Factors influencing bacterial microbiome composition in a wild non-human primate community in Taï National Park, Côte d’Ivoire

Gogarten, Jan F.; Davies, T. Jonathan; Benjamino, Jacquelynn; Gogarten, J. Peter; Graf, Joerg; Mielke, Alexander; Mundry, Roger; Nelson, Michael C.; Wittig, Roman M.; Leendertz, Fabian H.; Calvignac‐Spencer, Sébastien

doi:10.1038/s41396-018-0166-1

Cited by 39 publications

(46 citation statements)

References 82 publications

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“…TNP represents the largest remaining primary forest in West Africa and the wild NHP populations present in this ecosystem represent some of the best‐studied in the world; studies on the chimpanzees and monkeys of TNP were initiated in 1979 and 1989 respectively (Boesch & Achermann, ; McGraw, Zuberbühler, & Noë, ) and a veterinary programme that started in 2001 has targeted a broad array of pathogens associated with these populations (Gogarten et al, ; Hoffmann et al, ; Leendertz et al, ; Rich et al, ). We focused on a group of sooty mangabeys habituated to human observers in November 2012 (the Audrenisrou group), which consisted of ~60 individuals during the study period (Gogarten et al, ; Mielke et al, ). We also captured flies near a habituated chimpanzee community (the North group) with 17 individuals (in August 2013), whose territory overlaps that of the mangabey group, and two neighbouring habituated chimpanzee communities (the South and East groups, containing 41 and 36 individuals respectively in December 2018).…”

Section: Methodsmentioning

confidence: 99%

Tropical rainforest flies carrying pathogens form stable associations with social nonhuman primates

et al. 2019

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Living in groups provides benefits but also incurs costs such as attracting disease vectors. For example, synanthropic flies associate with human settlements, and higher fly densities increase pathogen transmission. We investigated whether such associations also exist in highly mobile nonhuman primate (NHP) Groups. We studied flies in a group of wild sooty mangabeys (Cercocebus atys atys) and three communities of wild chimpanzees (Pan troglodytes verus) in Taï National Park, Côte d'Ivoire. We observed markedly higher fly densities within both mangabey and chimpanzee groups. Using a mark–recapture experiment, we showed that flies stayed with the sooty mangabey group for up to 12 days and for up to 1.3 km. We also tested mangabey‐associated flies for pathogens infecting mangabeys in this ecosystem, Bacillus cereus biovar anthracis (Bcbva), causing sylvatic anthrax, and Treponema pallidum pertenue, causing yaws. Flies contained treponemal (6/103) and Bcbva (7/103) DNA. We cultured Bcbva from all PCR‐positive flies, confirming bacterial viability and suggesting that this bacterium might be transmitted and disseminated by flies. Whole genome sequences of Bcbva isolates revealed a diversity of Bcbva, probably derived from several sources. We conclude that flies actively track mangabeys and carry infectious bacterial pathogens; these associations represent an understudied cost of sociality and potentially expose many social animals to a diversity of pathogens.

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Section: Methodsmentioning

confidence: 99%

Tropical rainforest flies carrying pathogens form stable associations with social nonhuman primates

et al. 2019

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“…Comparative studies of gut microbiome structure across phylogenetically similar but ecologically distinct host species help clarify factors that regulate microbial community assembly, structure, and stability over time. In mammals, these patterns are shaped by a variety of factors including host gut physiology, diet, phylogeny [1][2][3][4][5][6], host age, geography [7,8], and social behavior [9,10]. Our current understanding of microbial community dynamics is shaped by a disproportionate focus on bacteria.…”

Section: Introductionmentioning

confidence: 99%

Biodiversity of protists and nematodes in the wild nonhuman primate gut

et al. 2019

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Documenting the natural diversity of eukaryotic organisms in the nonhuman primate (NHP) gut is important for understanding the evolution of the mammalian gut microbiome, its role in digestion, health and disease, and the consequences of anthropogenic change on primate biology and conservation. Despite the ecological significance of gutassociated eukaryotes, little is known about the factors that influence their assembly and diversity in mammals. In this study, we used an 18S rRNA gene fragment metabarcoding approach to assess the eukaryotic assemblage of 62 individuals representing 16 NHP species. We find that cercopithecoids, and especially the cercopithecines, have substantially higher alpha diversity than other NHP groups. Gut-associated protists and nematodes are widespread among NHPs, consistent with their ancient association with NHP hosts. However, we do not find a consistent signal of phylosymbiosis or host-species specificity. Rather, gut eukaryotes are only weakly structured by primate phylogeny with minimal signal from diet, in contrast to previous reports of NHP gut bacteria. The results of this study indicate that gut-associated eukaryotes offer different information than gut-associated bacteria and add to our understanding of the structure of the gut microbiome.

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“…Such long-term host-bacterial associations imply restricted transmission of bacterial lineages within-rather than between-host lineages (8). This pattern of transmission may be facilitated by the tendency for primates to live in stable social groups (11), creating opportunities for bacterial transmission to conspecifics (12,13). When removed from their natural social and ecological environments in captivity, primates quickly develop humanized bacterial microbiomes (14,15); this apparent plasticity makes the long-term associations of primates with particular bacterial lineages all the more striking (8,9).…”

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Primate phageomes are structured by superhost phylogeny and environment

Gogarten

Rühlemann

Archie

et al. 2020

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The evolutionary origins of human-associated bacteriophage communities are poorly understood.To address this question, we examined fecal phageomes of 23 wild non-human primate taxa, including multiple representatives of all the major primate radiations, and find relatives of the majority of human-associated phages. Primate taxa have distinct phageome compositions that exhibit a clear phylosymbiotic signal, and phage-superhost co-divergence is detected for 44 individual phages. Within species, neighboring social groups harbor evolutionarily and compositionally distinct phageomes, structured by superhost social behavior. However, captive non-human primate phageomes are more similar to humans than their wild counterparts, revealing replacement of wild-associated phages with human-associated ones. Together, our results suggest that potentially labile primate-phage associations persisted across millions of years of evolution, potentially facilitated by transmission between groupmates. One Sentence Summary:Relatives of human-associated phages in wild primates reveal ancient but dynamic superhostphage associations shaped by social transmission. Main Text:Mammals harbor diverse communities of microorganisms, the majority of which are bacteria in the gastrointestinal tract. Gut bacterial communities in turn host diverse bacteriophage communities that influence their structure, function, colonization patterns, and ultimately superhost health (the superhost is the host for bacteria that in turn host the bacteriophages; 1).

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Factors influencing bacterial microbiome composition in a wild non-human primate community in Taï National Park, Côte d’Ivoire

Cited by 39 publications

References 82 publications

Tropical rainforest flies carrying pathogens form stable associations with social nonhuman primates

Tropical rainforest flies carrying pathogens form stable associations with social nonhuman primates

Biodiversity of protists and nematodes in the wild nonhuman primate gut

Primate phageomes are structured by superhost phylogeny and environment

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