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The Rise and Fall of the Ancient Northern Pike Master Sex Determining Gene

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The Rise and Fall of the Ancient Northern Pike Master Sex Determining Gene The University of Southern Mississippi The Aquila Digital Community Faculty Publications 1-1-2021 The Rise and Fall of the Ancient Northern Pike Master Sex Determining Gene Qiaowei Pan Laboratoire de Physiologie et Génomique des Poissons (LPGP) Romain Feron Laboratoire de Physiologie et Génomique des Poissons (LPGP) Elodie Jouanno Laboratoire de Physiologie et Génomique des Poissons (LPGP) Hugo Darras Université de Lausanne (UNIL) Amaury Herpin Laboratoire de Physiologie et Génomique des Poissons (LPGP) See next page for additional authors Follow this and additional works at: https://aquila.usm.edu/fac_pubs Recommended Citation Pan, Q., Feron, R., Jouanno, E., Darras, H., Herpin, A., Koop, B., Rondeau, E., Goetz, F., Larson, W., Bernatchez, L., Tringali, M., Curran, S., Saillant, E., Denys, G., von Hippel, F., Chen, S., López, J., Verreycken, H., Ocalewicz, K., Guyomard, R., Eche, C., Lluch, J., Roques, C., Hu, H., Tabor, R., Dehaan, P., Nichols, K., Journot, L., Parrinello, H., Klopp, C., Interesova, E., Trifonov, V., Schartl, M., Postlethwait, J., Guiguen, Y. (2021). The Rise and Fall of the Ancient Northern Pike Master Sex Determining Gene. eLife, 10, 1-50. Available at: https://aquila.usm.edu/fac_pubs/18981 This Article is brought to you for free and open access by The Aquila Digital Community. It has been accepted for inclusion in Faculty Publications by an authorized administrator of The Aquila Digital Community. For more information, please contact [email protected]. Authors 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 P.J. 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, and Yann Guiguen This article is available at The Aquila Digital Community: https://aquila.usm.edu/fac_pubs/18981 RESEARCH ARTICLE The rise and fall of the ancient northern pike master sex-determining gene Qiaowei Pan1,2, Romain Feron1,2,3, 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 Denys11,12, Frank A von Hippel13, Songlin Chen14, J Andre´ s Lo´ pez15, 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* 1INRAE, LPGP, Rennes, France; 2Department of Ecology and Evolution, University of Lausanne, Lausanne, Switzerland; 3Swiss Institute of Bioinformatics, Lausanne, Switzerland; 4Department of Biology, Centre for Biomedical Research, University of Victoria, Victoria, Canada; 5Environmental and Fisheries Sciences Division, Northwest Fisheries Science Center, National Marine Fisheries Service, NOAA, Seattle, United States; 6Fisheries Aquatic Science and Technology Laboratory at Alaska Pacific University, Anchorage, United States; 7Institut de Biologie Inte´grative et des Syste`mes (IBIS), Universite´ Laval, Que´bec, Canada; 8Fish and Wildlife Conservation Commission, Florida Marine Research Institute, St. Petersburg, United States; 9School of Fisheries and Aquatic Sciences, Auburn University, Auburn, United States; 10Gulf Coast Research Laboratory, School of Ocean Science and Technology, The University of Southern Mississippi, Ocean Springs, United States; 11Laboratoire de Biologie des organismes et e´cosyste`mes aquatiques (BOREA), MNHN, CNRS, IRD, SU, UCN, Laboratoire de Biologie des organismes et e´cosyste`mes aquatiques (BOREA), Paris, France; 12Unite´ Mixte de Service *For correspondence: Patrimoine Naturelle – Centre d’expertise et de donne´es (UMS 2006 AFB, CNRS, [email protected] MNHN), Muse´um national d’Histoire naturelle, Paris, France; 13Department of Competing interests: The Biological Sciences, Northern Arizona University, Flagstaff, United States; 14Yellow authors declare that no Sea Fisheries Research Institute, CAFS, Laboratory for Marine Fisheries Science and competing interests exist. Food Production Processes, Pilot National Laboratory for Marine Science and Funding: See