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:	Nicholas O Burton, Alexandra Willis, Kinsey Fisher, Fabian Braukmann, Jonathan Price, Lewis Stevens, L Ryan Baugh, Aaron Reinke, Eric A Miska
Formato:	article
Lenguaje:	EN
Publicado:	eLife Sciences Publications Ltd 2021
Materias:	transgenerational P. vranovensis osmotic stress nutrient stress N. parisii infection intergenerational Medicine R Science Q Biology (General) QH301-705.5
Acceso en línea:	https://doaj.org/article/5d9319ea5a9c4c73a79716efcb5fe327
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spelling	oai:doaj.org-article:5d9319ea5a9c4c73a79716efcb5fe3272021-11-05T11:53:00ZIntergenerational adaptations to stress are evolutionarily conserved, stress-specific, and have deleterious trade-offs10.7554/eLife.734252050-084Xe73425https://doaj.org/article/5d9319ea5a9c4c73a79716efcb5fe3272021-10-01T00:00:00Zhttps://elifesciences.org/articles/73425https://doaj.org/toc/2050-084XDespite 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.Nicholas O BurtonAlexandra WillisKinsey FisherFabian BraukmannJonathan PriceLewis StevensL Ryan BaughAaron ReinkeEric A MiskaeLife Sciences Publications LtdarticletransgenerationalP. vranovensisosmotic stressnutrient stressN. parisii infectionintergenerationalMedicineRScienceQBiology (General)QH301-705.5ENeLife, Vol 10 (2021)
institution	DOAJ
collection	DOAJ
language	EN
topic	transgenerational P. vranovensis osmotic stress nutrient stress N. parisii infection intergenerational Medicine R Science Q Biology (General) QH301-705.5
spellingShingle	transgenerational P. vranovensis osmotic stress nutrient stress N. parisii infection intergenerational Medicine R Science Q Biology (General) QH301-705.5 Nicholas O Burton Alexandra Willis Kinsey Fisher Fabian Braukmann Jonathan Price Lewis Stevens L Ryan Baugh Aaron Reinke Eric A Miska Intergenerational adaptations to stress are evolutionarily conserved, stress-specific, and have deleterious trade-offs
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.
format	article
author	Nicholas O Burton Alexandra Willis Kinsey Fisher Fabian Braukmann Jonathan Price Lewis Stevens L Ryan Baugh Aaron Reinke Eric A Miska
author_facet	Nicholas O Burton Alexandra Willis Kinsey Fisher Fabian Braukmann Jonathan Price Lewis Stevens L Ryan Baugh Aaron Reinke Eric A Miska
author_sort	Nicholas O Burton
title	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_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_sort	intergenerational adaptations to stress are evolutionarily conserved, stress-specific, and have deleterious trade-offs
publisher	eLife Sciences Publications Ltd
publishDate	2021
url	https://doaj.org/article/5d9319ea5a9c4c73a79716efcb5fe327
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Intergenerational adaptations to stress are evolutionarily conserved, stress-specific, and have deleterious trade-offs

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