Captive rearing effects on the methylome of Atlantic salmon after oceanic migration: Sex‐specificity and intergenerational stability

Abstract Captive rearing in salmon hatcheries can have considerable impacts on both fish phenotype and fitness within a single generation, even in the absence of genetic change. Evidence for hatchery‐induced changes in DNA methylation is becoming abundant, though questions remain on the sex‐specific...

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Published in:Molecular Ecology Resources
Main Authors: Venney, Clare J., Bouchard, Raphaël, April, Julien, Normandeau, Eric, Lecomte, Laurie, Côté, Guillaume, Bernatchez, Louis
Other Authors: Ministère des Forêts, de la Faune et des Parcs, Natural Sciences and Engineering Research Council of Canada
Format: Article in Journal/Newspaper
Language:English
Published: Wiley 2023
Subjects:
Online Access:http://dx.doi.org/10.1111/1755-0998.13766
https://onlinelibrary.wiley.com/doi/pdf/10.1111/1755-0998.13766
https://onlinelibrary.wiley.com/doi/full-xml/10.1111/1755-0998.13766
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spelling crwiley:10.1111/1755-0998.13766 2024-09-15T17:56:17+00:00 Captive rearing effects on the methylome of Atlantic salmon after oceanic migration: Sex‐specificity and intergenerational stability Venney, Clare J. Bouchard, Raphaël April, Julien Normandeau, Eric Lecomte, Laurie Côté, Guillaume Bernatchez, Louis Ministère des Forêts, de la Faune et des Parcs Natural Sciences and Engineering Research Council of Canada Natural Sciences and Engineering Research Council of Canada 2023 http://dx.doi.org/10.1111/1755-0998.13766 https://onlinelibrary.wiley.com/doi/pdf/10.1111/1755-0998.13766 https://onlinelibrary.wiley.com/doi/full-xml/10.1111/1755-0998.13766 en eng Wiley http://creativecommons.org/licenses/by-nc/4.0/ Molecular Ecology Resources ISSN 1755-098X 1755-0998 journal-article 2023 crwiley https://doi.org/10.1111/1755-0998.13766 2024-08-27T04:28:28Z Abstract Captive rearing in salmon hatcheries can have considerable impacts on both fish phenotype and fitness within a single generation, even in the absence of genetic change. Evidence for hatchery‐induced changes in DNA methylation is becoming abundant, though questions remain on the sex‐specificity of these effects, their persistence until spawning and potential for transmission to future generations. Here we performed whole genome methylation sequencing of fin tissue for 16 hatchery and 16 wild Atlantic salmon ( Salmo salar ) returning to spawn in the Rimouski River, Québec, Canada. We identified two cohorts of hatchery‐reared salmon through methylation analysis, one of which was epigenetically similar to wild fish, suggesting that supplementation efforts may be able to minimize the epigenetic effects of hatchery rearing. We found considerable sex‐specific effects of hatchery rearing, with few genomic regions being affected in both males and females. We also analysed the methylome of 32 F 1 offspring from four groups (pure wild, pure hatchery origin and reciprocal hybrids). We found that few epigenetic changes due to parental hatchery rearing persisted in the F 1 offspring though the patterns of inheritance appear to be complex, involving nonadditive effects. Our results suggest that the epigenetic effects of hatchery rearing can be minimal in F 0 . There may also be minimal epigenetic inheritance and rapid loss of epigenetic changes associated with hatchery rearing. However, due to sex‐specificity and nonadditive patterns of inheritance, methylation changes due to captive rearing are rather complex and the field would benefit from further research on minimizing the epigenetic effects of captive rearing in conservation efforts. Article in Journal/Newspaper Atlantic salmon Salmo salar Wiley Online Library Molecular Ecology Resources
institution Open Polar
collection Wiley Online Library
op_collection_id crwiley
language English
description Abstract Captive rearing in salmon hatcheries can have considerable impacts on both fish phenotype and fitness within a single generation, even in the absence of genetic change. Evidence for hatchery‐induced changes in DNA methylation is becoming abundant, though questions remain on the sex‐specificity of these effects, their persistence until spawning and potential for transmission to future generations. Here we performed whole genome methylation sequencing of fin tissue for 16 hatchery and 16 wild Atlantic salmon ( Salmo salar ) returning to spawn in the Rimouski River, Québec, Canada. We identified two cohorts of hatchery‐reared salmon through methylation analysis, one of which was epigenetically similar to wild fish, suggesting that supplementation efforts may be able to minimize the epigenetic effects of hatchery rearing. We found considerable sex‐specific effects of hatchery rearing, with few genomic regions being affected in both males and females. We also analysed the methylome of 32 F 1 offspring from four groups (pure wild, pure hatchery origin and reciprocal hybrids). We found that few epigenetic changes due to parental hatchery rearing persisted in the F 1 offspring though the patterns of inheritance appear to be complex, involving nonadditive effects. Our results suggest that the epigenetic effects of hatchery rearing can be minimal in F 0 . There may also be minimal epigenetic inheritance and rapid loss of epigenetic changes associated with hatchery rearing. However, due to sex‐specificity and nonadditive patterns of inheritance, methylation changes due to captive rearing are rather complex and the field would benefit from further research on minimizing the epigenetic effects of captive rearing in conservation efforts.
author2 Ministère des Forêts, de la Faune et des Parcs
Natural Sciences and Engineering Research Council of Canada
Natural Sciences and Engineering Research Council of Canada
format Article in Journal/Newspaper
author Venney, Clare J.
Bouchard, Raphaël
April, Julien
Normandeau, Eric
Lecomte, Laurie
Côté, Guillaume
Bernatchez, Louis
spellingShingle Venney, Clare J.
Bouchard, Raphaël
April, Julien
Normandeau, Eric
Lecomte, Laurie
Côté, Guillaume
Bernatchez, Louis
Captive rearing effects on the methylome of Atlantic salmon after oceanic migration: Sex‐specificity and intergenerational stability
author_facet Venney, Clare J.
Bouchard, Raphaël
April, Julien
Normandeau, Eric
Lecomte, Laurie
Côté, Guillaume
Bernatchez, Louis
author_sort Venney, Clare J.
title Captive rearing effects on the methylome of Atlantic salmon after oceanic migration: Sex‐specificity and intergenerational stability
title_short Captive rearing effects on the methylome of Atlantic salmon after oceanic migration: Sex‐specificity and intergenerational stability
title_full Captive rearing effects on the methylome of Atlantic salmon after oceanic migration: Sex‐specificity and intergenerational stability
title_fullStr Captive rearing effects on the methylome of Atlantic salmon after oceanic migration: Sex‐specificity and intergenerational stability
title_full_unstemmed Captive rearing effects on the methylome of Atlantic salmon after oceanic migration: Sex‐specificity and intergenerational stability
title_sort captive rearing effects on the methylome of atlantic salmon after oceanic migration: sex‐specificity and intergenerational stability
publisher Wiley
publishDate 2023
url http://dx.doi.org/10.1111/1755-0998.13766
https://onlinelibrary.wiley.com/doi/pdf/10.1111/1755-0998.13766
https://onlinelibrary.wiley.com/doi/full-xml/10.1111/1755-0998.13766
genre Atlantic salmon
Salmo salar
genre_facet Atlantic salmon
Salmo salar
op_source Molecular Ecology Resources
ISSN 1755-098X 1755-0998
op_rights http://creativecommons.org/licenses/by-nc/4.0/
op_doi https://doi.org/10.1111/1755-0998.13766
container_title Molecular Ecology Resources
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