The gut microbiota of three avian species living in sympatry

Abstract Background Evolutionary divergence and genetic variation are often linked to differences in microbial community structure and diversity. While environmental factors and diet heavily influence gut microbial communities, host species contributions are harder to quantify. Closely related speci...

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Main Authors: Hugo Pereira, Nayden Chakarov, Barbara A. Caspers, Marc Gilles, William Jones, Tafitasoa Mijoro, Sama Zefania, Tamás Székely, Oliver Krüger, Joseph I. Hoffman
Format: Article
Language:English
Published: BMC 2024-11-01
Series:BMC Ecology and Evolution
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Online Access:https://doi.org/10.1186/s12862-024-02329-9
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author Hugo Pereira
Nayden Chakarov
Barbara A. Caspers
Marc Gilles
William Jones
Tafitasoa Mijoro
Sama Zefania
Tamás Székely
Oliver Krüger
Joseph I. Hoffman
author_facet Hugo Pereira
Nayden Chakarov
Barbara A. Caspers
Marc Gilles
William Jones
Tafitasoa Mijoro
Sama Zefania
Tamás Székely
Oliver Krüger
Joseph I. Hoffman
author_sort Hugo Pereira
collection DOAJ
description Abstract Background Evolutionary divergence and genetic variation are often linked to differences in microbial community structure and diversity. While environmental factors and diet heavily influence gut microbial communities, host species contributions are harder to quantify. Closely related species living in sympatry provide a unique opportunity to investigate species differences without the confounding effects of habitat and dietary variation. We therefore compared and contrasted the gut microbiota of three sympatric plover species: the widespread Kittlitz’s and white-fronted plovers (Anarhynchus pecuarius and A. marginatus) and the endemic and vulnerable Madagascar plover (A. thoracicus). Results We found no significant differences in the beta diversity (composition) of the gut microbiota of the three species. However, A. thoracicus exhibited higher intraspecific compositional similarity (i.e. lower pairwise distances) than the other two species; this pattern was especially pronounced among juveniles. By contrast, microbial alpha diversity varied significantly among the species, being highest in A. pecuarius, intermediate in A. marginatus and lowest in A. thoracicus. This pattern was again stronger among juveniles. Geographical distance did not significantly affect the composition of the gut microbiota, but genetic relatedness did. Conclusion While patterns of microbial diversity varied across species, the lack of compositional differences suggests that habitat and diet likely exert a strong influence on the gut microbiota of plovers. This may be enhanced by their precocial, ground-dwelling nature, which could facilitate the horizontal transmission of microbes from the environment. We hypothesise that gut microbiota diversity in plovers primarily reflects the ecological pool of microbiota, which is subsequently modified by host-specific factors including genetics. The reduced microbial and genetic diversity of the endemic A. thoracicus may hinder its ability to adapt to environmental changes, highlighting the need for increased conservation efforts for this vulnerable species.
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spelling doaj-art-ac38c933cc494601826d1bca4ebbd5bf2025-08-20T02:32:56ZengBMCBMC Ecology and Evolution2730-71822024-11-0124111510.1186/s12862-024-02329-9The gut microbiota of three avian species living in sympatryHugo Pereira0Nayden Chakarov1Barbara A. Caspers2Marc Gilles3William Jones4Tafitasoa Mijoro5Sama Zefania6Tamás Székely7Oliver Krüger8Joseph I. Hoffman9Department of Animal Behaviour, Bielefeld UniversityDepartment of Animal Behaviour, Bielefeld UniversityDepartment of Behavioural Ecology, Bielefeld UniversityDepartment of Behavioural Ecology, Bielefeld UniversityInstitut Supérieur de Technologie de Menabe, Université of Toliara & MorondavaHUN-REN-Debrecen University Reproductive Strategies Research Group, University of DebrecenHUN-REN-Debrecen University Reproductive Strategies Research Group, University of DebrecenInstitut Supérieur de Technologie de Menabe, Université of Toliara & MorondavaDepartment of Animal Behaviour, Bielefeld UniversityDepartment of Animal Behaviour, Bielefeld UniversityAbstract Background Evolutionary divergence and genetic variation are often linked to differences in microbial community structure and diversity. While environmental factors and diet heavily influence gut microbial communities, host species contributions are harder to quantify. Closely related species living in sympatry provide a unique opportunity to investigate species differences without the confounding effects of habitat and dietary variation. We therefore compared and contrasted the gut microbiota of three sympatric plover species: the widespread Kittlitz’s and white-fronted plovers (Anarhynchus pecuarius and A. marginatus) and the endemic and vulnerable Madagascar plover (A. thoracicus). Results We found no significant differences in the beta diversity (composition) of the gut microbiota of the three species. However, A. thoracicus exhibited higher intraspecific compositional similarity (i.e. lower pairwise distances) than the other two species; this pattern was especially pronounced among juveniles. By contrast, microbial alpha diversity varied significantly among the species, being highest in A. pecuarius, intermediate in A. marginatus and lowest in A. thoracicus. This pattern was again stronger among juveniles. Geographical distance did not significantly affect the composition of the gut microbiota, but genetic relatedness did. Conclusion While patterns of microbial diversity varied across species, the lack of compositional differences suggests that habitat and diet likely exert a strong influence on the gut microbiota of plovers. This may be enhanced by their precocial, ground-dwelling nature, which could facilitate the horizontal transmission of microbes from the environment. We hypothesise that gut microbiota diversity in plovers primarily reflects the ecological pool of microbiota, which is subsequently modified by host-specific factors including genetics. The reduced microbial and genetic diversity of the endemic A. thoracicus may hinder its ability to adapt to environmental changes, highlighting the need for increased conservation efforts for this vulnerable species.https://doi.org/10.1186/s12862-024-02329-9Gut microbiotaGeneticsHolobiontEndemicMadagascarPlovers
spellingShingle Hugo Pereira
Nayden Chakarov
Barbara A. Caspers
Marc Gilles
William Jones
Tafitasoa Mijoro
Sama Zefania
Tamás Székely
Oliver Krüger
Joseph I. Hoffman
The gut microbiota of three avian species living in sympatry
BMC Ecology and Evolution
Gut microbiota
Genetics
Holobiont
Endemic
Madagascar
Plovers
title The gut microbiota of three avian species living in sympatry
title_full The gut microbiota of three avian species living in sympatry
title_fullStr The gut microbiota of three avian species living in sympatry
title_full_unstemmed The gut microbiota of three avian species living in sympatry
title_short The gut microbiota of three avian species living in sympatry
title_sort gut microbiota of three avian species living in sympatry
topic Gut microbiota
Genetics
Holobiont
Endemic
Madagascar
Plovers
url https://doi.org/10.1186/s12862-024-02329-9
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