1. Evolutionary Biology
  2. Genetics and Genomics
Download icon

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
  • Cited 5
  • Views 1,794
  • Annotations
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.

Metrics

  • 1,794
    Page views
  • 326
    Downloads
  • 5
    Citations

Article citation count generated by polling the highest count across the following sources: Crossref, PubMed Central, Scopus.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Download citations (links to download the citations from this article in formats compatible with various reference manager tools)

Open citations (links to open the citations from this article in various online reference manager services)

Further reading

    1. Evolutionary Biology
    2. Genetics and Genomics
    Snigdha Misra, Mariana F Wolfner
    Research Article Updated

    When females mate with more than one male, the males’ paternity share is affected by biases in sperm use. These competitive interactions occur while female and male molecules and cells work interdependently to optimize fertility, including modifying the female’s physiology through interactions with male seminal fluid proteins (SFPs). Some modifications persist, indirectly benefiting later males. Indeed, rival males tailor their ejaculates accordingly. Here, we show that SFPs from one male can directly benefit a rival’s sperm. We report that Sex Peptide (SP) that a female Drosophila receives from a male can bind sperm that she had stored from a previous male, and rescue the sperm utilization and fertility defects of an SP-deficient first-male. Other seminal proteins received in the first mating ‘primed’ the sperm (or the female) for this binding. Thus, SP from one male can directly benefit another, making SP a key molecule in inter-ejaculate interaction.

    1. Evolutionary Biology
    Neal J Dawson et al.
    Research Article

    High-altitude environments require that animals meet the metabolic O2 demands for locomotion and thermogenesis in O2-thin air, but the degree to which convergent metabolic changes have arisen across independent high-altitude lineages or the speed at which such changes arise is unclear. We examined seven high-altitude waterfowl that have inhabited the Andes (3812-4806m elevation) over varying evolutionary time scales, to elucidate changes in biochemical pathways of energy metabolism in flight muscle relative to low-altitude sister-taxa. Convergent changes across high-altitude taxa included increased hydroxyacyl-coA dehydrogenase and succinate dehydrogenase activities, decreased lactate dehydrogenase, pyruvate kinase, creatine kinase, and cytochrome c oxidase activities, and increased myoglobin content. ATP synthase activity increased in only the longest established high-altitude taxa, whereas hexokinase activity increased in only newly established taxa. Therefore, changes in pathways of lipid oxidation, glycolysis, and mitochondrial oxidative phosphorylation are common strategies to cope with high-altitude hypoxia, but some changes require longer evolutionary time to arise.