The rise and fall of the ancient northern pike master sex determining gene

  1. Qiaowei Pan
  2. Romain Feron
  3. Elodie Jouanno
  4. Hugo Darras
  5. Amaury Herpin
  6. Ben Koop
  7. Eric Rondeau
  8. Frederick W Goetz
  9. Wesley A Larson
  10. Louis Bernatchez
  11. Mike Tringali
  12. Stephen S Curran
  13. Eric Saillant
  14. Gael PJ Denys
  15. Frank A von Hippel
  16. Songlin Chen
  17. J Andrés López
  18. Hugo Verreycken
  19. Konrad Ocalewicz
  20. Rene Guyomard
  21. Camille Eche
  22. Jerome Lluch
  23. Celine Roques
  24. Hongxia Hu
  25. Roger Tabor
  26. Patrick DeHaan
  27. Krista M Nichols
  28. Laurent Journot
  29. Hugues Parrinello
  30. Christophe Klopp
  31. Elena A Interesova
  32. Vladimir Trifonov
  33. Manfred Schartl
  34. John H Postlethwait
  35. Yann Guiguen  Is a corresponding author
  1. INRAE, France
  2. French National Institute for Agricultural Research, France
  3. University of Lausanne, Switzerland
  4. University of Victoria, Canada
  5. NOAA, United States
  6. 6.Fisheries Aquatic Science and Technology Laboratory at Alaska Pacific University, United States
  7. University Laval, Canada
  8. Fish and Wildlife Conservation Commission, United States
  9. Auburn University, United States
  10. The University of Southern Mississippi, United States
  11. Muséum national d'Histoire naturelle, France
  12. Northern Arizona University, United States
  13. Yellow Sea Fisheries Research Institute, China
  14. College of Fisheries and Ocean Sciences Fisheries, United States
  15. Research Institute for Nature and Forest (INBO), Belgium
  16. University of Gdansk, Poland
  17. Beijing Fisheries Research Institute, China
  18. U S Fish and Wildlife Service, United States
  19. National Oceanic and Atmospheric Administration, United States
  20. CNRS, INSERM, France
  21. Institut de Génomique Fonctionnelle, France
  22. Tomsk State University, Russian Federation
  23. Novosibirsk State University, Russian Federation
  24. University of Würzburg, Germany
  25. University of Oregon, United States

Abstract

The understanding of the evolution of variable sex determination mechanisms across taxa requires comparative studies among closely related species. Following the fate of a known master sex-determining gene, we traced the evolution of sex determination in an entire teleost order (Esociformes). We discovered that the northern pike (Esox lucius) master sex-determining gene originated from a 65 to 90 million-year-old gene duplication event and that it remained sex-linked on undifferentiated sex chromosomes for at least 56 million years in multiple species. We identified several independent species- or population-specific sex determination transitions, including a recent loss of a Y-chromosome. These findings highlight the diversity of evolutionary fates of master sex-determining genes and the importance of population demographic history in sex determination studies. We hypothesize that occasional sex reversals and genetic bottlenecks provide a non-adaptive explanation for sex determination transitions.

Data availability

All gene sequences, genomic, Pool-seq and RAD-Seq reads were deposited under the common project number PRJNA634624.

The following data sets were generated
The following previously published data sets were used

Article and author information

Author details

  1. Qiaowei Pan

    PHASE (Animal Phyiology and breeding systems), INRAE, Rennes, France
    Competing interests
    The authors declare that no competing interests exist.
  2. Romain Feron

    PHASE (Animal Phyiology and breeding systems), INRAE, Rennes, France
    Competing interests
    The authors declare that no competing interests exist.
  3. Elodie Jouanno

    PHASE, French National Institute for Agricultural Research, Rennes, France
    Competing interests
    The authors declare that no competing interests exist.
  4. Hugo Darras

    Department of Ecology and Evolution,, University of Lausanne, Lausanne, Switzerland
    Competing interests
    The authors declare that no competing interests exist.
  5. Amaury Herpin

    PHASE (Animal Phyiology and breeding systems), INRAE, Rennes, France
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-0630-4027
  6. Ben Koop

    Department of Biology, Centre for Biomedical Research, University of Victoria, Victoria, Canada
    Competing interests
    The authors declare that no competing interests exist.
  7. Eric Rondeau

    Department of Biology, Centre for Biomedical Research, University of Victoria, Victoria, Canada
    Competing interests
    The authors declare that no competing interests exist.
  8. Frederick W Goetz

    Environmental and Fisheries Sciences Division, NOAA, Seattle, United States
    Competing interests
    The authors declare that no competing interests exist.
  9. Wesley A Larson

    6.Fisheries Aquatic Science and Technology Laboratory at Alaska Pacific University, Anchorage, United States
    Competing interests
    The authors declare that no competing interests exist.
  10. Louis Bernatchez

    7.Institut de Biologie Intégrative et des Systèmes (IBIS), University Laval, Québec, Canada
    Competing interests
    The authors declare that no competing interests exist.
  11. Mike Tringali

    Florida Marine Research Institute, Fish and Wildlife Conservation Commission, St. Petersburg, United States
    Competing interests
    The authors declare that no competing interests exist.
  12. Stephen S Curran

    School of Fisheries and Aquatic Sciences, Auburn University, Auburn, United States
    Competing interests
    The authors declare that no competing interests exist.
  13. Eric Saillant

    Gulf Coast Research Laboratory, The University of Southern Mississippi, Ocean Springs, United States
    Competing interests
    The authors declare that no competing interests exist.
  14. Gael PJ Denys

