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

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.

Data availability

Data has been deposited to the Sequence Read Archive under the accession PRJNA530695. All scripts used in data analysis are available at https://github.com/jpverta/verta_jones_elife_2019.git

The following data sets were generated

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.

Reviewing Editor

  1. Juliette de Meaux, University of Cologne, Germany

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).

Version 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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  1. Jukka-Pekka Verta
  2. Felicity C Jones
(2019)
Predominance of cis-regulatory changes in parallel expression divergence of sticklebacks
eLife 8:e43785.
https://doi.org/10.7554/eLife.43785

Share this article

https://doi.org/10.7554/eLife.43785

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