1. Evolutionary Biology
  2. Genetics and Genomics
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Predominance of cis-regulatory changes in parallel expression divergence of sticklebacks

  1. Jukka-Pekka Verta  Is a corresponding author
  2. Felicity C Jones  Is a corresponding author
  1. University of Helsinki, Finland
  2. Friedrich Miescher Laboratory of the Max Planck Society, Germany
Research Article
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Cite this article as: eLife 2019;8:e43785 doi: 10.7554/eLife.43785

Abstract

Regulation of gene expression is thought to play a major role in adaptation but the relative importance of cis- and trans- regulatory mechanisms in the early stages of adaptive divergence is unclear. Using RNAseq of threespine stickleback fish gill tissue from four independent marine-freshwater ecotype pairs and their F1 hybrids, we show that cis-acting (allele-specific) regulation consistently predominates gene expression divergence. Genes showing parallel marine-freshwater expression divergence are found near to adaptive genomic regions, show signatures of natural selection around their transcription start sites and are enriched for cis-regulatory control. For genes with parallel increased expression among freshwater fish, the quantitative degree of cis- and trans-regulation is also highly correlated across populations, suggesting a shared genetic basis. Compared to other forms of regulation, cis-regulation tends to show greater additivity and stability across different genetic and environmental contexts, making it a fertile substrate for the early stages of adaptive evolution.

Article and author information

Author details

  1. Jukka-Pekka Verta

    Organismal and Evolutionary Biology, University of Helsinki, Helsinki, Finland
    For correspondence
    jukka-pekka.verta@helsinki.fi
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-1701-6124
  2. Felicity C Jones

    Friedrich Miescher Laboratory of the Max Planck Society, Tübingen, Germany
    For correspondence
    fcjones@tuebingen.mpg.de
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-5027-1031

Funding

H2020 European Research Council (FP7)

  • Felicity C Jones

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

Ethics

Animal experimentation: All of the animals were housed at an approved animal facility and handled according to Baden-Württemberg State approved protocols at the Max Planck Institute for Developmental Biology, Tübingen, Germany (license numbers 35/9185.82-5 and 35/9185.40).

Reviewing Editor

  1. Juliette de Meaux, University of Cologne, Germany

Publication history

  1. Received: November 27, 2018
  2. Accepted: May 1, 2019
  3. Accepted Manuscript published: May 15, 2019 (version 1)
  4. Version of Record published: June 5, 2019 (version 2)

Copyright

© 2019, Verta & Jones

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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