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Additive and mostly adaptive plastic responses of gene expression to multiple stress in Tribolium castaneum


Koch, Eva L; Guillaume, Frédéric (2020). Additive and mostly adaptive plastic responses of gene expression to multiple stress in Tribolium castaneum. PLoS Genetics, 16(5):e1008768.

Abstract

Gene expression is known to be highly responsive to the environment and important for adjustment of metabolism but there is also growing evidence that differences in gene regulation contribute to species divergence and differences among locally adapted populations. However, most studies so far investigated populations when divergence had already occurred. Selection acting on expression levels at the onset of adaptation to an environmental change has not been characterized. Understanding the mechanisms is further complicated by the fact that environmental change is often multivariate, meaning that organisms are exposed to multiple stressors simultaneously with potentially interactive effects. Here we use a novel approach by combining fitness and whole-transcriptome data in a large-scale experiment to investigate responses to drought, heat and their combination in Tribolium castaneum. We found that fitness was reduced by both stressors and their combined effect was almost additive. Expression data showed that stressor responses were acting independently and did not interfere physiologically. Since we measured expression and fitness within the same individuals, we were able to estimate selection on gene expression levels. We found that variation in fitness can be attributed to gene expression variation and that selection pressures were environment dependent and opposite between control and stress conditions. We could further show that plastic responses of expression were largely adaptive, i.e. in the direction that should increase fitness.

Abstract

Gene expression is known to be highly responsive to the environment and important for adjustment of metabolism but there is also growing evidence that differences in gene regulation contribute to species divergence and differences among locally adapted populations. However, most studies so far investigated populations when divergence had already occurred. Selection acting on expression levels at the onset of adaptation to an environmental change has not been characterized. Understanding the mechanisms is further complicated by the fact that environmental change is often multivariate, meaning that organisms are exposed to multiple stressors simultaneously with potentially interactive effects. Here we use a novel approach by combining fitness and whole-transcriptome data in a large-scale experiment to investigate responses to drought, heat and their combination in Tribolium castaneum. We found that fitness was reduced by both stressors and their combined effect was almost additive. Expression data showed that stressor responses were acting independently and did not interfere physiologically. Since we measured expression and fitness within the same individuals, we were able to estimate selection on gene expression levels. We found that variation in fitness can be attributed to gene expression variation and that selection pressures were environment dependent and opposite between control and stress conditions. We could further show that plastic responses of expression were largely adaptive, i.e. in the direction that should increase fitness.

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Additional indexing

Item Type:Journal Article, refereed, original work
Communities & Collections:07 Faculty of Science > Institute of Evolutionary Biology and Environmental Studies
Dewey Decimal Classification:570 Life sciences; biology
590 Animals (Zoology)
Scopus Subject Areas:Life Sciences > Ecology, Evolution, Behavior and Systematics
Life Sciences > Molecular Biology
Life Sciences > Genetics
Health Sciences > Genetics (clinical)
Life Sciences > Cancer Research
Uncontrolled Keywords:Genetics(clinical), Genetics, Cancer Research, Ecology, Evolution, Behavior and Systematics, Molecular Biology
Language:English
Date:7 May 2020
Deposited On:11 Aug 2020 16:01
Last Modified:12 Aug 2020 20:00
Publisher:Public Library of Science (PLoS)
ISSN:1553-7390
OA Status:Gold
Free access at:Publisher DOI. An embargo period may apply.
Publisher DOI:https://doi.org/10.1371/journal.pgen.1008768
PubMed ID:32379753
Project Information:
  • : FunderSNSF
  • : Grant IDPP00P3_144846
  • : Project TitleCauses and consequences of genetic constraints on adaptation: From gene pleiotropy to species' range evolution
  • : FunderSNSF
  • : Grant IDPP00P3_176965
  • : Project TitleCauses and consequences of genetic constraints on adaptation: From gene pleiotropy to species' range evolution

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