eLife (Jan 2021)
The rise and fall of the ancient northern pike master sex-determining gene
- Qiaowei Pan,
- Romain Feron,
- Elodie Jouanno,
- Hugo Darras,
- Amaury Herpin,
- Ben Koop,
- Eric Rondeau,
- Frederick W Goetz,
- Wesley A Larson,
- Louis Bernatchez,
- Mike Tringali,
- Stephen S Curran,
- Eric Saillant,
- Gael PJ Denys,
- Frank A von Hippel,
- Songlin Chen,
- J Andrés López,
- Hugo Verreycken,
- Konrad Ocalewicz,
- Rene Guyomard,
- Camille Eche,
- Jerome Lluch,
- Celine Roques,
- Hongxia Hu,
- Roger Tabor,
- Patrick DeHaan,
- Krista M Nichols,
- Laurent Journot,
- Hugues Parrinello,
- Christophe Klopp,
- Elena A Interesova,
- Vladimir Trifonov,
- Manfred Schartl,
- John Postlethwait,
- Yann Guiguen
Affiliations
- Qiaowei Pan
- ORCiD
- INRAE, LPGP, Rennes, France; Department of Ecology and Evolution, University of Lausanne, Lausanne, Switzerland
- Romain Feron
- INRAE, LPGP, Rennes, France; Department of Ecology and Evolution, University of Lausanne, Lausanne, Switzerland; Swiss Institute of Bioinformatics, Lausanne, Switzerland
- Elodie Jouanno
- INRAE, LPGP, Rennes, France
- Hugo Darras
- Department of Ecology and Evolution, University of Lausanne, Lausanne, Switzerland
- Amaury Herpin
- ORCiD
- INRAE, LPGP, Rennes, France
- Ben Koop
- Department of Biology, Centre for Biomedical Research, University of Victoria, Victoria, Canada
- Eric Rondeau
- Department of Biology, Centre for Biomedical Research, University of Victoria, Victoria, Canada
- Frederick W Goetz
- Environmental and Fisheries Sciences Division, Northwest Fisheries Science Center, National Marine Fisheries Service, NOAA, Seattle, United States
- Wesley A Larson
- Fisheries Aquatic Science and Technology Laboratory at Alaska Pacific University, Anchorage, United States
- Louis Bernatchez
- Institut de Biologie Intégrative et des Systèmes (IBIS), Université Laval, Québec, Canada
- Mike Tringali
- Fish and Wildlife Conservation Commission, Florida Marine Research Institute, St. Petersburg, United States
- Stephen S Curran
- School of Fisheries and Aquatic Sciences, Auburn University, Auburn, United States
- Eric Saillant
- Gulf Coast Research Laboratory, School of Ocean Science and Technology, The University of Southern Mississippi, Ocean Springs, United States
- Gael PJ Denys
- 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; Unité Mixte de Service Patrimoine Naturelle – Centre d’expertise et de données (UMS 2006 AFB, CNRS, MNHN), Muséum national d’Histoire naturelle, Paris, France
- Frank A von Hippel
- ORCiD
- Department of Biological Sciences, Northern Arizona University, Flagstaff, United States
- Songlin Chen
- 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
- J Andrés López
- College of Fisheries and Ocean Sciences Fisheries, Fairbanks, United States
- Hugo Verreycken
- ORCiD
- Research Institute for Nature and Forest (INBO), Brussels, Belgium
- Konrad Ocalewicz
- Department of Marine Biology and Ecology, Institute of Oceanography, University of Gdansk, Gdansk, Poland
- Rene Guyomard
- INRAE, GABI, Jouy-en-Josas, France
- Camille Eche
- GeT‐PlaGe, INRAE, Genotoul, Castanet-Tolosan, France
- Jerome Lluch
- GeT‐PlaGe, INRAE, Genotoul, Castanet-Tolosan, France
- Celine Roques
- GeT‐PlaGe, INRAE, Genotoul, Castanet-Tolosan, France
- Hongxia Hu
- Beijing Fisheries Research Institute & Beijing Key Laboratory of Fishery Biotechnology, Beijing, China
- Roger Tabor
- U.S. Fish and Wildlife Service, Lacey, United States
- Patrick DeHaan
- U.S. Fish and Wildlife Service, Lacey, United States
- Krista M Nichols
- Conservation Biology Division, Northwest Fisheries Science Center, National Marine Fisheries Service, National Oceanic and Atmospheric Administration, Seattle, United States
- Laurent Journot
- Institut de Génomique Fonctionnelle, IGF, CNRS, INSERM, Univ. Montpellier, Montpellier, France
- Hugues Parrinello
- Institut de Génomique Fonctionnelle, IGF, CNRS, INSERM, Univ. Montpellier, Montpellier, France
- Christophe Klopp
- ORCiD
- INRAE, Sigenae, Genotoul Bioinfo, Toulouse, France
- Elena A Interesova
- ORCiD
- Tomsk State University, Tomsk, Russian Federation
- Vladimir Trifonov
- Institute of Molecular and Cellular Biology, Siberian Branch of the Russian Academy of Sciences, Novosibirsk State University, Novosibirsk, Russian Federation
- Manfred Schartl
- University of Wuerzburg, Developmental Biochemistry, Biocenter, 97074 Würzburg, Germany; and The Xiphophorus Genetic Stock Center, Texas State University, San Marcos, United States
- John Postlethwait
- Institute of Neuroscience, University of Oregon, Eugene, United States
- Yann Guiguen
- ORCiD
- INRAE, LPGP, Rennes, France
- DOI
- https://doi.org/10.7554/eLife.62858
- Journal volume & issue
-
Vol. 10
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.
Keywords