Abstract
Diet and host phylogeny drive the taxonomic and functional contents of the gut microbiome in mammals, yet it is unknown whether these patterns hold across all vertebrate lineages. Here, we assessed gut microbiomes from <900 vertebrate species, including 315 mammals and 491 birds, assessing contributions of diet, phylogeny, and physiology to structuring gut microbiomes. In most nonflying mammals, strong correlations exist between microbial community similarity, host diet, and host phylogenetic distance up to the host order level. In birds, by contrast, gut microbiomes are only very weakly correlated to diet or host phylogeny. Further-more, while most microbes resident in mammalian guts are present in only a restricted taxonomic range of hosts, most microbes recovered from birds show little evidence of host specificity. Notably, among the mammals, bats host especially bird-like gut microbiomes, with little evidence for correlation to host diet or phylogeny. This suggests that host-gut microbiome phylosymbiosis depends on factors conver-gently absent in birds and bats, potentially associated with physiological adaptations to flight. Our findings expose major variations in the behavior of these important symbioses in endothermic vertebrates and may signal fundamental evolutionary shifts in the cost/benefit framework of the gut microbiome.
Original language | English (US) |
---|---|
Article number | e02901-19 |
Journal | mBio |
Volume | 11 |
Issue number | 1 |
DOIs | |
State | Published - Jan 1 2020 |
Keywords
- Diet
- Evolution
- Flight
- Microbiome
- Vertebrate
ASJC Scopus subject areas
- Virology
- Microbiology
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In: mBio, Vol. 11, No. 1, e02901-19, 01.01.2020.
Research output: Contribution to journal › Article › peer-review
TY - JOUR
T1 - Comparative analyses of vertebrate gut microbiomes reveal convergence between birds and bats
AU - Song, Se Jin
AU - Sanders, Jon G.
AU - Delsuc, Frédéric
AU - Metcalf, Jessica
AU - Amato, Katherine
AU - Taylor, Michael W.
AU - Mazel, Florent
AU - Lutz, Holly L.
AU - Winker, Kevin
AU - Graves, Gary R.
AU - Humphrey, Gregory
AU - Gilbert, Jack A.
AU - Hackett, Shannon J.
AU - White, Kevin P.
AU - Skeen, Heather R.
AU - Kurtis, Sarah M.
AU - Withrow, Jack
AU - Braile, Thomas
AU - Miller, Matthew
AU - McCracken, Kevin G.
AU - Maley, James M.
AU - Ezenwa, Vanessa O.
AU - Williams, Allison
AU - Blanton, Jessica M.
AU - McKenzie, Valerie J.
AU - Knight, Rob
N1 - Funding Information: We thank the following individuals and institutions for contributing samples and for their help in collecting samples: An Pas and Richard Jakob-Hoff (Auckland Zoo), Joseph Mendelson (Atlanta Zoo), Kenton Kerns and Sara Hallager (National Zoo), Sabrina Wehrli (Zurich Zoo), Paul Thompson (Taronga Zoo), Nicholas Holland (Scripps Institute of Oceanography), Marilyn Marigold (South Florida Museum), Baptiste Mulot, Antoine Leclerc, Alix Ortega, Alice Brunet, Nicolas Goddard, and Océane Graillot (ZooParc de Beauval), David Gomis, Baptiste Chenet, Elodie Trunet, and Cédric Libert (Parc Zoologique de Montpellier), Benjamin Lamglait (Réserve Africaine de Sigean), Mélanie Berthet and Sandrine Apery (Jardin Zoologique de la Citadelle de Besançon), Corine Esser (Zoo Fauverie du Mont Faron), Guillaume Douay (Jardin Zoologique de Lyon), Marie Simon (Zoo de Lille), Pierre Delrieu (Parc Animalier de Gramat), and Emeric Figuet, Marion Ballenghien, Lionel Hautier, and Guila Ganem (Institut des Sciences de l’Evolution de Montpellier). Benoit de Thoisy and Roxane Schaub (Institut Pasteur de la Guyane) provided access to samples from French Guiana. Nico Avenant (National Museum of South Africa, Bloemfontein), Wendy Panaino, and Nora Weyer (University of the Witwatersrand, Johannesburg) helped collect samples from Tswalu