Host habitat rather than evolutionary history explains gut microbiome diversity in sympatric stickleback species

Host-associated microbiota can influence host phenotypic variation, fitness and potential to adapt to local environmental conditions. In turn, both host evolutionary history and the abiotic and biotic environment can influence the diversity and composition of microbiota. Yet, to what extent environm...

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Published in:Frontiers in Microbiology
Main Authors: Aruna M. Shankregowda, Prabhugouda Siriyappagouder, Marijn Kuizenga, Thijs M. P. Bal, Yousri Abdelhafiz, Christophe Eizaguirre, Jorge M. O. Fernandes, Viswanath Kiron, Joost A. M. Raeymaekers
Format: Article
Language:English
Published: Frontiers Media S.A. 2023-10-01
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Online Access:https://www.frontiersin.org/articles/10.3389/fmicb.2023.1232358/full
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author Aruna M. Shankregowda
Prabhugouda Siriyappagouder
Marijn Kuizenga
Thijs M. P. Bal
Yousri Abdelhafiz
Christophe Eizaguirre
Jorge M. O. Fernandes
Viswanath Kiron
Joost A. M. Raeymaekers
author_facet Aruna M. Shankregowda
Prabhugouda Siriyappagouder
Marijn Kuizenga
Thijs M. P. Bal
Yousri Abdelhafiz
Christophe Eizaguirre
Jorge M. O. Fernandes
Viswanath Kiron
Joost A. M. Raeymaekers
author_sort Aruna M. Shankregowda
collection DOAJ
container_title Frontiers in Microbiology
description Host-associated microbiota can influence host phenotypic variation, fitness and potential to adapt to local environmental conditions. In turn, both host evolutionary history and the abiotic and biotic environment can influence the diversity and composition of microbiota. Yet, to what extent environmental and host-specific factors drive microbial diversity remains largely unknown, limiting our understanding of host-microbiome interactions in natural populations. Here, we compared the intestinal microbiota between two phylogenetically related fishes, the three-spined stickleback (Gasterosteus aculeatus) and the nine-spined stickleback (Pungitius pungitius) in a common landscape. Using amplicon sequencing of the V3-V4 region of the bacterial 16S rRNA gene, we characterised the α and β diversity of the microbial communities in these two fish species from both brackish water and freshwater habitats. Across eight locations, α diversity was higher in the nine-spined stickleback, suggesting a broader niche use in this host species. Habitat was a strong determinant of β diversity in both host species, while host species only explained a small fraction of the variation in gut microbial composition. Strong habitat-specific effects overruled effects of geographic distance and historical freshwater colonisation, suggesting that the gut microbiome correlates primarily with local environmental conditions. Interestingly, the effect of habitat divergence on gut microbial communities was stronger in three-spined stickleback than in nine-spined stickleback, possibly mirroring the stronger level of adaptive divergence in this host species. Overall, our results show that microbial communities reflect habitat divergence rather than colonisation history or dispersal limitation of host species.
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spelling doaj-art-ea9fe73ca88d4e07ab9ef47749ef51362025-08-19T22:46:02ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2023-10-011410.3389/fmicb.2023.12323581232358Host habitat rather than evolutionary history explains gut microbiome diversity in sympatric stickleback speciesAruna M. Shankregowda0Prabhugouda Siriyappagouder1Marijn Kuizenga2Thijs M. P. Bal3Yousri Abdelhafiz4Christophe Eizaguirre5Jorge M. O. Fernandes6Viswanath Kiron7Joost A. M. Raeymaekers8Faculty of Biosciences and Aquaculture, Nord University, Bodø, NorwayFaculty of Biosciences and Aquaculture, Nord University, Bodø, NorwayFaculty of Biosciences and Aquaculture, Nord University, Bodø, NorwayFaculty of Biosciences and Aquaculture, Nord University, Bodø, NorwayFaculty of Biosciences and Aquaculture, Nord University, Bodø, NorwaySchool of Biological and Behavioural Sciences, Queen Mary University of London, London, United KingdomFaculty of Biosciences and Aquaculture, Nord University, Bodø, NorwayFaculty of Biosciences and Aquaculture, Nord University, Bodø, NorwayFaculty of Biosciences and Aquaculture, Nord University, Bodø, NorwayHost-associated microbiota can influence host phenotypic variation, fitness and potential to adapt to local environmental conditions. In turn, both host evolutionary history and the abiotic and biotic environment can influence the diversity and composition of microbiota. Yet, to what extent environmental and host-specific factors drive microbial diversity remains largely unknown, limiting our understanding of host-microbiome interactions in natural populations. Here, we compared the intestinal microbiota between two phylogenetically related fishes, the three-spined stickleback (Gasterosteus aculeatus) and the nine-spined stickleback (Pungitius pungitius) in a common landscape. Using amplicon sequencing of the V3-V4 region of the bacterial 16S rRNA gene, we characterised the α and β diversity of the microbial communities in these two fish species from both brackish water and freshwater habitats. Across eight locations, α diversity was higher in the nine-spined stickleback, suggesting a broader niche use in this host species. Habitat was a strong determinant of β diversity in both host species, while host species only explained a small fraction of the variation in gut microbial composition. Strong habitat-specific effects overruled effects of geographic distance and historical freshwater colonisation, suggesting that the gut microbiome correlates primarily with local environmental conditions. Interestingly, the effect of habitat divergence on gut microbial communities was stronger in three-spined stickleback than in nine-spined stickleback, possibly mirroring the stronger level of adaptive divergence in this host species. Overall, our results show that microbial communities reflect habitat divergence rather than colonisation history or dispersal limitation of host species.https://www.frontiersin.org/articles/10.3389/fmicb.2023.1232358/fullhost microbiotasticklebacksevolutionary historyhost habitatadaptationsymbiotic microbiota
spellingShingle Aruna M. Shankregowda
Prabhugouda Siriyappagouder
Marijn Kuizenga
Thijs M. P. Bal
Yousri Abdelhafiz
Christophe Eizaguirre
Jorge M. O. Fernandes
Viswanath Kiron
Joost A. M. Raeymaekers
Host habitat rather than evolutionary history explains gut microbiome diversity in sympatric stickleback species
host microbiota
sticklebacks
evolutionary history
host habitat
adaptation
symbiotic microbiota
title Host habitat rather than evolutionary history explains gut microbiome diversity in sympatric stickleback species
title_full Host habitat rather than evolutionary history explains gut microbiome diversity in sympatric stickleback species
title_fullStr Host habitat rather than evolutionary history explains gut microbiome diversity in sympatric stickleback species
title_full_unstemmed Host habitat rather than evolutionary history explains gut microbiome diversity in sympatric stickleback species
title_short Host habitat rather than evolutionary history explains gut microbiome diversity in sympatric stickleback species
title_sort host habitat rather than evolutionary history explains gut microbiome diversity in sympatric stickleback species
topic host microbiota
sticklebacks
evolutionary history
host habitat
adaptation
symbiotic microbiota
url https://www.frontiersin.org/articles/10.3389/fmicb.2023.1232358/full
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