Ecological adaptation in Atlantic herring is associated with large shifts in allele frequencies at hundreds of loci

  1. Fan Han
  2. Minal Jamsandekar
  3. Mats E Pettersson
  4. Leyi Su
  5. Angela Fuentes-Pardo
  6. Brian Davis
  7. Dorte Bekkevold
  8. Florian Berg
  9. Michele Casini
  10. Geir Dahle
  11. Edward D Farrell
  12. Arild Folkvord
  13. Leif Andersson  Is a corresponding author
  1. Uppsala University, Sweden
  2. Texas A&M University, United States
  3. Technical University of Denmark, Denmark
  4. University of Bergen, Norway
  5. Swedish University of Agricultural Sciences, Sweden
  6. Institute of Marine Research, Norway
  7. University College Dublin, Ireland

Abstract

Atlantic herring is widespread in North Atlantic and adjacent waters and is one of the most abundant vertebrates on earth. This species is well suited to explore genetic adaptation due to minute genetic differentiation at selectively neutral loci. Here we report hundreds of loci underlying ecological adaptation to different geographic areas and spawning conditions. Four of these represent megabase inversions confirmed by long read sequencing. The genetic architecture underlying ecological adaptation in herring deviates from expectation under a classical infinitesimal model for complex traits because of large shifts in allele frequencies at hundreds of loci under selection.

Data availability

Data availability statement. The sequence data generated in this study is available in Bioproject PRJNA642736.Code availability statement. The analyses of data have been carried out with publicly available software and all are cited in the Methods section. Custom scripts used are available in Github (https://github.com/Fan-Han/Population-analysis-with-pooled-data)

The following data sets were generated

Article and author information

Author details

  1. Fan Han

    Science for Life Laboratory, Department of Medical Biochemistry and Microbiology, Uppsala University, Uppsala, Sweden
    Competing interests
    The authors declare that no competing interests exist.
  2. Minal Jamsandekar

    Veterinary Integrative Biosciences, Texas A&M University, College Station, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Mats E Pettersson

    Science for Life Laboratory, Department of Medical Biochemistry and Microbiology, Uppsala University, Uppsala, Sweden
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-7372-9076
  4. Leyi Su

    Science for Life Laboratory, Department of Medical Biochemistry and Microbiology, Uppsala University, Uppsala, Sweden
    Competing interests
    The authors declare that no competing interests exist.
  5. Angela Fuentes-Pardo

    Science for Life Laboratory, Department of Medical Biochemistry and Microbiology, Uppsala University, Uppsala, Sweden
    Competing interests
    The authors declare that no competing interests exist.
  6. Brian Davis

    Veterinary Integrative Biosciences, Texas A&M University, College Station, United States
    Competing interests
    The authors declare that no competing interests exist.
  7. Dorte Bekkevold

    National Institute of Aquatic Resources, Technical University of Denmark, Silkeborg, Denmark
    Competing interests
    The authors declare that no competing interests exist.
  8. Florian Berg

    Department of Biology, University of Bergen, Bergen, Norway
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-1543-8112
  9. Michele Casini

    Department of Aquatic Resources, Swedish University of Agricultural Sciences, Lysekil, Sweden
    Competing interests
    The authors declare that no competing interests exist.
  10. Geir Dahle

    Institute of Marine Research, Bergen, Norway
    Competing interests
    The authors declare that no competing interests exist.
  11. Edward D Farrell

    School of Biology and Environmental Science, University College Dublin, Dublin, Ireland
    Competing interests
    The authors declare that no competing interests exist.
  12. Arild Folkvord

    Department of Biological Sciences, University of Bergen, Bergen, Norway
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-4763-0590
  13. Leif Andersson

    Science for Life Laboratory, Department of Medical Biochemistry and Microbiology, Uppsala University, Uppsala, Sweden
    For correspondence
    leif.andersson@imbim.uu.se
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-4085-6968

Funding

Knut och Alice Wallenbergs Stiftelse (KAW scholar)

  • Leif Andersson

Vetenskapsrådet (Senior professor)

  • Leif Andersson

Research Council of Norway (254774)

  • Arild Folkvord

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

Reviewing Editor

  1. Jonathan Flint, University of California, Los Angeles, United States

Publication history

  1. Received: July 15, 2020
  2. Accepted: December 3, 2020
  3. Accepted Manuscript published: December 4, 2020 (version 1)
  4. Version of Record published: December 15, 2020 (version 2)

Copyright

© 2020, Han 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. Fan Han
  2. Minal Jamsandekar
  3. Mats E Pettersson
  4. Leyi Su
  5. Angela Fuentes-Pardo
  6. Brian Davis
  7. Dorte Bekkevold
  8. Florian Berg
  9. Michele Casini
  10. Geir Dahle
  11. Edward D Farrell
  12. Arild Folkvord
  13. Leif Andersson
(2020)
Ecological adaptation in Atlantic herring is associated with large shifts in allele frequencies at hundreds of loci
eLife 9:e61076.
https://doi.org/10.7554/eLife.61076

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