Kalahari Reserve (South Africa). Fieldwork sessions were conducted under the auspices of the Tswalu Foundation (http://www.tswalufoundation.org) with permission to collect fecal samples granted by Duncan MacFadyen (E Oppenheimer & Son), Dylan Smith, and Gus van Dyk (Tswalu Kalahari Reserve). Import permits were issued by the Direction Départementale de la Protection des Populations (DDPP) de l’Hérault. We thank Ian Realo, Andrew Engilis, Christina Gebhard, Christopher Milensky, Jacob Saucier, Brian Schmidt, and James Whatton for help collecting microbiome aspirations of specimens from the. United States National Museum. Collecting permits were issued by Maryland Department of Natural Resources, Montana Fish, Wildlife and Parks, Texas Parks and Wildlife, and the United States Fish and Wildlife Service. Collecting activities were conducted under protocols of the Institutional Animal Care and Use Committee of the National Museum of Natural History. Logistical support was provided by John Brennan, Louise and Ernie Davis, Chris Hale, and Tim Ward in Texas, Paul Rhymer and Carolyn Thome in Maryland, and Pat Gunderson in Montana. We thank members of the FMNH Emerging Pathogens Project (EPP) including Josh Engel and Jason Weckstein for assistance collecting avian samples for the Field Museum of Natural History. We thank Zifeng Jiang for sample processing and Neil Gottel for help processing bat, rodent, shrew, and herpetile samples from Uganda and Kenya. Permits were issued by the Malawi Departments of Forestry and National Parks and Wildlife, Uganda Wildlife Authority, Uganda National Council for Science and Technology, Kenya Wildlife Service, and Kenya Forestry Service. Field assistance was provided by Waswa Sadic Babyesiza, Charles Akora, Solomon Sebuliba, Julian Kerbis Peterhans, Paul Webala, and Beryl Makori. Animal silhouettes were from www.phylopic.org, with thanks to Lukasiniho, Cathy, Michelle Site, Chris Huh, Dori, Nevit Dilme, L. Shyamal, Matt Martyniuk, Michael Keesey, Roberto Díaz Sibaja, Rebecca Groom, Tony Hisgett, and Gareth Monger for artwork. Finally, we thank Luke Thompson for providing insightful conversation. This is contribution ISEM 2019-222 of the Institut des Sciences de l’Evolution de Montpellier. Fieldwork was supported by the Alexander Wetmore Fund (Smithsonian Insti-tution) and the Department of Vertebrate Zoology (USNM). The EPP was funded by the Davee Foundation and the Dr. Ralph and Marian Falk Medical Research Trust. Financial support for field assistance was from Bruce Patterson, Onnolee and Orlin Trapp, and the Council on Africa. This project was made possible by the following funding sources: John Templeton Foundation (Convergent Evolution of the Vertebrate Microbiome, grant ID 44000 to S.J.S., J.G.S., V.J.M., and R.K.), W.M. Keck Foundation (DT061413 to R.K.), the European Research Council (ConvergeAnt project, ERC-2015-CoG-683257), the Centre National de la Recherche Scientifique (CNRS), and the Agence Nationale de la Recherche (CEBA, ANR-10-LABX-25-01) (to F.D.), the Banting Postodoctoral Fellowship (to F.M.), the NSF PRFB (1611948 to H.L.L.), U.S. Department of Agriculture, the late John DuPont, the Eurasian Pacific Wildlife Conservation Foundation, and the Friends of Ornithology (to K.P.W.), Davee Foundation and the Dr. Ralph and Marian Falk Medical Research Trust (to S.J.H.), and NSF DEB-1102493 and NSF IOS-1101836 (to V.O.E.). S.J.S., F.D., V.J.M., and R.K. conceived of the project. S.J.S., J.G.S., J.M., F.D., H.L.L., K.W., G.R.G., J.W., T.B., M.M., K.G.M., J.M.M., V.O.E., A.W., and J.M.B. collected samples. F.D., M.W.T., K.W., G.R.G., J.A.G., S.J.H., K.P.W., V.O.E., V.J.M., and R.K. provided funding acquisition, resources, administrative, and supervisory roles that allowed for various samples included in the data set to be collected and