Comparative Analyses of Vertebrate Gut Microbiomes Reveal Convergence between Birds and Bats
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...
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| Format: | Article |
| Language: | English |
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American Society for Microbiology
2020-02-01
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| Series: | mBio |
| Subjects: | |
| Online Access: | https://journals.asm.org/doi/10.1128/mBio.02901-19 |
| _version_ | 1819004183408279552 |
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| author | Se Jin Song Jon G. Sanders Frédéric Delsuc Jessica Metcalf Katherine Amato Michael W. Taylor Florent Mazel Holly L. Lutz Kevin Winker Gary R. Graves Gregory Humphrey Jack A. Gilbert Shannon J. Hackett Kevin P. White Heather R. Skeen Sarah M. Kurtis Jack Withrow Thomas Braile Matthew Miller Kevin G. McCracken James M. Maley Vanessa O. Ezenwa Allison Williams Jessica M. Blanton Valerie J. McKenzie Rob Knight |
| author_facet | Se Jin Song Jon G. Sanders Frédéric Delsuc Jessica Metcalf Katherine Amato Michael W. Taylor Florent Mazel Holly L. Lutz Kevin Winker Gary R. Graves Gregory Humphrey Jack A. Gilbert Shannon J. Hackett Kevin P. White Heather R. Skeen Sarah M. Kurtis Jack Withrow Thomas Braile Matthew Miller Kevin G. McCracken James M. Maley Vanessa O. Ezenwa Allison Williams Jessica M. Blanton Valerie J. McKenzie Rob Knight |
| author_sort | Se Jin Song |
| collection | DOAJ |
| description | 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. Furthermore, 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 convergently 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. IMPORTANCE In this comprehensive survey of microbiomes of >900 species, including 315 mammals and 491 birds, we find a striking convergence of the microbiomes of birds and animals that fly. In nonflying mammals, diet and short-term evolutionary relatedness drive the microbiome, and many microbial species are specific to a particular kind of mammal, but flying mammals and birds break this pattern with many microbes shared across different species, with little correlation either with diet or with relatedness of the hosts. This finding suggests that adaptation to flight breaks long-held relationships between hosts and their microbes. |
| first_indexed | 2024-12-20T23:32:51Z |
| format | Article |
| id | doaj.art-4c88416112104851bafba75448d168c3 |
| institution | Directory Open Access Journal |
| issn | 2150-7511 |
| language | English |
| last_indexed | 2024-12-20T23:32:51Z |
| publishDate | 2020-02-01 |
| publisher | American Society for Microbiology |
| record_format | Article |
| series | mBio |
| spelling | doaj.art-4c88416112104851bafba75448d168c32022-12-21T19:23:15ZengAmerican Society for MicrobiologymBio2150-75112020-02-0111110.1128/mBio.02901-19Comparative Analyses of Vertebrate Gut Microbiomes Reveal Convergence between Birds and BatsSe Jin Song0Jon G. Sanders1Frédéric Delsuc2Jessica Metcalf3Katherine Amato4Michael W. Taylor5Florent Mazel6Holly L. Lutz7Kevin Winker8Gary R. Graves9Gregory Humphrey10Jack A. Gilbert11Shannon J. Hackett12Kevin P. White13Heather R. Skeen14Sarah M. Kurtis15Jack Withrow16Thomas Braile17Matthew Miller18Kevin G. McCracken19James M. Maley20Vanessa O. Ezenwa21Allison Williams22Jessica M. Blanton23Valerie J. McKenzie24Rob Knight25Department of Pediatrics, School of Medicine, University of California San Diego, La Jolla, California, USADepartment of Pediatrics, School of Medicine, University of California San Diego, La Jolla, California, USAInstitut des Sciences de l’Evolution de Montpellier (ISEM), CNRS, EPHE, IRD, Université de Montpellier, Montpellier, FranceDepartment of Animal Sciences, Colorado State University, Fort Collins, Colorado, USADepartment of Anthropology, Northwestern University, Evanston, Illinois, USASchool of Biological Sciences, University of Auckland, Auckland, New ZealandDepartment of Botany, Biodiversity