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

  1. Nicholas O Burton  Is a corresponding author
  2. Alexandra Willis
  3. Kinsey Fisher
  4. Fabian Braukmann
  5. Jonathan Price
  6. Lewis Stevens
  7. L Ryan Baugh
  8. Aaron W Reinke
  9. Eric A Miska
  1. University of Cambridge, United Kingdom
  2. University of Toronto, Canada
  3. Duke University, United States
  4. Northwestern University, United States

Abstract

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 C. 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 trade-offs 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 2-fold 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 2-fold 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.

Data availability

RNA-seq data that support the findings of this study have been deposited at NCBI GEO and are available under the accession code GSE173987.

The following data sets were generated
The following previously published data sets were used

Article and author information

Author details

  1. Nicholas O Burton

    Centre for Trophoblast Research, University of Cambridge, Cambridge, United Kingdom
    For correspondence
    nob20@cam.ac.uk
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-5495-3988
  2. Alexandra Willis

    University of Toronto, Toronto, Canada
    Competing interests
    The authors declare that no competing interests exist.
  3. Kinsey Fisher

    Duke University, Durham, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Fabian Braukmann

    Centre for Trophoblast Research, University of Cambridge, Cambridge, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  5. Jonathan Price

    The Gurdon Institute, University of Cambridge, Cambridge, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-6554-5667
  6. Lewis Stevens

    Department of Molecular Biosciences, Northwestern University, Evanston, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-6075-8273
  7. L Ryan Baugh

    Duke University, Durham, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-2148-5492
  8. Aaron W Reinke

    University of Toronto, Toronto, Canada
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-7612-5342
  9. Eric A Miska

    The Gurdon Institute, University of Cambridge, Cambridge, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-4450-576X

Funding

Centre Trophoblast Research (Next Generation fellowship)

  • Nicholas O Burton

National Institutes of Health

  • Kinsey Fisher
  • L Ryan Baugh

National Institutes of Health (GM117408)

  • L Ryan Baugh

Natural Sciences and Engineering Research Council of Canada (Grant #522691522691)

  • Alexandra Willis
  • Aaron W Reinke

Alfred P Sloan Research Fellowship (FG2019-12040)

  • Aaron W Reinke

Cancer Research UK (C13474/A18583)

  • Eric A Miska

Cancer Research UK (C6946/A14492)

  • Eric A Miska

Wellcome Trust (104640/Z/14/Z)

  • Eric A Miska

Wellcome Trust (092096/Z/10/Z)

  • Eric A Miska

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. Diethard Tautz, Max-Planck Institute for Evolutionary Biology, Germany

Publication history

  1. Preprint posted: May 8, 2021 (view preprint)
  2. Received: August 27, 2021
  3. Accepted: September 27, 2021
  4. Accepted Manuscript published: October 8, 2021 (version 1)
  5. Version of Record published: November 5, 2021 (version 2)

Copyright

© 2021, Burton et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Nicholas O Burton
  2. Alexandra Willis
  3. Kinsey Fisher
  4. Fabian Braukmann
  5. Jonathan Price
  6. Lewis Stevens
  7. L Ryan Baugh
  8. Aaron W Reinke
  9. Eric A Miska
(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

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