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Thermal regime during parental sexual maturation, but not during offspring rearing, modulates DNA methylation in brook charr (Salvelinus fontinalis)

Epigenetic inheritance can result in plastic responses to changing environments being faithfully transmitted to offspring. However, it remains unclear how epigenetic mechanisms such as DNA methylation can contribute to multigenerational acclimation and adaptation to environmental stressors. Brook ch...

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Autores principales: Venney, Clare J., Wellband, Kyle W., Normandeau, Eric, Houle, Carolyne, Garant, Dany, Audet, Céline, Bernatchez, Louis
Formato: Online Artículo Texto
Lenguaje:English
Publicado: The Royal Society 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9065957/
https://www.ncbi.nlm.nih.gov/pubmed/35506232
http://dx.doi.org/10.1098/rspb.2022.0670
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author Venney, Clare J.
Wellband, Kyle W.
Normandeau, Eric
Houle, Carolyne
Garant, Dany
Audet, Céline
Bernatchez, Louis
author_facet Venney, Clare J.
Wellband, Kyle W.
Normandeau, Eric
Houle, Carolyne
Garant, Dany
Audet, Céline
Bernatchez, Louis
author_sort Venney, Clare J.
collection PubMed
description Epigenetic inheritance can result in plastic responses to changing environments being faithfully transmitted to offspring. However, it remains unclear how epigenetic mechanisms such as DNA methylation can contribute to multigenerational acclimation and adaptation to environmental stressors. Brook charr (Salvelinus fontinalis), an economically important salmonid, is highly sensitive to thermal stress and is of conservation concern in the context of climate change. We studied the effects of temperature during parental sexual maturation and offspring rearing on whole-genome DNA methylation in brook charr juveniles (fry). Parents were split between warm and cold temperatures during sexual maturation, mated in controlled breeding designs, then offspring from each family were split between warm (8°C) and cold (5°C) rearing environments. Using whole-genome bisulfite sequencing, we found 188 differentially methylated regions (DMRs) due to parental maturation temperature after controlling for family structure. By contrast, offspring rearing temperature had a negligible effect on offspring methylation. Stable intergenerational inheritance of DNA methylation and minimal plasticity in progeny could result in the transmission of acclimatory epigenetic states to offspring, priming them for a warming environment. Our findings have implications pertaining to the role of intergenerational epigenetic inheritance in response to ongoing climate change.
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spelling pubmed-90659572022-05-18 Thermal regime during parental sexual maturation, but not during offspring rearing, modulates DNA methylation in brook charr (Salvelinus fontinalis) Venney, Clare J. Wellband, Kyle W. Normandeau, Eric Houle, Carolyne Garant, Dany Audet, Céline Bernatchez, Louis Proc Biol Sci Evolution Epigenetic inheritance can result in plastic responses to changing environments being faithfully transmitted to offspring. However, it remains unclear how epigenetic mechanisms such as DNA methylation can contribute to multigenerational acclimation and adaptation to environmental stressors. Brook charr (Salvelinus fontinalis), an economically important salmonid, is highly sensitive to thermal stress and is of conservation concern in the context of climate change. We studied the effects of temperature during parental sexual maturation and offspring rearing on whole-genome DNA methylation in brook charr juveniles (fry). Parents were split between warm and cold temperatures during sexual maturation, mated in controlled breeding designs, then offspring from each family were split between warm (8°C) and cold (5°C) rearing environments. Using whole-genome bisulfite sequencing, we found 188 differentially methylated regions (DMRs) due to parental maturation temperature after controlling for family structure. By contrast, offspring rearing temperature had a negligible effect on offspring methylation. Stable intergenerational inheritance of DNA methylation and minimal plasticity in progeny could result in the transmission of acclimatory epigenetic states to offspring, priming them for a warming environment. Our findings have implications pertaining to the role of intergenerational epigenetic inheritance in response to ongoing climate change. The Royal Society 2022-05-11 2022-05-04 /pmc/articles/PMC9065957/ /pubmed/35506232 http://dx.doi.org/10.1098/rspb.2022.0670 Text en © 2022 The Authors. https://creativecommons.org/licenses/by/4.0/Published by the Royal Society under the terms of the Creative Commons Attribution License http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, provided the original author and source are credited.
spellingShingle Evolution
Venney, Clare J.
Wellband, Kyle W.
Normandeau, Eric
Houle, Carolyne
Garant, Dany
Audet, Céline
Bernatchez, Louis
Thermal regime during parental sexual maturation, but not during offspring rearing, modulates DNA methylation in brook charr (Salvelinus fontinalis)
title Thermal regime during parental sexual maturation, but not during offspring rearing, modulates DNA methylation in brook charr (Salvelinus fontinalis)
title_full Thermal regime during parental sexual maturation, but not during offspring rearing, modulates DNA methylation in brook charr (Salvelinus fontinalis)
title_fullStr Thermal regime during parental sexual maturation, but not during offspring rearing, modulates DNA methylation in brook charr (Salvelinus fontinalis)
title_full_unstemmed Thermal regime during parental sexual maturation, but not during offspring rearing, modulates DNA methylation in brook charr (Salvelinus fontinalis)
title_short Thermal regime during parental sexual maturation, but not during offspring rearing, modulates DNA methylation in brook charr (Salvelinus fontinalis)
title_sort thermal regime during parental sexual maturation, but not during offspring rearing, modulates dna methylation in brook charr (salvelinus fontinalis)
topic Evolution
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9065957/
https://www.ncbi.nlm.nih.gov/pubmed/35506232
http://dx.doi.org/10.1098/rspb.2022.0670
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