processed. G.H., H.R.S., and S.M.K. helped process data. S.J.S, J.G.S., F.D., and F.M. analyzed the data. S.J.S., J.G.S., V.J.M., and R.K. prepared the original manuscript draft. All authors contributed to revising the manuscript. We declare no competing interests. Funding Information: United States National Museum. Collecting permits were issued by Maryland Department of Natural Resources, Montana Fish, Wildlife and Parks, Texas Parks and Wildlife, and the United States Fish and Wildlife Service. Collecting activities were conducted under protocols of the Institutional Animal Care and Use Committee of the National Museum of Natural History. Logistical support was provided by John Brennan, Louise and Ernie Davis, Chris Hale, and Tim Ward in Texas, Paul Rhymer and Carolyn Thome in Maryland, and Pat Gunderson in Montana. We thank members of the FMNH Emerging Pathogens Project (EPP) including Josh Engel and Jason Weckstein for assistance collecting avian samples for the Field Museum of Natural History. We thank Zifeng Jiang for sample processing and Neil Gottel for help processing bat, rodent, shrew, and herpetile samples from Uganda and Kenya. Permits were issued by the Malawi Departments of Forestry and National Parks and Wildlife, Uganda Wildlife Authority, Uganda National Council for Science and Technology, Kenya Wildlife Service, and Kenya Forestry Service. Field assistance was provided by Waswa Sadic Babyesiza, Charles Akora, Solomon Sebuliba, Julian Kerbis Peterhans, Paul Webala, and Beryl Makori. Animal silhouettes were from www.phylopic.org, with thanks to Lukasiniho, Cathy, Michelle Site, Chris Huh, Dori, Nevit Dilme, L. Shyamal, Matt Martyniuk, Michael Keesey, Roberto Díaz Sibaja, Rebecca Groom, Tony Hisgett, and Gareth Monger for artwork. Finally, we thank Luke Thompson for providing insightful conversation. This is contribution ISEM 2019-222 of the Institut des Sciences de l’Evolution de Montpellier. Fieldwork was supported by the Alexander Wetmore Fund (Smithsonian Institution) and the Department of Vertebrate Zoology (USNM). The EPP was funded by the Davee Foundation and the Dr. Ralph and Marian Falk Medical Research Trust. Financial support for field assistance was from Bruce Patterson, Onnolee and Orlin Trapp, and the Council on Africa. This project was made possible by the following funding sources: John Templeton Foundation (Convergent Evolution of the Vertebrate Microbiome, grant ID 44000 to S.J.S., J.G.S., V.J.M., and R.K.), W.M. Keck Foundation (DT061413 to R.K.), the European Research Council (ConvergeAnt project, ERC-2015-CoG-683257), the Centre National de la Recherche Scientifique (CNRS), and the Agence Nationale de la Recherche (CEBA, ANR-10-LABX-25-01) (to F.D.), the Banting Postodoctoral Fellowship (to F.M.), the NSF PRFB (1611948 to H.L.L.), U.S. Department of Agriculture, the late John DuPont, the Eurasian Pacific Wildlife Conservation Foundation, and the Friends of Ornithology (to K.P.W.), Davee Foundation and the Dr. Ralph and Marian Falk Medical Research Trust (to S.J.H.), and NSF DEB-1102493 and NSF IOS-1101836 (to V.O.E.). S.J.S., F.D., V.J.M., and R.K. conceived of the project. S.J.S., J.G.S., J.M., F.D., H.L.L., K.W., G.R.G., J.W., T.B., M.M., K.G.M., J.M.M., V.O.E., A.W., and J.M.B. collected samples. F.D., M.W.T., K.W., G.R.G., J.A.G., S.J.H., K.P.W., V.O.E., V.J.M., and R.K. provided funding acquisition, resources, administrative, and supervisory roles that allowed for various samples included in the data set to be collected and processed. G.H., H.R.S., and S.M.K. helped process data. S.J.S, J.G.S., F.D., and F.M. analyzed the data. S.J.S., J.G.S., V.J.M., and R.K. prepared the original manuscript draft. All authors contributed to revising the manuscript. We declare no competing interests. Publisher Copyright: © 2020 Song et al.