Research Centre, University of British Columbia, Vancouver, British Columbia, CanadaDepartment of Pediatrics, School of Medicine, University of California San Diego, La Jolla, California, USAUniversity of Alaska Museum, Fairbanks, Alaska, USADepartment of Vertebrate Zoology, National Museum of Natural History, Smithsonian Institution, Washington, DC, USADepartment of Pediatrics, School of Medicine, University of California San Diego, La Jolla, California, USADepartment of Pediatrics, School of Medicine, University of California San Diego, La Jolla, California, USAIntegrative Research Center, Field Museum of Natural History, Chicago, Illinois, USAInstitute for Genomics and Systems Biology, University of Chicago, Chicago, Illinois, USAIntegrative Research Center, Field Museum of Natural History, Chicago, Illinois, USADepartment of Biology, University of Florida, Gainesville, Florida, USAUniversity of Alaska Museum, Fairbanks, Alaska, USAUniversity of Alaska Museum, Fairbanks, Alaska, USAUniversity of Alaska Museum, Fairbanks, Alaska, USAUniversity of Alaska Museum, Fairbanks, Alaska, USAMoore Laboratory of Zoology, Occidental College, Los Angeles, California, USAOdum School of Ecology, University of Georgia, Athens, Georgia, USAOdum School of Ecology, University of Georgia, Athens, Georgia, USAMarine Biology Research Division, Scripps Institution of Oceanography, University of California San Diego, La Jolla, California, USADepartment of Ecology and Evolutionary Biology, University of Colorado Boulder, Boulder, Colorado, USADepartment of Pediatrics, School of Medicine, University of California San Diego, La Jolla, California, USAABSTRACT 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. Furthermore, 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 convergently 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. IMPORTANCE In this comprehensive survey of microbiomes of >900 species, including 315 mammals and 491 birds, we find a striking convergence of the microbiomes of birds and animals that fly. In nonflying mammals, diet and short-term evolutionary relatedness drive the microbiome, and many microbial species are specific to a particular kind of mammal, but flying mammals and birds break this pattern with many microbes shared across different species, with little correlation either with diet or with relatedness of the hosts. This finding suggests that adaptation to flight breaks long-held relationships between hosts and their microbes.https://journals.asm.org/doi/10.1128/mBio.02901-19dietevolutionflightmicrobiomevertebrate |
| spellingShingle | Se Jin Song Jon G. Sanders Frédéric Delsuc Jessica Metcalf Katherine Amato Michael W. Taylor Florent Mazel Holly L. Lutz Kevin Winker Gary R. Graves Gregory Humphrey Jack A. Gilbert Shannon J. Hackett Kevin P. White Heather R. Skeen Sarah M. Kurtis Jack Withrow Thomas Braile Matthew Miller Kevin G. McCracken James M. Maley Vanessa O. Ezenwa Allison Williams Jessica M. Blanton Valerie J. McKenzie Rob Knight Comparative Analyses of Vertebrate Gut Microbiomes Reveal Convergence between Birds and Bats mBio diet evolution flight microbiome vertebrate |
| title | Comparative Analyses of Vertebrate Gut Microbiomes Reveal Convergence between Birds and Bats |
| title_full | Comparative Analyses of Vertebrate Gut Microbiomes Reveal Convergence between Birds and Bats |
| title_fullStr | Comparative Analyses of Vertebrate Gut Microbiomes Reveal Convergence between Birds and Bats |
| title_full_unstemmed | Comparative Analyses of Vertebrate Gut Microbiomes Reveal Convergence between Birds and Bats |
| title_short | Comparative Analyses of Vertebrate Gut Microbiomes Reveal Convergence between Birds and Bats |
| title_sort | comparative analyses of vertebrate gut microbiomes reveal convergence between birds and bats |
| topic | diet evolution flight microbiome vertebrate |
| url | https://journals.asm.org/doi/10.1128/mBio.02901-19 |
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