GENOMIC PREDICTION AND GENOTYPE-BY-TEMPERATURE INTERACTION OF SEX TENDENCY IN EUROPEAN SEA BASS

Introduction

European sea bass (Dicentrarchus labrax) is an important European aquaculture species. Females, performing better than males with later maturation and larger size, are preferred. Unfortunately, in aquaculture conditions, the sex-ratio is typically biased towards males. Thus, deciphering the sex determinism system and finding routes for controlling the sex-ratio of this species has been a long-lasting challenge to support sea bass production and selective breeding programmes. 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 more balanced sex-ratios, and a high temperature masculinizing protocol (21°C, HT). We used genome-wide SNP genotypes to estimate the genetic parameters and genotype-by-temperature interaction of sex tendency in European sea bass.

Material and Methods

We produced 8 families by mating 8 males with a same female. The progenies were reared in common garden under two thermal treatment in triplicate: a LT (16°C) and a HT (21°C) temperature protocol. 1013 fish were sexed at one year and genotyped for 57k SNPs with the  DLabCHIP array (Griot et al., 2021). Pedigree was obtained using a subset of 1,000 highly polymorphic SNPs, using the R package APIS (Griot et al., 2020). After filtering SNPs with a call rate >0.90, a sufficient minor allele frequency (MAF>0.05) and no mendelian transmission errors, 39,607 polymorphic SNPs were retained to estimate genomic-based heritability, estimated sex tendency (with temperature as fixed effect) and the genetic correlation between treatments, with a threshold model using THRGIBBS1F90 (Tsuruta and Misztal, 2006). 

Results and Discussion

The proportion of females obtained was 53.4% at LT and 25.3% at HT. As expected, the high temperature induced a marked masculinization, producing half of the females than at LT treatment. Sex tendency at LT (sex_LT) and at HT (sex_HT) were estimated as highly heritable with h2sex_LT = 0.65±0.06 and h2sex_HT = 0.51±0.08. A strong genetic correlation between sex_LT and sex_HT was observed (rG = 0.91±0.09). The genomic-based estimation of the sex tendency of the animals is shown in Figure 1. Regarding the estimated sex tendency, as the combination of individual genetic sex tendency and the fixed effect of temperature, we observed that at LT, the mean sex tendency (0.12) is close to the theoretical threshold of zero (above which an animal is more likely to become a female). On the contrary, the distribution of the sex tendency estimated for animals at HT is typically displaced toward negative values with a mean at -0.89.

The lower heritability estimates for HT and the skewing of the estimated sex tendency toward negative values could result from the temperature-mediated impact on the sex at HT. At HT some phenotypically male fish can be considered as “reversed-females”, also known as “neomales”, confirming the hypothesis of a polygenic threshold model of sex determination.

These results confirm the high heritability of sex tendency in European sea bass, show the effect of larval rearing temperature on sex tendency is mostly additive (high genetic correlation between LT and HT), and highlight the efficiency of genomic-based mixed animal models to estimate breeding values for sex tendency in sea bass, with potential applications to identify sex-reversed “neomales” which would be of high interest to increase proportions of females in farmed populations of sea bass.

Acknowledgement

This work was partially supported by the 3S - Seabass Sex and Stress project (n° 4320175237) funded by the French Government and the European Union (EMFF, European Maritime and Fisheries Fund) at the “Appels à projets Innovants” managed by the France Agrimer Office, and the European Union’s 7th Framework Programme under Grant Agreement 652831 (AQUAEXCEL2020, Transnational Access project AE040073)

References

Griot R., Allal F., Brard‐Fudulea S., Morvezen R., Haffray P., Phocas F.,  Vandeputte M., 2020. APIS: an auto‐adaptive parentage inference software that tolerates missing parents. Mol. Ecol. Resour., 20, 579-590

Piferrer F., Blázquez M., Navarro L., González A., 2005. Genetic, Endocrine, and Environmental Components of Sex Determination and Differentiation in the European Sea Bass (Dicentrarchus Labrax L.). Gen. Comp. Endocrinol., 142, 102-110

Tsuruta S., Misztal I., 2006. THRGIBBS1F90 for estimation of variance components with threshold and linear models. Proc. 8th World Congr. Genet. Appl. Livest. Prod. Belo Horiz. Minas Gerais Braz. 13-18 August 2006, 27–31.

Vandeputte M., Dupont-Nivet M., Chavanne H., Chatain B., 2007. A Polygenic Hypothesis for Sex Determination in the European Sea Bass Dicentrarchus labrax. Genetics 176, 1049–1057.