Evolutionary adaptation to juvenile malnutrition impacts adult metabolism and impairs adult fitness in Drosophila

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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Article and author information

Author details

  1. Berra Erkosar

    Department of Ecology and Evolution, University of Lausanne, Lausanne, Switzerland
    Competing interests
    The authors declare that no competing interests exist.
  2. Cindy Dupuis

    Department of Ecology and Evolution, University of Lausanne, Lausanne, Switzerland
    Competing interests
    The authors declare that no competing interests exist.
  3. Fanny Cavigliasso

    Department of Ecology and Evolution, University of Lausanne, Lausanne, Switzerland
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-7764-4934
  4. Loriane Savary

    Department of Ecology and Evolution, University of Lausanne, Lausanne, Switzerland
    Competing interests
    The authors declare that no competing interests exist.
  5. Laurent Kremmer

    Department of Ecology and Evolution, University of Lausanne, Lausanne, Switzerland
    Competing interests
    The authors declare that no competing interests exist.
  6. Hector Gallart-Ayala

    Faculty of Biology and Medicine, University of Lausanne, Lausanne, Switzerland
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-2333-0646
  7. Julijana Ivanisevic

    Faculty of Biology and Medicine, University of Lausanne, Lausanne, Switzerland
    Competing interests
    The authors declare that no competing interests exist.
  8. Tadeusz J Kawecki

    Department of Ecology and Evolution, University of Lausanne, Lausanne, Switzerland
    For correspondence
    tadeusz.kawecki@unil.ch
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-9244-1991

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.

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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  1. Berra Erkosar
  2. Cindy Dupuis
  3. Fanny Cavigliasso
  4. Loriane Savary
  5. Laurent Kremmer
  6. Hector Gallart-Ayala
  7. Julijana Ivanisevic
  8. Tadeusz J Kawecki
(2023)
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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https://doi.org/10.7554/eLife.92465

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