Combined genomic approached to unravel sex determination in the European Sea Bass

Fish sex determination is often considered as governed by either genetic or environmental factors, but the European sea bass (Dicentrarchus labrax) defies this theory. In this species, a polygenic threshold sex determination system was demonstrated (Vandeputte et al. 2007), where the genetic sex tendency is influenced by larval rearing temperature to determine the phenotypic sex (Piferrer et al, 2005). In this study, we applied two thermal treatments during early larval stage, a low temperature protocol (16°C, LT), known to favour balanced sex-ratios and a high temperature masculinizing protocol (21°C, HT). We combined various “-omics” approaches to characterize this temperature-dependent polygenic sex determination of European sea bass. We produced 8 families by mating 8 males with the same female. The progenies were reared in common garden under two thermal treatments (LT, HT) in triplicate. Fish at four different key developmental stages encompassing the temperature sensitive period were sampled. We predicted the genetic sex tendency (eGST) of the animals using a genomic relationship matrix derived from 57K SNPs from the DLabCHIP array (Griot et al., 2021) with a threshold animal model. This was completed by a transcriptomic approach, whole-body energy measurements. The proportion of females was 53.4% at LT and 25.3% at HT, showing a marked masculinization at high temperature. We found that the eGST accurately predicted the future phenotypic sex. We provided 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. Overall, we describe for the first time a sex determination system resulting from continuous genetic and environmental influences in an animal, which provides significant progress in our understanding of the mechanisms underlying temperature-induced masculinization in fish