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Drivers of gut microbiome variation within and between groups of a wild Malagasy primate

BACKGROUND: Various aspects of sociality can benefit individuals’ health. The host social environment and its relative contributions to the host-microbiome relationship have emerged as key topics in microbial research. Yet, understanding the mechanisms that lead to structural variation in the social...

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Autores principales: Rudolph, Katja, Schneider, Dominik, Fichtel, Claudia, Daniel, Rolf, Heistermann, Michael, Kappeler, Peter M.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8827170/
https://www.ncbi.nlm.nih.gov/pubmed/35139921
http://dx.doi.org/10.1186/s40168-021-01223-6
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author Rudolph, Katja
Schneider, Dominik
Fichtel, Claudia
Daniel, Rolf
Heistermann, Michael
Kappeler, Peter M.
author_facet Rudolph, Katja
Schneider, Dominik
Fichtel, Claudia
Daniel, Rolf
Heistermann, Michael
Kappeler, Peter M.
author_sort Rudolph, Katja
collection PubMed
description BACKGROUND: Various aspects of sociality can benefit individuals’ health. The host social environment and its relative contributions to the host-microbiome relationship have emerged as key topics in microbial research. Yet, understanding the mechanisms that lead to structural variation in the social microbiome, the collective microbial metacommunity of an animal’s social network, remains difficult since multiple processes operate simultaneously within and among animal social networks. Here, we examined the potential drivers of the convergence of the gut microbiome on multiple scales among and within seven neighbouring groups of wild Verreaux’s sifakas (Propithecus verreauxi) — a folivorous primate of Madagascar. RESULTS: Over four field seasons, we collected 519 faecal samples of 41 animals and determined gut communities via 16S and 18S rRNA gene amplicon analyses. First, we examined whether group members share more similar gut microbiota and if diet, home range overlap, or habitat similarity drive between-group variation in gut communities, accounting for seasonality. Next, we examined within-group variation in gut microbiota by examining the potential effects of social contact rates, male rank, and maternal relatedness. To explore the host intrinsic effects on the gut community structure, we investigated age, sex, faecal glucocorticoid metabolites, and female reproductive state. We found that group members share more similar gut microbiota and differ in alpha diversity, while none of the environmental predictors explained the patterns of between-group variation. Maternal relatedness played an important role in within-group microbial homogeneity and may also explain why adult group members shared the least similar gut microbiota. Also, dominant males differed in their bacterial composition from their group mates, which might be driven by rank-related differences in physiology and scent-marking behaviours. Links to sex, female reproductive state, or faecal glucocorticoid metabolites were not detected. CONCLUSIONS: Environmental factors define the general set-up of population-specific gut microbiota, but intrinsic and social factors have a stronger impact on gut microbiome variation in this primate species. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s40168-021-01223-6.
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spelling pubmed-88271702022-02-10 Drivers of gut microbiome variation within and between groups of a wild Malagasy primate Rudolph, Katja Schneider, Dominik Fichtel, Claudia Daniel, Rolf Heistermann, Michael Kappeler, Peter M. Microbiome Research BACKGROUND: Various aspects of sociality can benefit individuals’ health. The host social environment and its relative contributions to the host-microbiome relationship have emerged as key topics in microbial research. Yet, understanding the mechanisms that lead to structural variation in the social microbiome, the collective microbial metacommunity of an animal’s social network, remains difficult since multiple processes operate simultaneously within and among animal social networks. Here, we examined the potential drivers of the convergence of the gut microbiome on multiple scales among and within seven neighbouring groups of wild Verreaux’s sifakas (Propithecus verreauxi) — a folivorous primate of Madagascar. RESULTS: Over four field seasons, we collected 519 faecal samples of 41 animals and determined gut communities via 16S and 18S rRNA gene amplicon analyses. First, we examined whether group members share more similar gut microbiota and if diet, home range overlap, or habitat similarity drive between-group variation in gut communities, accounting for seasonality. Next, we examined within-group variation in gut microbiota by examining the potential effects of social contact rates, male rank, and maternal relatedness. To explore the host intrinsic effects on the gut community structure, we investigated age, sex, faecal glucocorticoid metabolites, and female reproductive state. We found that group members share more similar gut microbiota and differ in alpha diversity, while none of the environmental predictors explained the patterns of between-group variation. Maternal relatedness played an important role in within-group microbial homogeneity and may also explain why adult group members shared the least similar gut microbiota. Also, dominant males differed in their bacterial composition from their group mates, which might be driven by rank-related differences in physiology and scent-marking behaviours. Links to sex, female reproductive state, or faecal glucocorticoid metabolites were not detected. CONCLUSIONS: Environmental factors define the general set-up of population-specific gut microbiota, but intrinsic and social factors have a stronger impact on gut microbiome variation in this primate species. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s40168-021-01223-6. BioMed Central 2022-02-09 /pmc/articles/PMC8827170/ /pubmed/35139921 http://dx.doi.org/10.1186/s40168-021-01223-6 Text en © The Author(s) 2022 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/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research
Rudolph, Katja
Schneider, Dominik
Fichtel, Claudia
Daniel, Rolf
Heistermann, Michael
Kappeler, Peter M.
Drivers of gut microbiome variation within and between groups of a wild Malagasy primate
title Drivers of gut microbiome variation within and between groups of a wild Malagasy primate
title_full Drivers of gut microbiome variation within and between groups of a wild Malagasy primate
title_fullStr Drivers of gut microbiome variation within and between groups of a wild Malagasy primate
title_full_unstemmed Drivers of gut microbiome variation within and between groups of a wild Malagasy primate
title_short Drivers of gut microbiome variation within and between groups of a wild Malagasy primate
title_sort drivers of gut microbiome variation within and between groups of a wild malagasy primate
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8827170/
https://www.ncbi.nlm.nih.gov/pubmed/35139921
http://dx.doi.org/10.1186/s40168-021-01223-6
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