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Gut microbiome diversity affects fish behaviour and is influenced by host genetics and early rearing conditions

Sofia Consuegra del Olmo Orcid Logo, ISHRAT ANKA, Tamsyn Uren Webster Orcid Logo, SAMUEL MCLAUGHLIN, Ben Overland, Matthew Hitchings Orcid Logo, Carlos Garcia De Leaniz Orcid Logo

Open Biology, Volume: 15, Issue: 4, Start page: 240232

Swansea University Authors: Sofia Consuegra del Olmo Orcid Logo, ISHRAT ANKA, Tamsyn Uren Webster Orcid Logo, SAMUEL MCLAUGHLIN, Ben Overland, Matthew Hitchings Orcid Logo, Carlos Garcia De Leaniz Orcid Logo

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DOI (Published version): 10.1098/rsob.240232

Abstract

The gut microbiota influences human and animal cognition and behaviour through its effects on the endocrine and immune systems. The microbiome–behaviour relationship may be especially relevant for fish, due to their diverse evolutionary history and potential implications for farming and conservation...

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Published in: Open Biology
ISSN: 2046-2441
Published: The Royal Society 2025
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URI: https://cronfa.swan.ac.uk/Record/cronfa69060
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The microbiome&#x2013;behaviour relationship may be especially relevant for fish, due to their diverse evolutionary history and potential implications for farming and conservation. Yet, there is limited research on the interaction between gut microbiome and behaviour in non-model fish. We manipulated the rearing environment and diet of fish from two inbred strains of the self-fertilizing mangrove killifish (Kryptolebias marmoratus) and assessed the effects on the gut microbiome and its interactions with anxiety-like behaviours. We found that microbiota composition and alpha diversity were significantly influenced by host genetics (strain), hatching mode (naturally or artificial dechorionation) and diet, but not by environmental enrichment. Fish activity level and inspections of a novel object were strongly associated with microbiota community composition and alpha diversity. The microbial taxa associated with differences in behaviour were dominated by Bacteroidales, potentially related to the production of metabolites affecting neural development. 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spelling 2025-04-24T15:16:20.7172511 v2 69060 2025-03-07 Gut microbiome diversity affects fish behaviour and is influenced by host genetics and early rearing conditions 241f2810ab8f56be53ca8af23e384c6e 0000-0003-4403-2509 Sofia Consuegra del Olmo Sofia Consuegra del Olmo true false a463eddc946c95f3a3f15e3c13fcfb7d ISHRAT ANKA ISHRAT ANKA true false 3ea91c154926c86f89ea6a761122ecf6 0000-0002-0072-9745 Tamsyn Uren Webster Tamsyn Uren Webster true false 26c3f90063f065727fd804e44916f9db SAMUEL MCLAUGHLIN SAMUEL MCLAUGHLIN true false c8b1fd35f9681473ea859281be90b3d2 Ben Overland Ben Overland true false be98847c72c14a731c4a6b7bc02b3bcf 0000-0002-5527-4709 Matthew Hitchings Matthew Hitchings true false 1c70acd0fd64edb0856b7cf34393ab02 0000-0003-1650-2729 Carlos Garcia De Leaniz Carlos Garcia De Leaniz true false 2025-03-07 BGPS The gut microbiota influences human and animal cognition and behaviour through its effects on the endocrine and immune systems. The microbiome–behaviour relationship may be especially relevant for fish, due to their diverse evolutionary history and potential implications for farming and conservation. Yet, there is limited research on the interaction between gut microbiome and behaviour in non-model fish. We manipulated the rearing environment and diet of fish from two inbred strains of the self-fertilizing mangrove killifish (Kryptolebias marmoratus) and assessed the effects on the gut microbiome and its interactions with anxiety-like behaviours. We found that microbiota composition and alpha diversity were significantly influenced by host genetics (strain), hatching mode (naturally or artificial dechorionation) and diet, but not by environmental enrichment. Fish activity level and inspections of a novel object were strongly associated with microbiota community composition and alpha diversity. The microbial taxa associated with differences in behaviour were dominated by Bacteroidales, potentially related to the production of metabolites affecting neural development. We suggest that the association between microbiome and fish behaviour could be an indirect effect of the modulation of the gut microbiota by host genetics and early rearing conditions, which could be affecting the production of microbial metabolites that interact with the fish physiology. Journal Article Open Biology 15 4 240232 The Royal Society 2046-2441 host–microbiome interaction, probiotic, environmental enrichment, fish microbiome, novel object 16 4 2025 2025-04-16 10.1098/rsob.240232 COLLEGE NANME Biosciences Geography and Physics School COLLEGE CODE BGPS Swansea University SU Library paid the OA fee (TA Institutional Deal) I.Z.A. was supported by a Commonwealth PhD Scholarship (BDCS-2020-41). S.C. was partially funded by a Royal Society Industry Fellowship (IF\R1\231030) and by the Programme ATRAE (REF ATR2023-144170 funded by MICIU/AEI/10.13039/501100011033). C.G.d.L. was partially supported by the Programme ATRAE (REF ATR2023-143937 funded by MICIU/AEI/10.13039/501100011033). 2025-04-24T15:16:20.7172511 2025-03-07T09:32:09.3868065 Faculty of Science and Engineering School of Biosciences, Geography and Physics - Biosciences Sofia Consuegra del Olmo 0000-0003-4403-2509 1 ISHRAT ANKA 2 Tamsyn Uren Webster 0000-0002-0072-9745 3 SAMUEL MCLAUGHLIN 4 Ben Overland 5 Matthew Hitchings 0000-0002-5527-4709 6 Carlos Garcia De Leaniz 0000-0003-1650-2729 7 69060__34104__873bcae55cfa4bf193efdac201c1d242.pdf 69060.VOR.pdf 2025-04-24T15:11:22.5885946 Output 5013759 application/pdf Version of Record true © 2025 The Authors. Published by the Royal Society under the terms of the Creative Commons Attribution License (CC BY). true eng https://creativecommons.org/licenses/by/4.0/
title Gut microbiome diversity affects fish behaviour and is influenced by host genetics and early rearing conditions
spellingShingle Gut microbiome diversity affects fish behaviour and is influenced by host genetics and early rearing conditions
Sofia Consuegra del Olmo
ISHRAT ANKA
Tamsyn Uren Webster
SAMUEL MCLAUGHLIN
Ben Overland
Matthew Hitchings
Carlos Garcia De Leaniz
title_short Gut microbiome diversity affects fish behaviour and is influenced by host genetics and early rearing conditions
title_full Gut microbiome diversity affects fish behaviour and is influenced by host genetics and early rearing conditions
title_fullStr Gut microbiome diversity affects fish behaviour and is influenced by host genetics and early rearing conditions
title_full_unstemmed Gut microbiome diversity affects fish behaviour and is influenced by host genetics and early rearing conditions
title_sort Gut microbiome diversity affects fish behaviour and is influenced by host genetics and early rearing conditions
author_id_str_mv 241f2810ab8f56be53ca8af23e384c6e
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1c70acd0fd64edb0856b7cf34393ab02
author_id_fullname_str_mv 241f2810ab8f56be53ca8af23e384c6e_***_Sofia Consuegra del Olmo
a463eddc946c95f3a3f15e3c13fcfb7d_***_ISHRAT ANKA
3ea91c154926c86f89ea6a761122ecf6_***_Tamsyn Uren Webster
26c3f90063f065727fd804e44916f9db_***_SAMUEL MCLAUGHLIN
c8b1fd35f9681473ea859281be90b3d2_***_Ben Overland
be98847c72c14a731c4a6b7bc02b3bcf_***_Matthew Hitchings
1c70acd0fd64edb0856b7cf34393ab02_***_Carlos Garcia De Leaniz
author Sofia Consuegra del Olmo
ISHRAT ANKA
Tamsyn Uren Webster
SAMUEL MCLAUGHLIN
Ben Overland
Matthew Hitchings
Carlos Garcia De Leaniz
author2 Sofia Consuegra del Olmo
ISHRAT ANKA
Tamsyn Uren Webster
SAMUEL MCLAUGHLIN
Ben Overland
Matthew Hitchings
Carlos Garcia De Leaniz
format Journal article
container_title Open Biology
container_volume 15
container_issue 4
container_start_page 240232
publishDate 2025
institution Swansea University
issn 2046-2441
doi_str_mv 10.1098/rsob.240232
publisher The Royal Society
college_str Faculty of Science and Engineering
hierarchytype
hierarchy_top_id facultyofscienceandengineering
hierarchy_top_title Faculty of Science and Engineering
hierarchy_parent_id facultyofscienceandengineering
hierarchy_parent_title Faculty of Science and Engineering
department_str School of Biosciences, Geography and Physics - Biosciences{{{_:::_}}}Faculty of Science and Engineering{{{_:::_}}}School of Biosciences, Geography and Physics - Biosciences
document_store_str 1
active_str 0
description The gut microbiota influences human and animal cognition and behaviour through its effects on the endocrine and immune systems. The microbiome–behaviour relationship may be especially relevant for fish, due to their diverse evolutionary history and potential implications for farming and conservation. Yet, there is limited research on the interaction between gut microbiome and behaviour in non-model fish. We manipulated the rearing environment and diet of fish from two inbred strains of the self-fertilizing mangrove killifish (Kryptolebias marmoratus) and assessed the effects on the gut microbiome and its interactions with anxiety-like behaviours. We found that microbiota composition and alpha diversity were significantly influenced by host genetics (strain), hatching mode (naturally or artificial dechorionation) and diet, but not by environmental enrichment. Fish activity level and inspections of a novel object were strongly associated with microbiota community composition and alpha diversity. The microbial taxa associated with differences in behaviour were dominated by Bacteroidales, potentially related to the production of metabolites affecting neural development. We suggest that the association between microbiome and fish behaviour could be an indirect effect of the modulation of the gut microbiota by host genetics and early rearing conditions, which could be affecting the production of microbial metabolites that interact with the fish physiology.
published_date 2025-04-16T08:27:36Z
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