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Environment‐driven shifts in interindividual variation and phenotypic integration within subnetworks of the mussel transcriptome and proteome

The environment can alter the magnitude of phenotypic variation among individuals, potentially influencing evolutionary trajectories. However, environmental influences on variation are complex and remain understudied. Populations in heterogeneous environments might exhibit more variation, the amount...

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Autores principales: Tanner, Richelle L., Gleason, Lani U., Dowd, W. Wesley
Formato: Online Artículo Texto
Lenguaje:English
Publicado: John Wiley and Sons Inc. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9321163/
https://www.ncbi.nlm.nih.gov/pubmed/35363903
http://dx.doi.org/10.1111/mec.16452
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author Tanner, Richelle L.
Gleason, Lani U.
Dowd, W. Wesley
author_facet Tanner, Richelle L.
Gleason, Lani U.
Dowd, W. Wesley
author_sort Tanner, Richelle L.
collection PubMed
description The environment can alter the magnitude of phenotypic variation among individuals, potentially influencing evolutionary trajectories. However, environmental influences on variation are complex and remain understudied. Populations in heterogeneous environments might exhibit more variation, the amount of variation could differ between benign and stressful conditions, and/or variation might manifest in different ways among stages of the gene‐to‐protein expression cascade or among physiological functions. Here, we explore these three issues by quantifying patterns of inter‐individual variation in both transcript and protein expression levels among California mussels, Mytilus californianus Conrad. Mussels were exposed to five ecologically relevant treatments that varied in the mean and interindividual heterogeneity of body temperature. To target a diverse set of physiological functions, we assessed variation within 19 expression subnetworks, including canonical stress‐response pathways and empirically derived coexpression clusters that represent a diffuse set of cellular processes. Variation in expression was particularly pronounced in the treatments with high mean and heterogeneous body temperatures. However, with few exceptions, environment‐dependent shifts of variation in the transcriptome were not reflected in the proteome. A metric of phenotypic integration provided evidence for a greater degree of constraint on relative expression levels (i.e., stronger correlation) within expression subnetworks in benign, homogeneous environments. Our results suggest that environments that are more stressful on average – and which also tend to be more heterogeneous – can relax these expression constraints and reduce phenotypic integration within biochemical subnetworks. Context‐dependent “unmasking” of functional variation may contribute to interindividual differences in physiological phenotype and performance in stressful environments.
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spelling pubmed-93211632022-07-30 Environment‐driven shifts in interindividual variation and phenotypic integration within subnetworks of the mussel transcriptome and proteome Tanner, Richelle L. Gleason, Lani U. Dowd, W. Wesley Mol Ecol ORIGINAL ARTICLES The environment can alter the magnitude of phenotypic variation among individuals, potentially influencing evolutionary trajectories. However, environmental influences on variation are complex and remain understudied. Populations in heterogeneous environments might exhibit more variation, the amount of variation could differ between benign and stressful conditions, and/or variation might manifest in different ways among stages of the gene‐to‐protein expression cascade or among physiological functions. Here, we explore these three issues by quantifying patterns of inter‐individual variation in both transcript and protein expression levels among California mussels, Mytilus californianus Conrad. Mussels were exposed to five ecologically relevant treatments that varied in the mean and interindividual heterogeneity of body temperature. To target a diverse set of physiological functions, we assessed variation within 19 expression subnetworks, including canonical stress‐response pathways and empirically derived coexpression clusters that represent a diffuse set of cellular processes. Variation in expression was particularly pronounced in the treatments with high mean and heterogeneous body temperatures. However, with few exceptions, environment‐dependent shifts of variation in the transcriptome were not reflected in the proteome. A metric of phenotypic integration provided evidence for a greater degree of constraint on relative expression levels (i.e., stronger correlation) within expression subnetworks in benign, homogeneous environments. Our results suggest that environments that are more stressful on average – and which also tend to be more heterogeneous – can relax these expression constraints and reduce phenotypic integration within biochemical subnetworks. Context‐dependent “unmasking” of functional variation may contribute to interindividual differences in physiological phenotype and performance in stressful environments. John Wiley and Sons Inc. 2022-04-11 2022-06 /pmc/articles/PMC9321163/ /pubmed/35363903 http://dx.doi.org/10.1111/mec.16452 Text en © 2022 The Authors. Molecular Ecology published by John Wiley & Sons Ltd. https://creativecommons.org/licenses/by-nc-nd/4.0/This is an open access article under the terms of the http://creativecommons.org/licenses/by-nc-nd/4.0/ (https://creativecommons.org/licenses/by-nc-nd/4.0/) License, which permits use and distribution in any medium, provided the original work is properly cited, the use is non‐commercial and no modifications or adaptations are made.
spellingShingle ORIGINAL ARTICLES
Tanner, Richelle L.
Gleason, Lani U.
Dowd, W. Wesley
Environment‐driven shifts in interindividual variation and phenotypic integration within subnetworks of the mussel transcriptome and proteome
title Environment‐driven shifts in interindividual variation and phenotypic integration within subnetworks of the mussel transcriptome and proteome
title_full Environment‐driven shifts in interindividual variation and phenotypic integration within subnetworks of the mussel transcriptome and proteome
title_fullStr Environment‐driven shifts in interindividual variation and phenotypic integration within subnetworks of the mussel transcriptome and proteome
title_full_unstemmed Environment‐driven shifts in interindividual variation and phenotypic integration within subnetworks of the mussel transcriptome and proteome
title_short Environment‐driven shifts in interindividual variation and phenotypic integration within subnetworks of the mussel transcriptome and proteome
title_sort environment‐driven shifts in interindividual variation and phenotypic integration within subnetworks of the mussel transcriptome and proteome
topic ORIGINAL ARTICLES
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9321163/
https://www.ncbi.nlm.nih.gov/pubmed/35363903
http://dx.doi.org/10.1111/mec.16452
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