TY - JOUR
T1 - Demography, life-history trade-offs, and the gastrointestinal virome of wild chimpanzees
T2 - The fecal virome of wild chimpanzees
AU - Negrey, Jacob D.
AU - Thompson, Melissa Emery
AU - Langergraber, Kevin E.
AU - Machanda, Zarin P.
AU - Mitani, John C.
AU - Muller, Martin N.
AU - Otali, Emily
AU - Owens, Leah A.
AU - Wrangham, Richard W.
AU - Goldberg, Tony L.
N1 - Funding Information:
Ethics. All procedures for this non-invasive study of wild chimpanzees were approved by the Uganda Wildlife Authority, the Uganda National Council for Science and Technology, and by the Institutional Animal Care and Use Committees (IACUCs) of Harvard University (protocol no. 96-03) and the University of New Mexico (protocol no. 14-101186-MCC). The study was exempt from review by the University of Michigan’s IACUC. Data accessibility. Viral nucleotide sequences are available on GenBank under accession nos. MT076199 to MT076210. Additional data and R code are available on the Dryad Digital Repository: https://datadryad.org/stash/share/3xAja5N0q5jYBTL 16pJzOfVkSQbP4nnCkdVG1fotHQs. Authors’ contributions. M.E.T., K.E.L., Z.P.M., J.C.M., M.N.M., E.O., R.W.W. and T.L.G. conceived the study; J.D.N. and T.L.G. drafted the manuscript; L.A.O. and J.D.N. performed laboratory work; J.D.N. completed bioinformatics and statistical analyses; M.E.T., K.E.L., Z.P.M., J.C.M., M.N.M., E.O. and R.W.W. coordinated sample collection; all authors made significant intellectual contributions, revised the manuscript and approved the final draft. Competing interests. We have no competing interests. Funding. This work was supported by NIH award no. R01AG049395 through the National Institute for Aging and the Office of Research on Women’s Health. Further support was provided by the National Science Foundation (grant no. 1355014) and the University of New Mexico. Acknowledgements. We thank the Uganda Wildlife Authority, Uganda National Council for Science and Technology, and Makerere University Biological Field Station for permission to work in Kibale National Park. We are grateful to the field assistants of the Kibale and Ngogo Chimpanzee Projects for help with sample collection, Sam Angedakin for logistical help in the field, and Chris Dunn for support in the laboratory.
Publisher Copyright:
© 2020 The Author(s).
PY - 2020/11/1
Y1 - 2020/11/1
N2 - In humans, senescence increases susceptibility to viral infection. However, comparative data on viral infection in free-living non-human primates - even in our closest living relatives, chimpanzees and bonobos (Pan troglodytes and P. paniscus) - are relatively scarce, thereby constraining an evolutionary understanding of age-related patterns of viral infection. We investigated a population of wild eastern chimpanzees (P. t. schweinfurthii), using metagenomics to characterize viromes (full viral communities) in the faeces of 42 sexually mature chimpanzees (22 males, 20 females) from the Kanyawara and Ngogo communities of Kibale National Park, Uganda. We identified 12 viruses from at least four viral families possessing genomes of both single-stranded RNA and single-stranded DNA. Faecal viromes of both sexes varied with chimpanzee age, but viral richness increased with age only in males. This effect was largely due to three viruses, salivirus, porprismacovirus and chimpanzee stool-associated RNA virus (chisavirus), which occurred most frequently in samples from older males. This finding is consistent with the hypothesis that selection on males for early-life reproduction compromises investment in somatic maintenance, which has delayed consequences for health later in life, in this case reflected in viral infection and/or shedding. Faecal viromes are therefore useful for studying processes related to the divergent reproductive strategies of males and females, ageing, and sex differences in longevity. This article is part of the theme issue 'Evolution of the primate ageing process'.
AB - In humans, senescence increases susceptibility to viral infection. However, comparative data on viral infection in free-living non-human primates - even in our closest living relatives, chimpanzees and bonobos (Pan troglodytes and P. paniscus) - are relatively scarce, thereby constraining an evolutionary understanding of age-related patterns of viral infection. We investigated a population of wild eastern chimpanzees (P. t. schweinfurthii), using metagenomics to characterize viromes (full viral communities) in the faeces of 42 sexually mature chimpanzees (22 males, 20 females) from the Kanyawara and Ngogo communities of Kibale National Park, Uganda. We identified 12 viruses from at least four viral families possessing genomes of both single-stranded RNA and single-stranded DNA. Faecal viromes of both sexes varied with chimpanzee age, but viral richness increased with age only in males. This effect was largely due to three viruses, salivirus, porprismacovirus and chimpanzee stool-associated RNA virus (chisavirus), which occurred most frequently in samples from older males. This finding is consistent with the hypothesis that selection on males for early-life reproduction compromises investment in somatic maintenance, which has delayed consequences for health later in life, in this case reflected in viral infection and/or shedding. Faecal viromes are therefore useful for studying processes related to the divergent reproductive strategies of males and females, ageing, and sex differences in longevity. This article is part of the theme issue 'Evolution of the primate ageing process'.
KW - ageing
KW - chimpanzee
KW - metagenomics
KW - senescence
KW - virome
KW - virus
UR - http://www.scopus.com/inward/record.url?scp=85091265866&partnerID=8YFLogxK
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U2 - 10.1098/rstb.2019.0613rstb20190613
DO - 10.1098/rstb.2019.0613rstb20190613
M3 - Article
C2 - 32951554
AN - SCOPUS:85091265866
VL - 375
JO - Philosophical Transactions of the Royal Society B: Biological Sciences
JF - Philosophical Transactions of the Royal Society B: Biological Sciences
SN - 0800-4622
IS - 1811
M1 - 20190613
ER -