page 16 Technology (Qingdao), Qingdao, China; 15College of Fisheries and Ocean Sciences 16 Received: 06 September 2020 Fisheries, Fairbanks, United States; Research Institute for Nature and Forest Accepted: 27 January 2021 (INBO), Brussels, Belgium; 17Department of Marine Biology and Ecology, Institute of Published: 28 January 2021 Oceanography, University of Gdansk, Gdansk, Poland; 18INRAE, GABI, Jouy-en- 19 20 Reviewing editor: Molly Josas, France; GeT-PlaGe, INRAE, Genotoul, Castanet-Tolosan, France; Beijing Przeworski, Columbia University, Fisheries Research Institute & Beijing Key Laboratory of Fishery Biotechnology, United States Beijing, China; 21U.S. Fish and Wildlife Service, Lacey, United States; 22Conservation Copyright Pan et al. This Biology Division, Northwest Fisheries Science Center, National Marine Fisheries article is distributed under the Service, National Oceanic and Atmospheric Administration, Seattle, United States; terms of the Creative Commons 23Institut de Ge´nomique Fonctionnelle, IGF, CNRS, INSERM, Univ. Montpellier, Attribution License, which 24 25 permits unrestricted use and Montpellier, France; INRAE, Sigenae, Genotoul Bioinfo, Toulouse, France; Tomsk 26 redistribution provided that the State University, Tomsk, Russian Federation; Institute of Molecular and Cellular original author and source are Biology, Siberian Branch of the Russian Academy of Sciences, Novosibirsk State credited. Pan et al. eLife 2021;10:e62858. DOI: https://doi.org/10.7554/eLife.62858 1 of 30 Research article Evolutionary Biology University, Novosibirsk, Russian Federation; 27University of Wuerzburg, Developmental Biochemistry, Biocenter, 97074 Wu¨ rzburg, Germany; and The Xiphophorus Genetic Stock Center, Texas State University, San Marcos, United States; 28Institute 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. Introduction Genetic sex determination (GSD) evolved independently and repeatedly in diverse taxa, including animals, plants, and fungi (Tree of Sex Consortium et al., 2014; Beukeboom and Perrin, 2014), but the stability of such systems varies drastically among groups. In mammals and birds, conserved male or female heterogametic sex determination (SD) systems have been maintained over a long evolutionary time with conserved master sex-determining (MSD) genes (Marshall Graves, 2008). In contrast, teleost fishes display both genetic and environmental sex determination (ESD), and a remarkable evolutionary lability driven by rapid turnovers of sex chromosomes and MSD genes (Kikuchi and Hamaguchi, 2013; Pan et al., 2017). These characteristics make teleosts an attractive group in which to study the evolution of SD systems. In the past two decades, the identity of a variety of MSD genes has been revealed in teleosts thanks to advances in sequencing technologies. These findings generated new hypotheses on how the birth of MSD genes through allelic diversification or duplication with or without translocation may drive sex chromosome turnover in vertebrates (Kikuchi and Hamaguchi, 2013; Pan et al., 2017). These teleost MSD genes also provided empirical support for the ‘limited option’ idea that states that certain genes known to be implicated in sex differentiation pathways are more likely to be recruited as new MSD genes (Marshall Graves and Peichel, 2010). The majority of these recently discovered MSD genes, however, were phylogenetically scattered, making it challenging to infer evolutionary patterns and conserved themes of sex chromosomes and/or MSD gene turnovers. Although comparative studies have been accomplished in medakas, poeciliids, tilapiine cichlids, sal- monids, and sticklebacks (Kikuchi and Hamaguchi, 2013), transitions of SD systems in relation to the fate of known MSD genes within closely related species have only been explored in medakas (Myosho et al., 2015) and salmonids (Guiguen et al., 2018). Esociformes is a small order of teleost fishes (Figure 1) that
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