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

Author

Pan Q, Feron R, Jouanno E, Darras H, Herpin A, Koop B, Rondeau E, Goetz FW, Larson WA, Bernatchez L, Tringali M, Curran SS, Saillant E, Denys GP, von Hippel FA, Chen S, López JA, Verreycken H, Ocalewicz K, Guyomard R, Eche C, Lluch J, Roques C, Hu H, Tabor R, DeHaan P, Nichols KM, Journot L, Parrinello H, Klopp C, Interesova EA, Trifonov V, Schartl M, Postlethwait J, and Guiguen Y

Subjects
Animals, Female, Male, Phylogeny, Esocidae genetics, Gene Duplication, Sex Chromosomes genetics, Sex Determination Processes physiology
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., Competing Interests: QP, RF, EJ, HD, AH, BK, ER, FG, WL, LB, MT, SC, ES, GD, Fv, SC, JL, HV, KO, RG, CE, JL, CR, HH, RT, PD, KN, LJ, HP, CK, EI, VT, MS, JP, YG No competing interests declared, (© 2021, Pan et al.)

Published
2021
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2. The rise and fall of the ancient northern pike master sex-determining gene

Author

Mike Tringali, Hongxia Hu, Amaury Herpin, Patrick W. DeHaan, Eric Rondeau, Louis Bernatchez, Wesley A. Larson, Manfred Schartl, Elodie Jouanno, E. A. Interesova, Yann Guiguen, Eric Saillant, Stephen S. Curran, Hugo Verreycken, Gaël P.J. Denys, Roger A. Tabor, Vladimir A. Trifonov, Hugo Darras, Christophe Klopp, Hugues Parrinello, Frederick W. Goetz, John H. Postlethwait, Qiaowei Pan, Céline Roques, J. Andrés López, Camille Eché, Jérôme Lluch, Laurent Journot, Frank A. von Hippel, Krista M. Nichols, Konrad Ocalewicz, Romain Feron, René Guyomard, Song-Lin Chen, Ben F. Koop, Laboratoire de Physiologie et Génomique des Poissons (LPGP), Structure Fédérative de Recherche en Biologie et Santé de Rennes ( Biosit : Biologie - Santé - Innovation Technologique )-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE), Department of Ecology and Evolution [Lausanne], Université de Lausanne (UNIL), Swiss Institute of Bioinformatics [Lausanne] (SIB), Department of Biology, University of Victoria, Northwest Fisheries Science Center (NWFSC), NOAA National Marine Fisheries Service (NMFS), National Oceanic and Atmospheric Administration (NOAA)-National Oceanic and Atmospheric Administration (NOAA), Alaska Pacific University, Institut de Biologie Intégrative et des Systèmes [Québec] (IBIS), Florida Marine Research Institute, Florida Fish and Wildlife Conservation Commission, School of Ocean Science and Technology [Mississippi] (SOST), University of Southern Mississippi (USM), Gulf Coast Research Laboratory, Biologie des Organismes et Ecosystèmes Aquatiques (BOREA), Centre National de la Recherche Scientifique (CNRS)-Université des Antilles (UA)-Muséum national d'Histoire naturelle (MNHN)-Institut de Recherche pour le Développement (IRD)-Sorbonne Université (SU)-Université de Caen Normandie (UNICAEN), Normandie Université (NU)-Normandie Université (NU), Patrimoine naturel (PatriNat), Muséum national d'Histoire naturelle (MNHN)-Centre National de la Recherche Scientifique (CNRS)-Office français de la biodiversité (OFB), Department of Biological Sciences [Flagstaff], Northern Arizona University [Flagstaff], Yellow Sea Fisheries Research Institute, Chinese Academy of Fishery Sciences, College of Fisheries and Ocean Sciences (CFOS), University of Alaska [Fairbanks] (UAF), Research Institute for Nature and Forest (INBO), Department of Marine Biology and Ecology, University of Gdansk, Génétique Animale et Biologie Intégrative (GABI), Université Paris-Saclay-AgroParisTech-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE), Génopole Toulouse Midi-Pyrénées [Auzeville] (GENOTOUL), Institut National des Sciences Appliquées - Toulouse (INSA Toulouse), Institut National des Sciences Appliquées (INSA)-Institut National des Sciences Appliquées (INSA)-Université Toulouse III - Paul Sabatier (UT3), Université Fédérale Toulouse Midi-Pyrénées-Université Fédérale Toulouse Midi-Pyrénées-Ecole Nationale Vétérinaire de Toulouse (ENVT), Institut National Polytechnique (Toulouse) (Toulouse INP), Université Fédérale Toulouse Midi-Pyrénées-Université Fédérale Toulouse Midi-Pyrénées-Institut National Polytechnique (Toulouse) (Toulouse INP), Université Fédérale Toulouse Midi-Pyrénées-Institut National de la Santé et de la Recherche Médicale (INSERM)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE), Beijing Fisheries Research Institute, U.S. Fish and Wildlife Service, Institut de Génomique Fonctionnelle (IGF), Université de Montpellier (UM)-Université Montpellier 1 (UM1)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Université Montpellier 2 - Sciences et Techniques (UM2)-Centre National de la Recherche Scientifique (CNRS), Système d'Information des GENomes des Animaux d'Elevage (SIGENAE), Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE), Tomsk State University [Tomsk], Siberian Branch of the Russian Academy of Sciences (SB RAS), Developmental Biochemistry, Biocenter, Julius-Maximilians-Universität Würzburg [Wurtzbourg, Allemagne] (JMU), Institute of Neuroscience, University of Oregon, Eugene, Oregon, University of Oregon [Eugene], This work was supported by the Agence Nationale de la Recherche, the Deutsche Forschungsgemeinschaft (ANR/DFG, PhyloSex project, 2014–2016, SCHA 408/10–1, to YG and MS), and the U.S. National Institutes of Health (R01GM085318 to JHP). The MGX and Get-Plage core sequencing facilities were supported by France Genomique National infrastructure, funded as part of the ‘Investissement d’avenir’ program managed by the Agence Nationale pour la Recherche (contract ANR-10-INBS-09)., ANR-13-ISV7-0005,PhyloSex,Evolution des déterminants majeurs du sexe chez les poissons.(2013), ANR-10-INBS-0009,France-Génomique,Organisation et montée en puissance d'une Infrastructure Nationale de Génomique(2010), Université de Lausanne = University of Lausanne (UNIL), Université de Caen Normandie (UNICAEN), Normandie Université (NU)-Normandie Université (NU)-Muséum national d'Histoire naturelle (MNHN)-Institut de Recherche pour le Développement (IRD)-Sorbonne Université (SU)-Centre National de la Recherche Scientifique (CNRS)-Université des Antilles (UA), AgroParisTech-Université Paris-Saclay-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE), Université Toulouse III - Paul Sabatier (UT3), Institut National de la Santé et de la Recherche Médicale (INSERM)-Université de Montpellier (UM)-Centre National de la Recherche Scientifique (CNRS), University of Victoria [Canada] (UVIC), Qingdao National Laboratory for Marine Science and Technology, University of Gdańsk (UG), Université de Toulouse (UT)-Université de Toulouse (UT)-Ecole Nationale Vétérinaire de Toulouse (ENVT), Université de Toulouse (UT)-Université de Toulouse (UT)-Institut National Polytechnique (Toulouse) (Toulouse INP), Université de Toulouse (UT)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE), Texas State University, Agence Nationale de la Recherche, Deutsche Forschungsgemeinschaft (ANR/DFG, PhyloSex project, 2014–2016, SCHA 408/10–1, to YG and MS), U.S. National Institutes of Health (R01GM085318 to JHP), France Genomique National infrastructure, funded as part of the ‘Investissement d’avenir’ program managed by the Agence Nationale pour la Recherche (contract ANR-10-INBS-09), Julius-Maximilians-Universität Würzburg (JMU), Corvaisier, Maryse, Blanc – Accords bilatéraux 2013 - Evolution des déterminants majeurs du sexe chez les poissons. - - PhyloSex2013 - ANR-13-ISV7-0005 - Blanc – Accords bilatéraux 2013 - VALID, Organisation et montée en puissance d'une Infrastructure Nationale de Génomique - - France-Génomique2010 - ANR-10-INBS-0009 - INBS - VALID, and Przeworski, Molly (ed.)

