Natural variation in sugar tolerance associates with changes in signaling and mitochondrial ribosome biogenesis

  1. Richard G Melvin
  2. Nicole Lamichane
  3. Essi Havula
  4. Krista Kokki
  5. Charles Soeder
  6. Corbin D Jones
  7. Ville Hietakangas  Is a corresponding author
  1. University of Minnesota, United States
  2. University of Helsinki, Finland
  3. The University of North Carolina at Chapel Hill, United States

Abstract

How dietary selection impacts genome evolution to define the optimal range of nutrient intake is a poorly understood question with medical relevance. We have addressed this question by analyzing Drosophila simulans and sechellia, recently diverged species with differential diet choice. D. sechellia larvae, specialized to a nutrient scarce diet, did not survive on sugar rich conditions, while the generalist species D. simulans was sugar tolerant. Sugar tolerance in D. simulans was a tradeoff for performance on low energy diet and was associated with global reprogramming of metabolic gene expression. Hybridization and phenotype-based introgression revealed the genomic regions of D. simulans that were sufficient for sugar tolerance. These regions included genes that are involved in mitochondrial ribosome biogenesis and intracellular signaling, such as PPP1R15/Gadd34 and SERCA, which contributed to sugar tolerance. In conclusion, genomic variation affecting genes involved in global metabolic control defines the optimal range for dietary macronutrient composition.

Data availability

Genome sequencing and RNA sequencing datasets have bee placed into NCBI SRA archive, Study # SRP158000. A link is provided for reviewers in the Materials and Methods.

The following data sets were generated
The following previously published data sets were used

Article and author information

Author details

  1. Richard G Melvin

    Faculty of Biological and Environmental Sciences, University of Minnesota, Duluth, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-6428-6763
  2. Nicole Lamichane

    Faculty of Biological and Environmental Sciences, University of Helsinki, Helsinki, Finland
    Competing interests
    The authors declare that no competing interests exist.
  3. Essi Havula

    Faculty of Biological and Environmental Sciences, University of Helsinki, Helsinki, Finland
    Competing interests
    The authors declare that no competing interests exist.
  4. Krista Kokki

    Faculty of Biological and Environmental Sciences, University of Helsinki, Helsinki, Finland
    Competing interests
    The authors declare that no competing interests exist.
  5. Charles Soeder

    Biology Department, The University of North Carolina at Chapel Hill, Chapel Hill, United States
    Competing interests
    The authors declare that no competing interests exist.
  6. Corbin D Jones

    Biology Department, The University of North Carolina at Chapel Hill, Chapel Hill, United States
    Competing interests
    The authors declare that no competing interests exist.
  7. Ville Hietakangas

    Faculty of Biological and Environmental Sciences, University of Helsinki, Helsinki, Finland
    For correspondence
    ville.hietakangas@helsinki.fi
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-9900-7549

Funding

Suomen Akatemia (286767)

  • Ville Hietakangas

Novo Nordisk Foundation (NNF16OC0021460)

  • Ville Hietakangas

Sigrid Juséliuksen Säätiö

  • Ville Hietakangas

Finnish Diabetes Foundation

  • Ville Hietakangas

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. Patricia J Wittkopp, University of Michigan, United States

Publication history

  1. Received: August 6, 2018
  2. Accepted: November 27, 2018
  3. Accepted Manuscript published: November 27, 2018 (version 1)
  4. Version of Record published: December 20, 2018 (version 2)

Copyright

© 2018, Melvin 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. Richard G Melvin
  2. Nicole Lamichane
  3. Essi Havula
  4. Krista Kokki
  5. Charles Soeder
  6. Corbin D Jones
  7. Ville Hietakangas
(2018)
Natural variation in sugar tolerance associates with changes in signaling and mitochondrial ribosome biogenesis
eLife 7:e40841.
https://doi.org/10.7554/eLife.40841

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