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

Version 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.

Metrics

  • 3,890
    views
  • 488
    downloads
  • 58
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

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)

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

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

  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

Share this article

https://doi.org/10.7554/eLife.61076

Further reading

    1. Evolutionary Biology
    Deng Wang, Yaqin Qiang ... Jian Han
    Research Article

    Extant ecdysozoans (moulting animals) are represented by a great variety of soft-bodied or articulated organisms that may or may not have appendages. However, controversies remain about the vermiform nature (i.e. elongated and tubular) of their ancestral body plan. We describe here Beretella spinosa gen. et sp. nov. a tiny (maximal length 3 mm) ecdysozoan from the lowermost Cambrian, Yanjiahe Formation, South China, characterized by an unusual sack-like appearance, single opening, and spiny ornament. Beretella spinosa gen. et sp. nov has no equivalent among animals, except Saccorhytus coronarius, also from the basal Cambrian. Phylogenetic analyses resolve both fossil species as a sister group (Saccorhytida) to all known Ecdysozoa, thus suggesting that ancestral ecdysozoans may have been non-vermiform animals. Saccorhytids are likely to represent an early off-shot along the stem-line Ecdysozoa. Although it became extinct during the Cambrian, this animal lineage provides precious insight into the early evolution of Ecdysozoa and the nature of the earliest representatives of the group.

    1. Biochemistry and Chemical Biology
    2. Evolutionary Biology
    Foteini Karapanagioti, Úlfur Águst Atlason ... Sebastian Obermaier
    Research Article

    The emergence of new protein functions is crucial for the evolution of organisms. This process has been extensively researched for soluble enzymes, but it is largely unexplored for membrane transporters, even though the ability to acquire new nutrients from a changing environment requires evolvability of transport functions. Here, we demonstrate the importance of environmental pressure in obtaining a new activity or altering a promiscuous activity in members of the amino acid-polyamine-organocation (APC)-type yeast amino acid transporters family. We identify APC members that have broader substrate spectra than previously described. Using in vivo experimental evolution, we evolve two of these transporter genes, AGP1 and PUT4, toward new substrate specificities. Single mutations on these transporters are found to be sufficient for expanding the substrate range of the proteins, while retaining the capacity to transport all original substrates. Nonetheless, each adaptive mutation comes with a distinct effect on the fitness for each of the original substrates, illustrating a trade-off between the ancestral and evolved functions. Collectively, our findings reveal how substrate-adaptive mutations in membrane transporters contribute to fitness and provide insights into how organisms can use transporter evolution to explore new ecological niches.