Subjects
Male, 0106 biological sciences, 0301 basic medicine, Evolution of sexual reproduction, Lineage (evolution), [SDV]Life Sciences [q-bio], sex determination, 01 natural sciences, mudminnows, Gene Duplication, Gene duplication, Biology (General), Clade, master sex determining gene, Phylogeny, северная щука, computer.programming_language, гены, определяющие пол, 0303 health sciences, education.field_of_study, Sex Chromosomes, biology, umbridae, General Neuroscience, General Medicine, [SDV] Life Sciences [q-bio], Medicine, Female, Research Article, QH301-705.5, Demographic history, Science, Population, esocidae, Y chromosome, 010603 evolutionary biology, General Biochemistry, Genetics and Molecular Biology, 03 medical and health sciences, Animals, education, Esox, pikes, 030304 developmental biology, Pike, fish, General Immunology and Microbiology, evolutionary biology, Sex Determination Processes, biology.organism_classification, esociforms, Sexual reproduction, 030104 developmental biology, Evolutionary biology, Other, [SDE.BE]Environmental Sciences/Biodiversity and Ecology, computer, Sex linkage
Abstract

Sexual reproduction is a ubiquitous basic feature of life and genetic sex determination is thus widespread, at least among eukaryotes. Understanding the remarkable diversity of sex determination mechanisms, however, is limited by the paucity of empirical studies. Here, we traced back the evolution of sex determination in an entire clade of vertebrates and uncovered that the northern pike (Esox lucius) master sex-determining gene initiated from a 65 to 90 million-year-old gene duplication and remained sex-linked on undifferentiated sex chromosomes for at least 56 million years. Contrasting with its ancient origin, we identified several independent species- or population-specific transitions of sex determination mechanisms in this lineage, including an unexpected complete and recent Y-chromosome loss in some North American northern pike populations. These findings highlight the diversity of the evolutionary fates of master sex-determining genes and raise the importance of careful considerations of population demographic history in sex determination studies. Our study also puts forward the hypothesis that occasional sex reversals and genetic bottlenecks provide a non-adaptive explanation for sex determination transitions.

Published
2020

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