Elevated Temperature Applied during Gonadal Transformation Leads to Male Bias in Zebrafish <b><i>(Danio rerio)</i></b>

Abstract

Temperature effects on sex determination or differentiation exist in many fish species, with high temperatures predominantly producing more males. The present study aimed at elucidating the genetic background of temperature effects on sex differentiation in zebrafish. Experimental fish were generated by matings between 4 or 6 golden females and a normal or a mitotic gynogenetic male, respectively. All the larvae were reared at 28.5°C until they were divided into 3 groups per full-sib family, a control group raised at 28.5°C and 2 treatment groups reared at 35°C from 20 to 30 dpf or 25 to 35 dpf, respectively. Backcross progenies, reared at 28.5°C, were derived from F1 temperature-treated sons (35°C, 25–35 dpf) that were sired by a mitotic gynogenetic male and their corresponding mothers. No significant differences were observed regarding the survival rate between the control and treatment groups. Significant differences in the phenotypic male proportions from the controls were observed in groups treated at 35°C. The sex ratio in zebrafish was influenced by the male spawner, the female spawner, and a significant interaction of genotype by temperature. Backcross experiments point to a continuum of major genetic, minor genetic, and environmental factors in the expression of the phenotypic sex in zebrafish.

Heat-induced masculinization in domesticated zebrafish is family-specific and yields a set of different gonadal transcriptomes

“…Our results, therefore, emphasize the interplay between genetic and environmental influences and provide a potential explanation for the variable sex ratios observed in zebrafish facilities across the world, which are often unpredictable and biased. The masculinizing effect of elevated temperature confirms previous results in zebrafish (36,39) and correlates with results found in the literature in many other fish species (for reviews, see refs. 16 and 18).…”

“…In domesticated zebrafish, the effects of elevated temperature have been studied after exposure periods concerning embryos (35), juveniles (36,37), or development until adults (38,39). In agreement with the general pattern in fish (18), elevated temperatures result in a higher number of males, although, surprisingly, one study reported more females (40).…”

Wild Sex in Zebrafish: Loss of the Natural Sex Determinant in Domesticated Strains

“…Answers likely lie in environmental factors and background genetic features that affect the strength of a meiotic oocyte-derived pro-female signal that inhibits oocyte apoptosis, probably by maintaining aromatase production (Slanchev et al 2005;Houwing et al 2007;Wang et al 2007;Siegfried and Nusslein-Volhard 2008;Rodriguez-Mari et al 2010Rodríguez-Marí and Postlethwait 2011;Pradhan et al 2012;Dranow et al 2013). In general, harsh conditions, including high density and poor nutrition, tend to promote male development (Walker-Durchanek 1980;Pelegri and Schulte-Merker 1999;Shang et al 2006;Lawrence et al 2008;Abozaid et al 2011Abozaid et al , 2012Liew et al 2012;Villamizar et al 2012). These harsh factors may act to decrease the pro-female signal by depressing the pool of meiotic oocytes, either by inhibiting primary germ-cell proliferation or entry into meiosis or by promoting oocyte apoptosis.…”

“…As expected from the hypothesis that oocyte death is a major feature of zebrafish sex determination, harsh environmental conditions tend to shift sex ratios in favor of males; such factors include gamma rays, hypoxia, high density, high temperature, altered thermocycles, and poor nutrition (Walker-Durchanek 1980;Shang et al 2006;Lawrence et al 2008;Abozaid et al 2011Abozaid et al , 2012Liew et al 2012;Villamizar et al 2012). Zebrafish does not, however, have a typical environmental sex-determination (ESD) mechanism like some sauropsids for which temperature is a cue (Charnier 1966;Lang and Andrews 1994;Merchant-Larios and Diaz-Hernandez 2013;Mork et al 2014).…”

“…In the absence of germ cells (Slanchev et al 2005;Siegfried and Nusslein-Volhard 2008) and in mutants in which oocytes undergo apoptosis (Rodríguez-Marí et al 2005, 2010Rodríguez-Marí and Postlethwait 2011), gonads develop as testes and individuals become males. Remarkably, mutants that produce oocytes early and reproduce as females can transform into fertile males after oocyte depletion, showing that oocytes are necessary both for primary sex determination and for maintenance of female phenotype in adult zebrafish (Dranow et al 2013).As expected from the hypothesis that oocyte death is a major feature of zebrafish sex determination, harsh environmental conditions tend to shift sex ratios in favor of males; such factors include gamma rays, hypoxia, high density, high temperature, altered thermocycles, and poor nutrition (Walker-Durchanek 1980;Shang et al 2006;Lawrence et al 2008;Abozaid et al 2011Abozaid et al , 2012Liew et al 2012;Villamizar et al 2012). Zebrafish does not, however, have a typical environmental sex-determination (ESD) mechanism like some sauropsids for which temperature is a cue (Charnier 1966;Lang and Andrews 1994;Merchant-Larios and Diaz-Hernandez 2013;Mork et al 2014).…”