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

Publication ,  Journal Article
Burton, NO; Willis, A; Fisher, K; Braukmann, F; Price, J; Stevens, L; Baugh, LR; Reinke, A; Miska, EA
Published in: eLife
October 2021

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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Published In

eLife

DOI

EISSN

2050-084X

ISSN

2050-084X

Publication Date

October 2021

Volume

10

Start / End Page

e73425

Related Subject Headings

  • Osmotic Pressure
  • Nutritional Status
  • Evolution, Molecular
  • Caenorhabditis elegans
  • Animals
  • Adaptation, Biological
  • 42 Health sciences
  • 32 Biomedical and clinical sciences
  • 31 Biological sciences
  • 0601 Biochemistry and Cell Biology
 

Citation

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Burton, N. O., Willis, A., Fisher, K., Braukmann, F., Price, J., Stevens, L., … Miska, E. A. (2021). Intergenerational adaptations to stress are evolutionarily conserved, stress-specific, and have deleterious trade-offs. ELife, 10, e73425. https://doi.org/10.7554/elife.73425
Burton, Nicholas O., Alexandra Willis, Kinsey Fisher, Fabian Braukmann, Jonathan Price, Lewis Stevens, L Ryan Baugh, Aaron Reinke, and Eric A. Miska. “Intergenerational adaptations to stress are evolutionarily conserved, stress-specific, and have deleterious trade-offs.ELife 10 (October 2021): e73425. https://doi.org/10.7554/elife.73425.
Burton NO, Willis A, Fisher K, Braukmann F, Price J, Stevens L, et al. Intergenerational adaptations to stress are evolutionarily conserved, stress-specific, and have deleterious trade-offs. eLife. 2021 Oct;10:e73425.
Burton, Nicholas O., et al. “Intergenerational adaptations to stress are evolutionarily conserved, stress-specific, and have deleterious trade-offs.ELife, vol. 10, Oct. 2021, p. e73425. Epmc, doi:10.7554/elife.73425.
Burton NO, Willis A, Fisher K, Braukmann F, Price J, Stevens L, Baugh LR, Reinke A, Miska EA. Intergenerational adaptations to stress are evolutionarily conserved, stress-specific, and have deleterious trade-offs. eLife. 2021 Oct;10:e73425.

Published In

eLife

DOI

EISSN

2050-084X

ISSN

2050-084X

Publication Date

October 2021

Volume

10

Start / End Page

e73425

Related Subject Headings

  • Osmotic Pressure
  • Nutritional Status
  • Evolution, Molecular
  • Caenorhabditis elegans
  • Animals
  • Adaptation, Biological
  • 42 Health sciences
  • 32 Biomedical and clinical sciences
  • 31 Biological sciences
  • 0601 Biochemistry and Cell Biology