Intergenerational adaptations to stress are evolutionarily conserved, stress-specific, and have deleterious trade-offs
- University of Cambridge, United Kingdom
- University of Toronto, Canada
- Duke University, United States
- 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.
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The time-resolved transcriptome of C. elegansNCBI Sequence Read Archive - Supplemental Table 1.
Article and author information
Author details
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
- Diethard Tautz, Max-Planck Institute for Evolutionary Biology, Germany
Version history
- Preprint posted: May 8, 2021 (view preprint)
- Received: August 27, 2021
- Accepted: September 27, 2021
- Accepted Manuscript published: October 8, 2021 (version 1)
- 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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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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