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Intergenerational adaptations to stress are evolutionarily conserved, stress-specific, and have deleterious trade-offs

Despite reports of parental exposure to stress promoting physiological adaptations in progeny in diverse organisms, there remains considerable debate over the significance and evolutionary conservation of such multigenerational effects. Here, we investigate four independent models of intergeneration...

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Autores principales: Burton, Nicholas O, Willis, Alexandra, Fisher, Kinsey, Braukmann, Fabian, Price, Jonathan, Stevens, Lewis, Baugh, L Ryan, Reinke, Aaron, Miska, Eric A
Formato: Online Artículo Texto
Lenguaje:English
Publicado: eLife Sciences Publications, Ltd 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8570697/
https://www.ncbi.nlm.nih.gov/pubmed/34622777
http://dx.doi.org/10.7554/eLife.73425
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author Burton, Nicholas O
Willis, Alexandra
Fisher, Kinsey
Braukmann, Fabian
Price, Jonathan
Stevens, Lewis
Baugh, L Ryan
Reinke, Aaron
Miska, Eric A
author_facet Burton, Nicholas O
Willis, Alexandra
Fisher, Kinsey
Braukmann, Fabian
Price, Jonathan
Stevens, Lewis
Baugh, L Ryan
Reinke, Aaron
Miska, Eric A
author_sort Burton, Nicholas O
collection PubMed
description Despite reports of parental exposure to stress promoting physiological adaptations in progeny in diverse organisms, there remains considerable debate over the significance and evolutionary conservation of such multigenerational effects. Here, we investigate four independent models of intergenerational adaptations to stress in Caenorhabditis elegans – bacterial infection, eukaryotic infection, osmotic stress, and nutrient stress – across multiple species. We found that all four intergenerational physiological adaptations are conserved in at least one other species, that they are stress -specific, and that they have deleterious tradeoffs in mismatched environments. By profiling the effects of parental bacterial infection and osmotic stress exposure on progeny gene expression across species, we established a core set of 587 genes that exhibited a greater than twofold intergenerational change in expression in response to stress in C. elegans and at least one other species, as well as a set of 37 highly conserved genes that exhibited a greater than twofold intergenerational change in expression in all four species tested. Furthermore, we provide evidence suggesting that presumed adaptive and deleterious intergenerational effects are molecularly related at the gene expression level. Lastly, we found that none of the effects we detected of these stresses on C. elegans F1 progeny gene expression persisted transgenerationally three generations after stress exposure. We conclude that intergenerational responses to stress play a substantial and evolutionarily conserved role in regulating animal physiology and that the vast majority of the effects of parental stress on progeny gene expression are reversible and not maintained transgenerationally.
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spelling pubmed-85706972021-11-08 Intergenerational adaptations to stress are evolutionarily conserved, stress-specific, and have deleterious trade-offs Burton, Nicholas O Willis, Alexandra Fisher, Kinsey Braukmann, Fabian Price, Jonathan Stevens, Lewis Baugh, L Ryan Reinke, Aaron Miska, Eric A eLife Evolutionary Biology Despite reports of parental exposure to stress promoting physiological adaptations in progeny in diverse organisms, there remains considerable debate over the significance and evolutionary conservation of such multigenerational effects. Here, we investigate four independent models of intergenerational adaptations to stress in Caenorhabditis elegans – bacterial infection, eukaryotic infection, osmotic stress, and nutrient stress – across multiple species. We found that all four intergenerational physiological adaptations are conserved in at least one other species, that they are stress -specific, and that they have deleterious tradeoffs in mismatched environments. By profiling the effects of parental bacterial infection and osmotic stress exposure on progeny gene expression across species, we established a core set of 587 genes that exhibited a greater than twofold intergenerational change in expression in response to stress in C. elegans and at least one other species, as well as a set of 37 highly conserved genes that exhibited a greater than twofold intergenerational change in expression in all four species tested. Furthermore, we provide evidence suggesting that presumed adaptive and deleterious intergenerational effects are molecularly related at the gene expression level. Lastly, we found that none of the effects we detected of these stresses on C. elegans F1 progeny gene expression persisted transgenerationally three generations after stress exposure. We conclude that intergenerational responses to stress play a substantial and evolutionarily conserved role in regulating animal physiology and that the vast majority of the effects of parental stress on progeny gene expression are reversible and not maintained transgenerationally. eLife Sciences Publications, Ltd 2021-10-08 /pmc/articles/PMC8570697/ /pubmed/34622777 http://dx.doi.org/10.7554/eLife.73425 Text en © 2021, Burton et al https://creativecommons.org/licenses/by/4.0/This article is distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use and redistribution provided that the original author and source are credited.
spellingShingle Evolutionary Biology
Burton, Nicholas O
Willis, Alexandra
Fisher, Kinsey
Braukmann, Fabian
Price, Jonathan
Stevens, Lewis
Baugh, L Ryan
Reinke, Aaron
Miska, Eric A
Intergenerational adaptations to stress are evolutionarily conserved, stress-specific, and have deleterious trade-offs
title Intergenerational adaptations to stress are evolutionarily conserved, stress-specific, and have deleterious trade-offs
title_full Intergenerational adaptations to stress are evolutionarily conserved, stress-specific, and have deleterious trade-offs
title_fullStr Intergenerational adaptations to stress are evolutionarily conserved, stress-specific, and have deleterious trade-offs
title_full_unstemmed Intergenerational adaptations to stress are evolutionarily conserved, stress-specific, and have deleterious trade-offs
title_short Intergenerational adaptations to stress are evolutionarily conserved, stress-specific, and have deleterious trade-offs
title_sort intergenerational adaptations to stress are evolutionarily conserved, stress-specific, and have deleterious trade-offs
topic Evolutionary Biology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8570697/
https://www.ncbi.nlm.nih.gov/pubmed/34622777
http://dx.doi.org/10.7554/eLife.73425
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