPubMed