Antibiotic-altered gut microbiota explain host memory plasticity and disrupt pace-of-life covariation for an aquatic snail

Davidson, Gabrielle L. ORCID: https://orcid.org/0000-0001-5663-2662, Cienfuegos, Ignacio A. and Dalesman, Sarah (2024) Antibiotic-altered gut microbiota explain host memory plasticity and disrupt pace-of-life covariation for an aquatic snail. The ISME Journal, 18 (1). ISSN 1751-7362

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Abstract

There is mounting evidence that intestinal microbiota communities and their genes (the gut microbiome) influence how animals behave and interact with their environment, driving individual variation. Individual covariation in behavioural, physiological, and cognitive traits among individuals along a fast-slow continuum is thought to arise because these traits are linked as part of an adaptive pace-of-life strategy. Yet paradoxically, trait intercorrelation is absent, or disrupted in some populations but not others. Here we provide experimental evidence from aquatic pond snails (Lymnaea stagnalis) that environmental stressors and the gut microbiota explain host phenotypic plasticity and disrupted co-variation among traits. Antibiotic exposure at varying levels of ecologically relevant concentrations had multiple effects starting with gut microbiota diversity, differential abundance and inferred function. Memory declined in line with antibiotic concentrations that caused the most profound gut microbiota disruption, and although pace-of-life traits remained rigid, their covariation did not. Moreover, inferred microbial metabolic pathways with biologically relevant host functions explained individual and treatment variation in phenotypes. Together, our results point to the gut microbiome as a proximate mechanism influencing the emergence and maintenance of phenotypic variation within populations and highlights the need to decipher whether the gut microbiome’s sensitivity to environmental pollution facilitates adaptive, or maladaptive phenotypic plasticity.

Item Type: Article
Additional Information: Data and code availability: Sequence data are deposited at the National Center for Biotechnology Information (NCBI) Sequence Read Archive BioProject ID PRJNA1078756. All metadata and R code has been deposited on git hub: https://github.com/DrGLDavidson/lymnaeastagnalis-microbiome. Funding information: This study was supported by an Association for the Study of Animal Behaviour research grant (2018) to G.L.D.
Uncontrolled Keywords: gut microbiota,lymnaea stagnalis,cognition,behavioural plastcity,pace-of-life,syndromes,antibiotic pollution,microbiome-gut-brain axis,memory,behavioural plasticity,personality,microbiome–gut–brain axis,ecology, evolution, behavior and systematics,microbiology,sdg 12 - responsible consumption and production ,/dk/atira/pure/subjectarea/asjc/1100/1105
Faculty \ School: Faculty of Science > School of Biological Sciences
UEA Research Groups: Faculty of Science > Research Centres > Centre for Ecology, Evolution and Conservation
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Depositing User: LivePure Connector
Date Deposited: 31 May 2024 08:30
Last Modified: 10 Oct 2024 11:30
URI: https://ueaeprints.uea.ac.uk/id/eprint/95346
DOI: 10.1093/ismejo/wrae078

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