PY - 2020/1/1
Y1 - 2020/1/1
N2 - Diet and host phylogeny drive the taxonomic and functional contents of the gut microbiome in mammals, yet it is unknown whether these patterns hold across all vertebrate lineages. Here, we assessed gut microbiomes from <900 vertebrate species, including 315 mammals and 491 birds, assessing contributions of diet, phylogeny, and physiology to structuring gut microbiomes. In most nonflying mammals, strong correlations exist between microbial community similarity, host diet, and host phylogenetic distance up to the host order level. In birds, by contrast, gut microbiomes are only very weakly correlated to diet or host phylogeny. Further-more, while most microbes resident in mammalian guts are present in only a restricted taxonomic range of hosts, most microbes recovered from birds show little evidence of host specificity. Notably, among the mammals, bats host especially bird-like gut microbiomes, with little evidence for correlation to host diet or phylogeny. This suggests that host-gut microbiome phylosymbiosis depends on factors conver-gently absent in birds and bats, potentially associated with physiological adaptations to flight. Our findings expose major variations in the behavior of these important symbioses in endothermic vertebrates and may signal fundamental evolutionary shifts in the cost/benefit framework of the gut microbiome.
AB - Diet and host phylogeny drive the taxonomic and functional contents of the gut microbiome in mammals, yet it is unknown whether these patterns hold across all vertebrate lineages. Here, we assessed gut microbiomes from <900 vertebrate species, including 315 mammals and 491 birds, assessing contributions of diet, phylogeny, and physiology to structuring gut microbiomes. In most nonflying mammals, strong correlations exist between microbial community similarity, host diet, and host phylogenetic distance up to the host order level. In birds, by contrast, gut microbiomes are only very weakly correlated to diet or host phylogeny. Further-more, while most microbes resident in mammalian guts are present in only a restricted taxonomic range of hosts, most microbes recovered from birds show little evidence of host specificity. Notably, among the mammals, bats host especially bird-like gut microbiomes, with little evidence for correlation to host diet or phylogeny. This suggests that host-gut microbiome phylosymbiosis depends on factors conver-gently absent in birds and bats, potentially associated with physiological adaptations to flight. Our findings expose major variations in the behavior of these important symbioses in endothermic vertebrates and may signal fundamental evolutionary shifts in the cost/benefit framework of the gut microbiome.
KW - Diet
KW - Evolution
KW - Flight
KW - Microbiome
KW - Vertebrate
UR - http://www.scopus.com/inward/record.url?scp=85077699972&partnerID=8YFLogxK
UR - http://www.scopus.com/inward/citedby.url?scp=85077699972&partnerID=8YFLogxK
U2 - 10.1128/mBio.02901-19
DO - 10.1128/mBio.02901-19
M3 - Article
C2 - 31911491
AN - SCOPUS:85077699972
SN - 2161-2129
VL - 11
JO - mBio
JF - mBio
IS - 1
M1 - e02901-19
ER -