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

View ORCID ProfileNicholas O. Burton, Alexandra Willis, Kinsey Fisher, Fabian Braukmann, Jon Price, Lewis Stevens, L. Ryan Baugh, View ORCID ProfileAaron Reinke, Eric A. Miska
doi: https://doi.org/10.1101/2021.05.07.443118
Nicholas O. Burton
1Centre for Trophoblast Research, Department of Physiology, Development and Neuroscience, University of Cambridge, Cambridge, CB2 3EG, UK
2Gurdon Institute, University of Cambridge, Cambridge, CB2 1QN, UK
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  • ORCID record for Nicholas O. Burton
  • For correspondence: nob20@cam.ac.uk
Alexandra Willis
3Department of Molecular Genetics, University of Toronto, Toronto, ON, M5G 1M1, Canada
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Kinsey Fisher
4Department of Biology, Duke University, Durham, NC, 27708, USA
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Fabian Braukmann
2Gurdon Institute, University of Cambridge, Cambridge, CB2 1QN, UK
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Jon Price
2Gurdon Institute, University of Cambridge, Cambridge, CB2 1QN, UK
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Lewis Stevens
5Department of Molecular Biosciences, Northwestern University, Evanston, IL, USA
6Wellcome Sanger Institute, Wellcome Genome Campus, Cambridge CB10 1SA, UK
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L. Ryan Baugh
4Department of Biology, Duke University, Durham, NC, 27708, USA
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Aaron Reinke
3Department of Molecular Genetics, University of Toronto, Toronto, ON, M5G 1M1, Canada
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Eric A. Miska
2Gurdon Institute, University of Cambridge, Cambridge, CB2 1QN, UK
6Wellcome Sanger Institute, Wellcome Genome Campus, Cambridge CB10 1SA, UK
7Department of Genetics, University of Cambridge, Downing Street, Cambridge CB2 3EH, UK
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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 279 highly conserved genes that exhibited intergenerational changes in expression in response to stress in all species tested and provide evidence suggesting that presumed adaptive and deleterious intergenerational effects are molecularly related at the gene expression level. By contrast, we found that these same stresses did not elicit any similarly conserved transgenerational changes in progeny gene expression 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.

Competing Interest Statement

The authors have declared no competing interest.

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The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC 4.0 International license.
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Posted May 08, 2021.
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Intergenerational adaptations to stress are evolutionarily conserved, stress-specific, and have deleterious trade-offs
Nicholas O. Burton, Alexandra Willis, Kinsey Fisher, Fabian Braukmann, Jon Price, Lewis Stevens, L. Ryan Baugh, Aaron Reinke, Eric A. Miska
bioRxiv 2021.05.07.443118; doi: https://doi.org/10.1101/2021.05.07.443118
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Intergenerational adaptations to stress are evolutionarily conserved, stress-specific, and have deleterious trade-offs
Nicholas O. Burton, Alexandra Willis, Kinsey Fisher, Fabian Braukmann, Jon Price, Lewis Stevens, L. Ryan Baugh, Aaron Reinke, Eric A. Miska
bioRxiv 2021.05.07.443118; doi: https://doi.org/10.1101/2021.05.07.443118

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