Comparative Analyses of Vertebrate Gut Microbiomes Reveal Convergence between Birds and Bats
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 ar...
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| Published in | mBio Vol. 11; no. 1 |
|---|---|
| Main Authors | , , , , , , , , , , , , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
American Society for Microbiology
07.01.2020
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| Subjects | |
| Online Access | Get full text |
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| Abstract | 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.
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. |
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| AbstractList | 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. 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. 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. 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.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. 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. 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. 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. 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. |
| Author | McKenzie, Valerie J. White, Kevin P. Gilbert, Jack A. Taylor, Michael W. Knight, Rob Miller, Matthew McCracken, Kevin G. Williams, Allison Sanders, Jon G. Winker, Kevin Humphrey, Gregory Withrow, Jack Ezenwa, Vanessa O. Blanton, Jessica M. Graves, Gary R. Delsuc, Frédéric Maley, James M. Metcalf, Jessica Amato, Katherine Skeen, Heather R. Mazel, Florent Lutz, Holly L. Braile, Thomas Hackett, Shannon J. Kurtis, Sarah M. Song, Se Jin |
| Author_xml | – sequence: 1 givenname: Se Jin orcidid: 0000-0003-0750-5709 surname: Song fullname: Song, Se Jin organization: Department of Pediatrics, School of Medicine, University of California San Diego, La Jolla, California, USA – sequence: 2 givenname: Jon G. orcidid: 0000-0001-6077-4014 surname: Sanders fullname: Sanders, Jon G. organization: Department of Pediatrics, School of Medicine, University of California San Diego, La Jolla, California, USA – sequence: 3 givenname: Frédéric surname: Delsuc fullname: Delsuc, Frédéric organization: Institut des Sciences de l’Evolution de Montpellier (ISEM), CNRS, EPHE, IRD, Université de Montpellier, Montpellier, France – sequence: 4 givenname: Jessica surname: Metcalf fullname: Metcalf, Jessica organization: Department of Animal Sciences, Colorado State University, Fort Collins, Colorado, USA – sequence: 5 givenname: Katherine surname: Amato fullname: Amato, Katherine organization: Department of Anthropology, Northwestern University, Evanston, Illinois, USA – sequence: 6 givenname: Michael W. surname: Taylor fullname: Taylor, Michael W. organization: School of Biological Sciences, University of Auckland, Auckland, New Zealand – sequence: 7 givenname: Florent orcidid: 0000-0003-0572-9901 surname: Mazel fullname: Mazel, Florent organization: Department of Botany, Biodiversity Research Centre, University of British Columbia, Vancouver, British Columbia, Canada – sequence: 8 givenname: Holly L. orcidid: 0000-0001-6454-809X surname: Lutz fullname: Lutz, Holly L. organization: Department of Pediatrics, School of Medicine, University of California San Diego, La Jolla, California, USA, Integrative Research Center, Field Museum of Natural History, Chicago, Illinois, USA – sequence: 9 givenname: Kevin surname: Winker fullname: Winker, Kevin organization: University of Alaska Museum, Fairbanks, Alaska, USA – sequence: 10 givenname: Gary R. surname: Graves fullname: Graves, Gary R. organization: Department of Vertebrate Zoology, National Museum of Natural History, Smithsonian Institution, Washington, DC, USA, Center for Macroecology, Evolution and Climate National Museum of Denmark, University of Copenhagen, Copenhagen, Denmark – sequence: 11 givenname: Gregory surname: Humphrey fullname: Humphrey, Gregory organization: Department of Pediatrics, School of Medicine, University of California San Diego, La Jolla, California, USA – sequence: 12 givenname: Jack A. surname: Gilbert fullname: Gilbert, Jack A. organization: Department of Pediatrics, School of Medicine, University of California San Diego, La Jolla, California, USA – sequence: 13 givenname: Shannon J. surname: Hackett fullname: Hackett, Shannon J. organization: Integrative Research Center, Field Museum of Natural History, Chicago, Illinois, USA – sequence: 14 givenname: Kevin P. surname: White fullname: White, Kevin P. organization: Institute for Genomics and Systems Biology, University of Chicago, Chicago, Illinois, USA – sequence: 15 givenname: Heather R. surname: Skeen fullname: Skeen, Heather R. organization: Integrative Research Center, Field Museum of Natural History, Chicago, Illinois, USA, Committee on Evolutionary Biology, University of Chicago, Chicago, Illinois, USA – sequence: 16 givenname: Sarah M. surname: Kurtis fullname: Kurtis, Sarah M. organization: Department of Biology, University of Florida, Gainesville, Florida, USA – sequence: 17 givenname: Jack surname: Withrow fullname: Withrow, Jack organization: University of Alaska Museum, Fairbanks, Alaska, USA – sequence: 18 givenname: Thomas surname: Braile fullname: Braile, Thomas organization: University of Alaska Museum, Fairbanks, Alaska, USA – sequence: 19 givenname: Matthew surname: Miller fullname: Miller, Matthew organization: University of Alaska Museum, Fairbanks, Alaska, USA, Sam Noble Oklahoma Museum of Natural History, Department of Biology, University of Oklahoma, Norman, Oklahoma, USA – sequence: 20 givenname: Kevin G. surname: McCracken fullname: McCracken, Kevin G. organization: University of Alaska Museum, Fairbanks, Alaska, USA, Department of Biology, University of Miami, Coral Gables, Florida, USA, Rosenstiel School of Marine and Atmospheric Sciences, University of Miami, Miami, Florida, USA, Human Genetics and Genomics, Hussman Institute for Human Genomics, University of Miami Miller School of Medicine, Miami, Florida, USA, Institute of Arctic Biology, University of Alaska, Fairbanks, Fairbanks, Alaska, USA – sequence: 21 givenname: James M. surname: Maley fullname: Maley, James M. organization: Moore Laboratory of Zoology, Occidental College, Los Angeles, California, USA – sequence: 22 givenname: Vanessa O. surname: Ezenwa fullname: Ezenwa, Vanessa O. organization: Odum School of Ecology, University of Georgia, Athens, Georgia, USA, Department of Infectious Diseases, College of Veterinary Medicine, University of Georgia, Athens, Georgia, USA – sequence: 23 givenname: Allison surname: Williams fullname: Williams, Allison organization: Odum School of Ecology, University of Georgia, Athens, Georgia, USA – sequence: 24 givenname: Jessica M. surname: Blanton fullname: Blanton, Jessica M. organization: Marine Biology Research Division, Scripps Institution of Oceanography, University of California San Diego, La Jolla, California, USA – sequence: 25 givenname: Valerie J. surname: McKenzie fullname: McKenzie, Valerie J. organization: Department of Ecology and Evolutionary Biology, University of Colorado Boulder, Boulder, Colorado, USA – sequence: 26 givenname: Rob surname: Knight fullname: Knight, Rob organization: Department of Pediatrics, School of Medicine, University of California San Diego, La Jolla, California, USA, Department of Computer Science & Engineering, Jacobs School of Engineering, University of California San Diego, La Jolla, California, USA, Center for Microbiome Innovation, University of California San Diego, La Jolla, California, USA |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/31911491$$D View this record in MEDLINE/PubMed |
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| Snippet | 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... 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... 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... |
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| Title | Comparative Analyses of Vertebrate Gut Microbiomes Reveal Convergence between Birds and Bats |
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