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

doi:10.7554/eLife.62858

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

Elife. 2021 Jan 28:10:e62858. doi: 10.7554/eLife.62858.

Authors

Qiaowei Pan^{1

2}, Romain Feron^{1

2

3}, Elodie Jouanno¹, Hugo Darras², Amaury Herpin¹, Ben Koop⁴, Eric Rondeau⁴, Frederick W Goetz⁵, Wesley A Larson⁶, Louis Bernatchez⁷, Mike Tringali⁸, Stephen S Curran⁹, Eric Saillant¹⁰, Gael Pj Denys^{11

12}, Frank A von Hippel¹³, Songlin Chen¹⁴, J Andrés López¹⁵, Hugo Verreycken¹⁶, Konrad Ocalewicz¹⁷, Rene Guyomard¹⁸, Camille Eche¹⁹, Jerome Lluch¹⁹, Celine Roques¹⁹, Hongxia Hu²⁰, Roger Tabor²¹, Patrick DeHaan²¹, Krista M Nichols²², Laurent Journot²³, Hugues Parrinello²³, Christophe Klopp²⁴, Elena A Interesova²⁵, Vladimir Trifonov²⁶, Manfred Schartl²⁷, John Postlethwait²⁸, Yann Guiguen¹

Affiliations

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.

Keywords: esocidae; esociforms; evolutionary biology; fish; master sex determining gene; mudminnows; pikes; sex determination; umbridae.

Publication types

Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't

MeSH terms

Animals
Esocidae / genetics*
Female
Gene Duplication*
Male
Phylogeny
Sex Chromosomes / genetics*
Sex Determination Processes / physiology*

Abstract

Publication types

MeSH terms

Grants and funding