A Polygenic Hypothesis for Sex Determination in the European Sea Bass Dicentrarchus labrax

Abstract

Polygenic sex determination, although suspected in several species, is thought to be evolutionarily unstable and has been proven in very few cases. In the European sea bass, temperature is known to influence the sex ratio. We set up a factorial mating, producing 5.893 individuals from 253 full-sib families, all reared in a single batch to avoid any between-families environmental effects. The proportion of females in the offspring was 18.3%, with a large variation between families. Interpreting sex as a threshold trait, the heritability estimate was 0.62 6 0.12. The observed distribution of family sex ratios was in accordance with a polygenic model or with a four-sex-factors system with environmental variance and could not be explained by any genetic model without environmental variance. We showed that there was a positive genetic correlation between weight and sex (r A ¼ 0.50 6 0.09), apart from the phenotypic sex dimorphism in favor of females. This supports the hypothesis that a minimum size is required for sea bass juveniles to differentiate as females. An evolution of sex ratio by frequency-dependent selection is expected during the domestication process of Dicentrarchus labrax populations, raising concern about the release of such fish in the wild.

Metapopulation patterns of additive and nonadditive genetic variance in the sea bass (Dicentrarchus labrax)

“…Together with correlations between early survival, early growth, and observed proportions of females, this reflects a pleiotropic effect among traits, a pattern commonly assessed in cultured plants (e.g., Frascaroli et al., 2007; Fu et al., 2009). A positive genetic correlation between growth rate and a trend in expressing the female sex has been demonstrated earlier for the NAT population (Vandeputte et al., 2007), also supporting a pleiotropic effect on sex and growth in sea bass.…”

“…In the sea bass, it was previously shown that sex ratio was mostly additive at the family level in a North Atlantic population and could be considered a polygenic threshold trait (Vandeputte et al., 2007). Theory predicts that polygenic sex ratio is evolutionarily unstable (Bulmer & Bull, 1982; Van Dooren & Leimar, 2003) and should evolve toward either genetic sex determination with major sex factors or environmental sex determination.…”

“…Therefore, full‐sib families of sea bass grew in a common environment until 111 dpf in order to minimize early‐life genotype‐by‐environment (G×E) interactions. The range of rearing temperatures used until 111 dpf is known to produce an excess of male sea bass (reviewed in Piferrer, Blázquez, Navarro, & González, 2005), certainly due to interactions between genetic, environmental, and epigenetic factors occurring during early development (Navarro‐Martín et al., 2011; Vandeputte, Dupont‐Nivet, Chavanne, & Chatain, 2007). The fish remaining in Portugal were transferred to a 78 m 3 tank with natural temperature at 127 dpf ( N  =   105,767; 9.7% survival).…”

Sex determination in dioecious Mercurialis annua and its close diploid and polyploid relatives

“…Multi-locus systems of s.d. are known from several animal species, including the swordtail fish Xiphophorus helleri (Woolcock et al, 2006), the European sea bass Dicentrarchus labrax (Vandeputte et al, 2007) and the housefly Musca domestica (Dubendorfer et al, 2002;Kozielska et al, 2006), but M. annua is cited as the only plant species known to display such a system (Dellaporta and Calderonurrea, 1993;Grant et al, 1994;Ainsworth, 2000;Janousek and Mrackova, 2010). The discovery of the single sexlinked SCAR marker OPB01-1562 (that is, a Sequence Characterized Amplified Region of 1562 bp in length) in dioecious M. annua (Khadka et al, 2002), which was found in all males tested but not in females, casts doubt on the three-locus model.…”

Identification of the Major Sex-Determining Region of Turbot (Scophthalmus maximus)

“…Both genetic (GSD) and environmental sex determination has been reported in this group (Devlin and Nagahama 2002;Penman and Piferrer 2008), although primary sex determination is genetic in most species (Valenzuela et al 2003). Among GSD, single, multiple, or polygenic sex-determining (SD) gene systems have been documented (Kallman 1984;Matsuda et al 2002;Lee et al 2004;Vandeputte et al 2007).…”