Unraveling the genotype by environment interaction in a thermosensitive fish with a polygenic sex determination system

Type Article
Date 2021-12
Language English
Author(s) Geffroy BenjaminORCID1, Besson Mathieu2, 3, Sánchez-Baizán NúriaORCID4, Clota Frederic1, 3, Goikoetxea AlexanderORCID1, Sadoul Bastien1, 5, Ruelle Francois6, Blanc Marie-Odile6, Parrinello Hugues7, Hermet SophieORCID8, Blondeau-Bidet EvaORCID8, Pratlong Marine7, Piferrer FrancescORCID4, Vandeputte MarcORCID1, 3, Allal FrancoisORCID1
Affiliation(s) 1 : MARBEC Université de Montpellier, CNRS, Ifremer, IRD, Palavas-les-Flots, France
2 : SYSAAF, Station LPGP/INRAE, 35042 Rennes, France
3 : Université Paris-Saclay, INRAE, AgroParisTech, GABI, 78350, Jouy-en-Josas, France
4 : Institut de Ciències del Mar, Spanish National Research Council, Barcelona, Spain
5 : ESE, Ecology and Ecosystem Health, Institut Agro, INRAE, Rennes, France
6 : Laboratoire Service d'Expérimentations Aquacoles, Ifremer, Palavas-les-Flots, France
7 : MGX, BCM, Université de Montpellier, CNRS, INSERM, Montpellier, France
8 : MARBEC Université de Montpellier, CNRS, Ifremer, IRD, Montpellier, France
Source Proceedings Of The National Academy Of Sciences Of The United States Of America (0027-8424) (Proceedings of the National Academy of Sciences), 2021-12 , Vol. 118 , N. 50 , P. e2112660118 (12p.)
DOI 10.1073/pnas.2112660118
WOS© Times Cited 10
Keyword(s) sex determination, genomics, temperature, fish, epigenetic
Abstract

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.

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Appendix 27 3 MB Open access
Dataset S01 4 MB Open access
Dataset S02 30 KB Open access
Dataset S03 25 MB Open access
Dataset S04 16 MB Open access
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Geffroy Benjamin, Besson Mathieu, Sánchez-Baizán Núria, Clota Frederic, Goikoetxea Alexander, Sadoul Bastien, Ruelle Francois, Blanc Marie-Odile, Parrinello Hugues, Hermet Sophie, Blondeau-Bidet Eva, Pratlong Marine, Piferrer Francesc, Vandeputte Marc, Allal Francois (2021). Unraveling the genotype by environment interaction in a thermosensitive fish with a polygenic sex determination system. Proceedings Of The National Academy Of Sciences Of The United States Of America, 118(50), e2112660118 (12p.). Publisher's official version : https://doi.org/10.1073/pnas.2112660118 , Open Access version : https://archimer.ifremer.fr/doc/00740/85205/