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

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)

Peer reviewed