    Unité Mixte de Service Patrimoine Naturelle, Muséum national d'Histoire naturelle, Paris, France
    Competing interests
    The authors declare that no competing interests exist.
  15. Frank A von Hippel

    Department of Biological Sciences, Northern Arizona University, Flagstaff, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-9247-0231
  16. Songlin Chen

    Laboratory for Marine Fisheries Science and Food Production Processes, Yellow Sea Fisheries Research Institute, Qingdao, China
    Competing interests
    The authors declare that no competing interests exist.
  17. J Andrés López

    College of Fisheries and Ocean Sciences Fisheries, Fairbanks, United States
    Competing interests
    The authors declare that no competing interests exist.
  18. Hugo Verreycken

    Research Institute for Nature and Forest (INBO), Brussels, Belgium
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-2060-7005
  19. Konrad Ocalewicz

    Department of Marine Biology and Ecology, University of Gdansk, Gdansk, Poland
    Competing interests
    The authors declare that no competing interests exist.
  20. Rene Guyomard

    Animal genetics, INRAE, Jouy-en-Josas, France
    Competing interests
    The authors declare that no competing interests exist.
  21. Camille Eche

    Animal Genetics, INRAE, Toulouse, France
    Competing interests
    The authors declare that no competing interests exist.
  22. Jerome Lluch

    Animal Genetics, INRAE, Toulouse, France
    Competing interests
    The authors declare that no competing interests exist.
  23. Celine Roques

    Animal Genetics, INRAE, Toulouse, France
    Competing interests
    The authors declare that no competing interests exist.
  24. Hongxia Hu

    Beijing Key Laboratory of Fishery Biotechnology, Beijing Fisheries Research Institute, Beijing, China
    Competing interests
    The authors declare that no competing interests exist.
  25. Roger Tabor

    U S Fish and Wildlife Service, Lacey, United States
    Competing interests
    The authors declare that no competing interests exist.
  26. Patrick DeHaan

    U S Fish and Wildlife Service, Lacey, United States
    Competing interests
    The authors declare that no competing interests exist.
  27. Krista M Nichols

    Conservation Biology Division, Northwest Fisheries Science Center, National Oceanic and Atmospheric Administration, Seattle, United States
    Competing interests
    The authors declare that no competing interests exist.
  28. Laurent Journot

    Institut de Génomique Fonctionnelle, CNRS, INSERM, Montpellier, France
    Competing interests
    The authors declare that no competing interests exist.
  29. Hugues Parrinello

    MGX-Montpellier GenomiX, Institut de Génomique Fonctionnelle, Montpellier, France
    Competing interests
    The authors declare that no competing interests exist.
  30. Christophe Klopp

    MIAT, INRAE, Toulouse, France
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-7126-5477
  31. Elena A Interesova

    Tomsk State University, Tomsk, Russian Federation
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-1148-6283
  32. Vladimir Trifonov

    Institute of Molecular and Cellular Biology, Novosibirsk State University, Novosibirsk, Russian Federation
    Competing interests
    The authors declare that no competing interests exist.
  33. Manfred Schartl

    University of Würzburg, Würzburg, Germany
    Competing interests
    The authors declare that no competing interests exist.
  34. John H Postlethwait

    Institute of Neuroscience, University of Oregon, Eugene, United States
    Competing interests
    The authors declare that no competing interests exist.
  35. Yann Guiguen

    PHASE (Animal Phyiology and breeding systems), INRAE, Rennes, France
    For correspondence
    yann.guiguen@inrae.fr
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-5464-6219

Funding

Agence Nationale de la Recherche (ANR-13-ISV7-0005)

  • Yann Guiguen

Deutsche Forschungsgemeinschaft

  • Manfred Schartl

Agence Nationale de la Recherche (ANR-10-INBS-09)

  • Laurent Journot

Agence Nationale de la Recherche (ANR-10-INBS-09)

  • Celine Roques

National Institute of Health (R01GM085318)

  • John H Postlethwait

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

Reviewing Editor

  1. Molly Przeworski, Columbia University, United States

Version history

  1. Received: September 6, 2020
  2. Accepted: January 27, 2021
  3. Accepted Manuscript published: January 28, 2021 (version 1)
  4. Version of Record published: February 8, 2021 (version 2)

Copyright

© 2021, Pan 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. Qiaowei Pan
  2. Romain Feron
  3. Elodie Jouanno
  4. Hugo Darras
  5. Amaury Herpin
  6. Ben Koop
  7. Eric Rondeau
  8. Frederick W Goetz
  9. Wesley A Larson
  10. Louis Bernatchez
  11. Mike Tringali
  12. Stephen S Curran
  13. Eric Saillant
  14. Gael PJ Denys
  15. Frank A von Hippel
  16. Songlin Chen
  17. J Andrés López
  18. Hugo Verreycken
  19. Konrad Ocalewicz
  20. Rene Guyomard
  21. Camille Eche
  22. Jerome Lluch
  23. Celine Roques
  24. Hongxia Hu
  25. Roger Tabor
  26. Patrick DeHaan
  27. Krista M Nichols
  28. Laurent Journot
  29. Hugues Parrinello
  30. Christophe Klopp
  31. Elena A Interesova
  32. Vladimir Trifonov
  33. Manfred Schartl
  34. John H Postlethwait
  35. Yann Guiguen
(2021)
The rise and fall of the ancient northern pike master sex determining gene
eLife 10:e62858.
https://doi.org/10.7554/eLife.62858

Share this article

https://doi.org/10.7554/eLife.62858

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