Covariation of diet and gut microbiome in African megafauna
Edited by John Terborgh, University of Florida, Cedar Key, FL, and approved October 10, 2019 (received for review April 2, 2019)
Significance
Diet and gut microbiome composition are important for health and nutrition in mammals, but how they covary in response to environmental change remains poorly understood—both because diet composition is rarely quantified precisely, and because studies of diet−microbiome linkages in captive animals may not accurately reflect the dynamics of natural communities. By analyzing diet−microbiome linkages in an assemblage of large mammalian herbivores in Kenya, we found that seasonal changes in diet and microbiome composition were strongly correlated within some populations, whereas other populations exhibited little temporal turnover in either diet or microbiome. Identifying mechanisms that generate species-specific variation in the sensitivity of the diet−microbiome nexus to environmental changes could help to explain differential population performance and food-web structure within ecological communities.
Abstract
A major challenge in biology is to understand how phylogeny, diet, and environment shape the mammalian gut microbiome. Yet most studies of nonhuman microbiomes have relied on relatively coarse dietary categorizations and have focused either on individual wild populations or on captive animals that are sheltered from environmental pressures, which may obscure the effects of dietary and environmental variation on microbiome composition in diverse natural communities. We analyzed plant and bacterial DNA in fecal samples from an assemblage of 33 sympatric large-herbivore species (27 native, 6 domesticated) in a semiarid East African savanna, which enabled high-resolution assessment of seasonal variation in both diet and microbiome composition. Phylogenetic relatedness strongly predicted microbiome composition (r = 0.91) and was weakly but significantly correlated with diet composition (r = 0.20). Dietary diversity did not significantly predict microbiome diversity across species or within any species except kudu; however, diet composition was significantly correlated with microbiome composition both across and within most species. We found a spectrum of seasonal sensitivity at the diet−microbiome nexus: Seasonal changes in diet composition explained 25% of seasonal variation in microbiome composition across species. Species’ positions on (and deviations from) this spectrum were not obviously driven by phylogeny, body size, digestive strategy, or diet composition; however, domesticated species tended to exhibit greater diet−microbiome turnover than wildlife. Our results reveal marked differences in the influence of environment on the degree of diet−microbiome covariation in free-ranging African megafauna, and this variation is not well explained by canonical predictors of nutritional ecology.
Data Availability
Data deposition: Illumina data and unrarefied sequence count tables are available at Dryad (https://doi.org/10.5061/dryad.c119gm5); mitochondrial DNA sequences are available at GenBank (accession nos. MN262920–MN262991 and MN262700–MN262919).
Acknowledgments
We thank the Government of Kenya, National Museums of Kenya, Mpala Research Centre, and Ol Jogi Conservancy for permission to conduct this research; Sam Kurukura and Ali Hassan for field assistance; Patricia Chen and Tina Hansen for sample preparation; Lawrence David and 2 anonymous reviewers for comments; and funders including The Institute at Brown for Environment and Society, The Nature Conservancy’s NatureNet Fellowship, The Princeton Environmental Institute, The Fund for New Ideas in the Natural Sciences from the Office of the Dean of Research at Princeton University, The Cameron Schrier Foundation, and NSF Grants DEB-1355122, DEB-1457697, and IOS-1656527 and Graduate Research Fellowship Program.
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Copyright © 2019 the Author(s). Published by PNAS. This open access article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND).
Data Availability
Data deposition: Illumina data and unrarefied sequence count tables are available at Dryad (https://doi.org/10.5061/dryad.c119gm5); mitochondrial DNA sequences are available at GenBank (accession nos. MN262920–MN262991 and MN262700–MN262919).
Submission history
Published online: November 4, 2019
Published in issue: November 19, 2019
Keywords
Acknowledgments
We thank the Government of Kenya, National Museums of Kenya, Mpala Research Centre, and Ol Jogi Conservancy for permission to conduct this research; Sam Kurukura and Ali Hassan for field assistance; Patricia Chen and Tina Hansen for sample preparation; Lawrence David and 2 anonymous reviewers for comments; and funders including The Institute at Brown for Environment and Society, The Nature Conservancy’s NatureNet Fellowship, The Princeton Environmental Institute, The Fund for New Ideas in the Natural Sciences from the Office of the Dean of Research at Princeton University, The Cameron Schrier Foundation, and NSF Grants DEB-1355122, DEB-1457697, and IOS-1656527 and Graduate Research Fellowship Program.
Notes
This article is a PNAS Direct Submission.
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Competing Interests
The authors declare no competing interest.
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Cite this article
Covariation of diet and gut microbiome in African megafauna, Proc. Natl. Acad. Sci. U.S.A.
116 (47) 23588-23593,
https://doi.org/10.1073/pnas.1905666116
(2019).
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