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

Author:

Pan Qiaowei12ORCID,Feron Romain123,Jouanno Elodie1,Darras Hugo2,Herpin Amaury1ORCID,Koop Ben4,Rondeau Eric4,Goetz Frederick W5,Larson Wesley A6,Bernatchez Louis7,Tringali Mike8,Curran Stephen S9,Saillant Eric10,Denys Gael PJ1112,von Hippel Frank A13ORCID,Chen Songlin14,López J Andrés15,Verreycken Hugo16ORCID,Ocalewicz Konrad17,Guyomard Rene18,Eche Camille19,Lluch Jerome19,Roques Celine19,Hu Hongxia20,Tabor Roger21,DeHaan Patrick21,Nichols Krista M22,Journot Laurent23,Parrinello Hugues23,Klopp Christophe24ORCID,Interesova Elena A25ORCID,Trifonov Vladimir26,Schartl Manfred27,Postlethwait John28,Guiguen Yann1ORCID

Affiliation:

1. INRAE, LPGP, Rennes, France

2. Department of Ecology and Evolution, University of Lausanne, Lausanne, Switzerland

3. Swiss Institute of Bioinformatics, Lausanne, Switzerland

4. Department of Biology, Centre for Biomedical Research, University of Victoria, Victoria, Canada

5. Environmental and Fisheries Sciences Division, Northwest Fisheries Science Center, National Marine Fisheries Service, NOAA, Seattle, United States

6. Fisheries Aquatic Science and Technology Laboratory at Alaska Pacific University, Anchorage, United States

7. Institut de Biologie Intégrative et des Systèmes (IBIS), Université Laval, Québec, Canada

8. Fish and Wildlife Conservation Commission, Florida Marine Research Institute, St. Petersburg, United States

9. School of Fisheries and Aquatic Sciences, Auburn University, Auburn, United States

10. Gulf Coast Research Laboratory, School of Ocean Science and Technology, The University of Southern Mississippi, Ocean Springs, United States

11. Laboratoire de Biologie des organismes et écosystèmes aquatiques (BOREA), MNHN, CNRS, IRD, SU, UCN, Laboratoire de Biologie des organismes et écosystèmes aquatiques (BOREA), Paris, France

12. Unité Mixte de Service Patrimoine Naturelle – Centre d’expertise et de données (UMS 2006 AFB, CNRS, MNHN), Muséum national d’Histoire naturelle, Paris, France

13. Department of Biological Sciences, Northern Arizona University, Flagstaff, United States

14. Yellow Sea Fisheries Research Institute, CAFS, Laboratory for Marine Fisheries Science and Food Production Processes, Pilot National Laboratory for Marine Science and Technology (Qingdao), Qingdao, China

15. College of Fisheries and Ocean Sciences Fisheries, Fairbanks, United States

16. Research Institute for Nature and Forest (INBO), Brussels, Belgium

17. Department of Marine Biology and Ecology, Institute of Oceanography, University of Gdansk, Gdansk, Poland

18. INRAE, GABI, Jouy-en-Josas, France

19. GeT‐PlaGe, INRAE, Genotoul, Castanet-Tolosan, France

20. Beijing Fisheries Research Institute & Beijing Key Laboratory of Fishery Biotechnology, Beijing, China

21. U.S. Fish and Wildlife Service, Lacey, United States

22. Conservation Biology Division, Northwest Fisheries Science Center, National Marine Fisheries Service, National Oceanic and Atmospheric Administration, Seattle, United States

23. Institut de Génomique Fonctionnelle, IGF, CNRS, INSERM, Univ. Montpellier, Montpellier, France

24. INRAE, Sigenae, Genotoul Bioinfo, Toulouse, France

25. Tomsk State University, Tomsk, Russian Federation

26. Institute of Molecular and Cellular Biology, Siberian Branch of the Russian Academy of Sciences, Novosibirsk State University, Novosibirsk, Russian Federation

27. University of Wuerzburg, Developmental Biochemistry, Biocenter, 97074 Würzburg, Germany; and The Xiphophorus Genetic Stock Center, Texas State University, San Marcos, United States

28. Institute of Neuroscience, University of Oregon, Eugene, 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.

Funder

Agence Nationale de la Recherche

Deutsche Forschungsgemeinschaft

Korea National Institute of Health

ANR

Publisher

eLife Sciences Publications, Ltd

Subject

General Immunology and Microbiology,General Biochemistry, Genetics and Molecular Biology,General Medicine,General Neuroscience

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