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Gut microbiome composition, not alpha diversity, is associated with survival in a natural vertebrate population

BACKGROUND: The vertebrate gut microbiome (GM) can vary substantially across individuals within the same natural population. Although there is evidence linking the GM to health in captive animals, very little is known about the consequences of GM variation for host fitness in the wild. Here, we expl...

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Autores principales: Worsley, Sarah F., Davies, Charli S., Mannarelli, Maria-Elena, Hutchings, Matthew I., Komdeur, Jan, Burke, Terry, Dugdale, Hannah L., Richardson, David S.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8685825/
https://www.ncbi.nlm.nih.gov/pubmed/34930493
http://dx.doi.org/10.1186/s42523-021-00149-6
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author Worsley, Sarah F.
Davies, Charli S.
Mannarelli, Maria-Elena
Hutchings, Matthew I.
Komdeur, Jan
Burke, Terry
Dugdale, Hannah L.
Richardson, David S.
author_facet Worsley, Sarah F.
Davies, Charli S.
Mannarelli, Maria-Elena
Hutchings, Matthew I.
Komdeur, Jan
Burke, Terry
Dugdale, Hannah L.
Richardson, David S.
author_sort Worsley, Sarah F.
collection PubMed
description BACKGROUND: The vertebrate gut microbiome (GM) can vary substantially across individuals within the same natural population. Although there is evidence linking the GM to health in captive animals, very little is known about the consequences of GM variation for host fitness in the wild. Here, we explore the relationship between faecal microbiome diversity, body condition, and survival using data from the long-term study of a discrete natural population of the Seychelles warbler (Acrocephalus sechellensis) on Cousin Island. To our knowledge, this is the first time that GM differences associated with survival have been fully characterised for a natural vertebrate species, across multiple age groups and breeding seasons. RESULTS: We identified substantial variation in GM community structure among sampled individuals, which was partially explained by breeding season (5% of the variance), and host age class (up to 1% of the variance). We also identified significant differences in GM community membership between adult birds that survived, versus those that had died by the following breeding season. Individuals that died carried increased abundances of taxa that are known to be opportunistic pathogens, including several ASVs in the genus Mycobacterium. However, there was no association between GM alpha diversity (the diversity of bacterial taxa within a sample) and survival to the next breeding season, or with individual body condition. Additionally, we found no association between GM community membership and individual body condition. CONCLUSIONS: These results demonstrate that components of the vertebrate GM can be associated with host fitness in the wild. However, further research is needed to establish whether changes in bacterial abundance contribute to, or are only correlated with, differential survival; this will add to our understanding of the importance of the GM in the evolution of host species living in natural populations. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s42523-021-00149-6.
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spelling pubmed-86858252021-12-20 Gut microbiome composition, not alpha diversity, is associated with survival in a natural vertebrate population Worsley, Sarah F. Davies, Charli S. Mannarelli, Maria-Elena Hutchings, Matthew I. Komdeur, Jan Burke, Terry Dugdale, Hannah L. Richardson, David S. Anim Microbiome Research Article BACKGROUND: The vertebrate gut microbiome (GM) can vary substantially across individuals within the same natural population. Although there is evidence linking the GM to health in captive animals, very little is known about the consequences of GM variation for host fitness in the wild. Here, we explore the relationship between faecal microbiome diversity, body condition, and survival using data from the long-term study of a discrete natural population of the Seychelles warbler (Acrocephalus sechellensis) on Cousin Island. To our knowledge, this is the first time that GM differences associated with survival have been fully characterised for a natural vertebrate species, across multiple age groups and breeding seasons. RESULTS: We identified substantial variation in GM community structure among sampled individuals, which was partially explained by breeding season (5% of the variance), and host age class (up to 1% of the variance). We also identified significant differences in GM community membership between adult birds that survived, versus those that had died by the following breeding season. Individuals that died carried increased abundances of taxa that are known to be opportunistic pathogens, including several ASVs in the genus Mycobacterium. However, there was no association between GM alpha diversity (the diversity of bacterial taxa within a sample) and survival to the next breeding season, or with individual body condition. Additionally, we found no association between GM community membership and individual body condition. CONCLUSIONS: These results demonstrate that components of the vertebrate GM can be associated with host fitness in the wild. However, further research is needed to establish whether changes in bacterial abundance contribute to, or are only correlated with, differential survival; this will add to our understanding of the importance of the GM in the evolution of host species living in natural populations. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s42523-021-00149-6. BioMed Central 2021-12-20 /pmc/articles/PMC8685825/ /pubmed/34930493 http://dx.doi.org/10.1186/s42523-021-00149-6 Text en © The Author(s) 2021 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Research Article
Worsley, Sarah F.
Davies, Charli S.
Mannarelli, Maria-Elena
Hutchings, Matthew I.
Komdeur, Jan
Burke, Terry
Dugdale, Hannah L.
Richardson, David S.
Gut microbiome composition, not alpha diversity, is associated with survival in a natural vertebrate population
title Gut microbiome composition, not alpha diversity, is associated with survival in a natural vertebrate population
title_full Gut microbiome composition, not alpha diversity, is associated with survival in a natural vertebrate population
title_fullStr Gut microbiome composition, not alpha diversity, is associated with survival in a natural vertebrate population
title_full_unstemmed Gut microbiome composition, not alpha diversity, is associated with survival in a natural vertebrate population
title_short Gut microbiome composition, not alpha diversity, is associated with survival in a natural vertebrate population
title_sort gut microbiome composition, not alpha diversity, is associated with survival in a natural vertebrate population
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8685825/
https://www.ncbi.nlm.nih.gov/pubmed/34930493
http://dx.doi.org/10.1186/s42523-021-00149-6
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