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Mechanisms governing avian phylosymbiosis: Genetic dissimilarity based on neutral and MHC regions exhibits little relationship with gut microbiome distributions of Galápagos mockingbirds

The gut microbiome of animals, which serves important functions but can also contain potential pathogens, is to varying degrees under host genetic control. This can generate signals of phylosymbiosis, whereby gut microbiome composition matches host phylogenetic structure. However, the genetic mechan...

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Autores principales: Fleischer, Ramona, Risely, Alice, Hoeck, Paquita E. A., Keller, Lukas F., Sommer, Simone
Formato: Online Artículo Texto
Lenguaje:English
Publicado: John Wiley and Sons Inc. 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7713960/
https://www.ncbi.nlm.nih.gov/pubmed/33304542
http://dx.doi.org/10.1002/ece3.6934
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author Fleischer, Ramona
Risely, Alice
Hoeck, Paquita E. A.
Keller, Lukas F.
Sommer, Simone
author_facet Fleischer, Ramona
Risely, Alice
Hoeck, Paquita E. A.
Keller, Lukas F.
Sommer, Simone
author_sort Fleischer, Ramona
collection PubMed
description The gut microbiome of animals, which serves important functions but can also contain potential pathogens, is to varying degrees under host genetic control. This can generate signals of phylosymbiosis, whereby gut microbiome composition matches host phylogenetic structure. However, the genetic mechanisms that generate phylosymbiosis and the scale at which they act remain unclear. Two non‐mutually exclusive hypotheses are that phylosymbiosis is driven by immunogenetic regions such as the major histocompatibility complex (MHC) controlling microbial composition, or by spatial structuring of neutral host genetic diversity via founder effects, genetic drift, or isolation by distance. Alternatively, associations between microbes and host phylogeny may be generated by their spatial autocorrelation across landscapes, rather than the direct effects of host genetics. In this study, we collected MHC, microsatellite, and gut microbiome data from separate individuals belonging to the Galápagos mockingbird species complex, which consists of four allopatrically distributed species. We applied multiple regression with distance matrices and Bayesian inference to test for correlations between average genetic and microbiome similarity across nine islands for which all three levels of data were available. Clustering of individuals by species was strongest when measured with microsatellite markers and weakest for gut microbiome distributions, with intermediate clustering of MHC allele frequencies. We found that while correlations between island‐averaged gut microbiome composition and both microsatellite and MHC dissimilarity existed across species, these relationships were greatly weakened when accounting for geographic distance. Overall, our study finds little support for large‐scale control of gut microbiome composition by neutral or adaptive genetic regions across closely related bird phylogenies, although this does not preclude the possibility that host genetics shapes gut microbiome at the individual level.
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spelling pubmed-77139602020-12-09 Mechanisms governing avian phylosymbiosis: Genetic dissimilarity based on neutral and MHC regions exhibits little relationship with gut microbiome distributions of Galápagos mockingbirds Fleischer, Ramona Risely, Alice Hoeck, Paquita E. A. Keller, Lukas F. Sommer, Simone Ecol Evol Original Research The gut microbiome of animals, which serves important functions but can also contain potential pathogens, is to varying degrees under host genetic control. This can generate signals of phylosymbiosis, whereby gut microbiome composition matches host phylogenetic structure. However, the genetic mechanisms that generate phylosymbiosis and the scale at which they act remain unclear. Two non‐mutually exclusive hypotheses are that phylosymbiosis is driven by immunogenetic regions such as the major histocompatibility complex (MHC) controlling microbial composition, or by spatial structuring of neutral host genetic diversity via founder effects, genetic drift, or isolation by distance. Alternatively, associations between microbes and host phylogeny may be generated by their spatial autocorrelation across landscapes, rather than the direct effects of host genetics. In this study, we collected MHC, microsatellite, and gut microbiome data from separate individuals belonging to the Galápagos mockingbird species complex, which consists of four allopatrically distributed species. We applied multiple regression with distance matrices and Bayesian inference to test for correlations between average genetic and microbiome similarity across nine islands for which all three levels of data were available. Clustering of individuals by species was strongest when measured with microsatellite markers and weakest for gut microbiome distributions, with intermediate clustering of MHC allele frequencies. We found that while correlations between island‐averaged gut microbiome composition and both microsatellite and MHC dissimilarity existed across species, these relationships were greatly weakened when accounting for geographic distance. Overall, our study finds little support for large‐scale control of gut microbiome composition by neutral or adaptive genetic regions across closely related bird phylogenies, although this does not preclude the possibility that host genetics shapes gut microbiome at the individual level. John Wiley and Sons Inc. 2020-10-27 /pmc/articles/PMC7713960/ /pubmed/33304542 http://dx.doi.org/10.1002/ece3.6934 Text en © 2020 The Authors. Ecology and Evolution published by John Wiley & Sons Ltd This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.
spellingShingle Original Research
Fleischer, Ramona
Risely, Alice
Hoeck, Paquita E. A.
Keller, Lukas F.
Sommer, Simone
Mechanisms governing avian phylosymbiosis: Genetic dissimilarity based on neutral and MHC regions exhibits little relationship with gut microbiome distributions of Galápagos mockingbirds
title Mechanisms governing avian phylosymbiosis: Genetic dissimilarity based on neutral and MHC regions exhibits little relationship with gut microbiome distributions of Galápagos mockingbirds
title_full Mechanisms governing avian phylosymbiosis: Genetic dissimilarity based on neutral and MHC regions exhibits little relationship with gut microbiome distributions of Galápagos mockingbirds
title_fullStr Mechanisms governing avian phylosymbiosis: Genetic dissimilarity based on neutral and MHC regions exhibits little relationship with gut microbiome distributions of Galápagos mockingbirds
title_full_unstemmed Mechanisms governing avian phylosymbiosis: Genetic dissimilarity based on neutral and MHC regions exhibits little relationship with gut microbiome distributions of Galápagos mockingbirds
title_short Mechanisms governing avian phylosymbiosis: Genetic dissimilarity based on neutral and MHC regions exhibits little relationship with gut microbiome distributions of Galápagos mockingbirds
title_sort mechanisms governing avian phylosymbiosis: genetic dissimilarity based on neutral and mhc regions exhibits little relationship with gut microbiome distributions of galápagos mockingbirds
topic Original Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7713960/
https://www.ncbi.nlm.nih.gov/pubmed/33304542
http://dx.doi.org/10.1002/ece3.6934
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