Evolutionary adaptation to juvenile malnutrition impacts adult metabolism and impairs adult fitness in Drosophila
- University of Lausanne, Switzerland
Abstract
Juvenile undernutrition has lasting effects on adult metabolism of the affected individuals, but it is unclear how adult physiology is shaped over evolutionary time by natural selection driven by juvenile undernutrition. We combined RNAseq, targeted metabolomics and genomics to study the consequences of evolution under juvenile undernutrition for metabolism of reproductively active adult females of Drosophila melanogaster. Compared to Control populations maintained on standard diet, Selected populations maintained for over 230 generations on a nutrient-poor larval diet evolved major changes in adult gene expression and metabolite abundance, in particular affecting amino-acid and purine metabolism. The evolved differences in adult gene expression and metabolite abundance between Selected and Control populations were positively correlated with the corresponding differences previously reported for Selected versus Control larvae. This implies that genetic variants affect both stages similarly. Even when well fed, the metabolic profile of Selected flies resembled that of flies subject to starvation. Finally, Selected flies had lower reproductive output than Controls even when both were raised under the conditions under which the Selected populations evolved. These results imply that evolutionary adaptation to juvenile undernutrition has large pleiotropic consequences for adult metabolism, and that they are costly rather than adaptive for adult fitness. Thus, juvenile and adult metabolism do not appear to evolve independently from each other even in a holometabolous species where the two life stages are separated by a complete metamorphosis.
Data availability
The raw and processed data from the RNAseq on adult carcasses are available from NCBI GEO (accession number GSE193105). Raw data for the previously published larval RNAseq are available from NCBI SRA (accession numbers SAMN07723150-SAMN07723173). Previously published larval metabolome data are available as supplementary material to Cavigliasso, et al. (2023). The adult metabolite abundance data are provided in Supplementary file 8), fecundity and ovariole data in Figure 7-source data 1.
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RNAseq on Drosophila larvae genetically adapted to poor diet in microbiota-colonized and germ-free stateNCBI Short Read Archive, PRJNA412704.
Article and author information
Author details
Hector Gallart-Ayala
Funding
Swiss National Science Foundation (31003A_162732)
- Tadeusz J Kawecki
Swiss National Science Foundation (310030_184791)
- Tadeusz J Kawecki
Research funds of the University of Lausanne
- Tadeusz J Kawecki
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Reviewing Editor
- Luisa Pallares, Friedrich Miescher Laboratory, Germany
Version history
- Preprint posted: January 12, 2022 (view preprint)
- Received: September 3, 2023
- Accepted: October 12, 2023
- Accepted Manuscript published: October 17, 2023 (version 1)
- Version of Record published: November 10, 2023 (version 2)
Copyright
© 2023, Erkosar 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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Evolutionary adaptation to juvenile malnutrition impacts adult metabolism and impairs adult fitness in Drosophila
eLife 12:e92465.
https://doi.org/10.7554/eLife.92465
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