1. Unraveling the genotype by environment interaction in a thermosensitive fish with a polygenic sex determination system
- Author
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Benjamin Geffroy, Mathieu Besson, Núria Sánchez-Baizán, Frederic Clota, Alexander Goikoetxea, Bastien Sadoul, François Ruelle, Marie-Odile Blanc, Hugues Parrinello, Sophie Hermet, Eva Blondeau-Bidet, Marine Pratlong, Francesc Piferrer, Marc Vandeputte, François Allal, MARine Biodiversity Exploitation and Conservation (UMR MARBEC), Centre National de la Recherche Scientifique (CNRS)-Université de Montpellier (UM)-Institut Français de Recherche pour l'Exploitation de la Mer (IFREMER)-Institut de Recherche pour le Développement (IRD), Syndicat des Sélectionneurs Avicoles et Aquacoles Français (SYSAAF), Institute of Marine Sciences / Institut de Ciències del Mar [Barcelona] (ICM), Consejo Superior de Investigaciones Científicas [Madrid] (CSIC), 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), Université de Montpellier (UM), Institut de Génomique Fonctionnelle - Montpellier GenomiX (IGF MGX), 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)-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), Génétique Animale et Biologie Intégrative (GABI), Université Paris-Saclay-AgroParisTech-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE), European Maritime and Fisheries Fund, Ministerio de Ciencia, Innovación y Universidades (España), and Agencia Estatal de Investigación (España)
- Subjects
Male ,0106 biological sciences ,Multifactorial Inheritance ,Genotype ,sex determination ,[SDV.SA.ZOO]Life Sciences [q-bio]/Agricultural sciences/Zootechny ,010603 evolutionary biology ,01 natural sciences ,Histones ,03 medical and health sciences ,genomics ,Animals ,Body Size ,14. Life underwater ,Gonads ,SOX Transcription Factors ,030304 developmental biology ,fish ,0303 health sciences ,Temperatures ,Multidisciplinary ,Temperature ,Reproducibility of Results ,temperature ,Epigenetic ,Genomics ,DNA Methylation ,Sex Determination Processes ,Biological Sciences ,Sex determination ,[SDV.GEN.GA]Life Sciences [q-bio]/Genetics/Animal genetics ,Fish ,Gene Expression Regulation ,[SDV.SA.SPA]Life Sciences [q-bio]/Agricultural sciences/Animal production studies ,[SDV.SA.STP]Life Sciences [q-bio]/Agricultural sciences/Sciences and technics of fishery ,Bass ,Female ,Energy Metabolism ,epigenetic ,Body Temperature Regulation - Abstract
12 pages, 6 figures, supporting information online at https://www.pnas.org/lookup/suppl/doi:10.1073/pnas.2112660118/-/DCSupplemental.-- Data Availability: RNA-Seq and .xls tables data have been deposited in a publicly accessible database: SEXTAN (https://sextant.ifremer.fr/record/5cb1485f-385e-46e9-9cc1-4b4d77802183/). All other study data are included in the article and/or supporting information, In most animals, sex determination occurs at conception, when sex chromosomes are segregated following Mendelian laws. However, in multiple reptiles and fishes, this genetic sex can be overridden by external factors after fertilization or birth. In some species, the genetic sex may also be governed by multiple genes, further limiting our understanding of sex determination in such species. We used the European sea bass (Dicentrarchus labrax) as a model and combined genomic (using a single nucleotide polymorphism chip) and transcriptomic (RNA-Sequencing) approaches to thoroughly depict this polygenic sex determination system and its interaction with temperature. We estimated genetic sex tendency (eGST), defined as the estimated genetic liability to become a given sex under a liability threshold model for sex determination, which accurately predicts the future phenotypic sex. We found evidence that energetic pathways, concerning the regulation of lipids and glucose, are involved in sex determination and could explain why females tend to exhibit higher energy levels and improved growth compared to males. Besides, early exposure to high-temperature up-regulated sox3, followed by sox9a in individuals with intermediate eGST, but not in individuals showing highly female-biased eGST, providing the most parsimonious explanation for temperature-induced masculinization. This gonadal state was maintained likely by DNA methylation and the up-regulation of several genes involved in histone modifications, including jmjd1c. Overall, we describe a sex determination system resulting from continuous genetic and environmental influences in an animal. Our results provide significant progress in our understanding of the mechanisms underlying temperature-induced masculinization in fish, The study was supported by the European Maritime and Fisheries Fund (3S, Seabass Sex and Stress, Grant No. 4320175237) allocated to B.G. Production of the fish benefited from AQUAEXCEL2020 Transnational access grant “Transsexbass” to F.P. and M.V. Research at the F.P. laboratory was supported by Spanish Ministry of Science Grant No. PID2019-108888RB-I00., With the institutional support of the ‘Severo Ochoa Centre of Excellence’ accreditation (CEX2019-000928-S)
- Published
- 2021
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