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Structure of chimpanzee gut microbiomes across tropical Africa

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Date
22/06/2021
Author
Bueno De Mesquita, Clifton P.
Nichols, Lauren M.
Gebert, Matthew J.
Vanderburgh, Caihong
Bocksberger, Gaëlle
Lester, Jack D.
Kalan, Ammie K.
Dieguez, Paula
Mccarthy, Maureen S.
Agbor, Anthony
Álvarez Varona, Paula
Ayimisin, Ayuk Emmanuel
Bessone, Mattia
Chancellor, Rebecca
Cohen, Heather
Coupland, Charlotte
Deschner, Tobias
Egbe, Villard Ebot
Goedmakers, Annemarie
Granjon, Anne-Céline
Grueter, Cyril C.
Head, Josephine
Hernandez-Aguilar, R. Adriana
Jeffery, Kathryn J.
Jones, Sorrel
Kadam, Parag
Kaiser, Michael
Lapuente, Juan
Larson, Bradley
Marrocoli, Sergio
Morgan, David
Mugerwa, Badru
Mulindahabi, Felix
Neil, Emily
Niyigaba, Protais
Pacheco, Liliana
Piel, Alex K.
Robbins, Martha M.
Rundus, Aaron
Sanz, Crickette M.
Sciaky, Lilah
Sheil, Douglas
Sommer, Volker
Stewart, Fiona A.
Ton, Els
Van Schijndel, Joost
Vergnes, Virginie
Wessling, Erin G.
Wittig, Roman M.
Ginath Yuh, Yisa
Yurkiw, Kyle
Zuberbühler, Klaus
Gogarten, Jan F.
Heintz-Buschart, Anna
Muellner-Riehl, Alexandra N.
Boesch, Christophe
Kühl, Hjalmar S.
Fierer, Noah
Arandjelovic, Mimi
Dunn, Robert R.
Keywords
prokaryotes
parasites
diet
tools
host genetics
climate
WILD CHIMPANZEES
PAN-TROGLODYTES
SPECIES RICHNESS
TOOL
DIVERSITY
PATTERNS
IMPACT
DATABASE
BACTERIA
FOREST
QL Zoology
DAS
Metadata
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Abstract
Understanding variation in host-associated microbial communities is important given the relevance of microbiomes to host physiology and health. Using 560 fecal samples collected from wild chimpanzees (Pan troglodytes) across their range, we assessed how geography, genetics, climate, vegetation, and diet relate to gut microbial community structure (prokaryotes, eukaryotic parasites) at multiple spatial scales. We observed a high degree of regional specificity in the microbiome composition, which was associated with host genetics, available plant foods, and potentially with cultural differences in tool use, which affect diet. Genetic differences drove community composition at large scales, while vegetation and potentially tool use drove within-region differences, likely due to their influence on diet. Unlike industrialized human populations in the United States, where regional differences in the gut microbiome are undetectable, chimpanzee gut microbiomes are far more variable across space, suggesting that technological developments have decoupled humans from their local environments, obscuring regional differences that could have been important during human evolution. IMPORTANCE Gut microbial communities are drivers of primate physiology and health, but the factors that influence the gut microbiome in wild primate populations remain largely undetermined. We report data from a continent-wide survey of wild chimpanzee gut microbiota and highlight the effects of genetics, vegetation, and potentially even tool use at different spatial scales on the chimpanzee gut microbiome, including bacteria, archaea, and eukaryotic parasites. Microbial community dissimilarity was strongly correlated with chimpanzee population genetic dissimilarity, and vegetation composition and consumption of algae, honey, nuts, and termites were potentially associated with additional divergence in microbial communities between sampling sites. Our results suggest that host genetics, geography, and climate play a far stronger role in structuring the gut microbiome in chimpanzees than in humans.
Citation
Bueno De Mesquita , C P , Nichols , L M , Gebert , M J , Vanderburgh , C , Bocksberger , G , Lester , J D , Kalan , A K , Dieguez , P , Mccarthy , M S , Agbor , A , Álvarez Varona , P , Ayimisin , A E , Bessone , M , Chancellor , R , Cohen , H , Coupland , C , Deschner , T , Egbe , V E , Goedmakers , A , Granjon , A-C , Grueter , C C , Head , J , Hernandez-Aguilar , R A , Jeffery , K J , Jones , S , Kadam , P , Kaiser , M , Lapuente , J , Larson , B , Marrocoli , S , Morgan , D , Mugerwa , B , Mulindahabi , F , Neil , E , Niyigaba , P , Pacheco , L , Piel , A K , Robbins , M M , Rundus , A , Sanz , C M , Sciaky , L , Sheil , D , Sommer , V , Stewart , F A , Ton , E , Van Schijndel , J , Vergnes , V , Wessling , E G , Wittig , R M , Ginath Yuh , Y , Yurkiw , K , Zuberbühler , K , Gogarten , J F , Heintz-Buschart , A , Muellner-Riehl , A N , Boesch , C , Kühl , H S , Fierer , N , Arandjelovic , M & Dunn , R R 2021 , ' Structure of chimpanzee gut microbiomes across tropical Africa ' , mSystems , vol. 6 , no. 3 , e01269-20 . https://doi.org/10.1128/mSystems.01269-20
Publication
mSystems
Status
Peer reviewed
DOI
https://doi.org/10.1128/mSystems.01269-20
ISSN
2379-5077
Type
Journal article
Rights
Copyright © 2021 Bueno de Mesquita et al. This is an open-access article distributed under the terms of the Creative Commons https://creativecommons.org/licenses/by/4.0/
Description
We acknowledge the Max Planck Society, the Max Planck Society Innovation Fund, and the Heinz L. Krekeler Foundation for funding. J.F.G. was supported by the Deutsche Forschungsgemeinschaft (DFG) Research Group “Sociality and Health in Primates” (FOR2136). Publication of this article was funded by the University of Colorado Boulder Libraries Open Access Fund.
Collections
  • University of St Andrews Research
URI
http://hdl.handle.net/10023/23630

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