Balancing the effects of rearing at low temperature during early development on sex ratios, growth and maturation in the European sea bass (Dicentrarchus labrax).

Navarro‐Martín, Laia; Blázquez, Mercedes; Viñas, Jordi; Joly, Sílvia; Piferrer, Francesc

doi:10.1016/j.aquaculture.2009.07.022

Cited by 58 publications

(67 citation statements)

References 46 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…An interesting open question for future studies concerns the number and type of additional genes that would need to be altered to cause not only transcriptional but also morphological sex reversal. Threshold hypothesis for heat-induced masculinization supports previous observations in the European sea bass in which heatresistant fish were females that could not be masculinized by high temperature (55).…”

Section: Discussionsupporting

confidence: 78%

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

Ribas

Liew

Díaz

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

Self Cite

116

136

View full text Add to dashboard Cite

Understanding environmental influences on sex ratios is important for the study of the evolution of sex-determining mechanisms and for evaluating the effects of global warming and chemical pollution. Fishes exhibit sexual plasticity, but the underlying mechanisms of environmental effects on their reproduction are unclear even in the well-established teleost research model, the zebrafish. Here we established the conditions to study the effects of elevated temperature on zebrafish sex. We showed that sex ratio response to elevated temperature is family-specific and typically leads to masculinization (female-to-male sex reversal), resulting in neomales. These results uncovered genotype-by-environment interactions that support a polygenic sex determination system in domesticated (laboratory) zebrafish. We found that some heat-treated fish had gene expression profiles similar to untreated controls of the same sex, indicating that they were resistant to thermal effects. Further, most neomales had gonadal transcriptomes similar to that of regular males. Strikingly, we discovered heat-treated females that displayed a normal ovarian phenotype but with a "male-like" gonadal transcriptome. Such major transcriptomic reprogramming with preserved organ structure has never been reported. Juveniles were also found to have a male-like transcriptome shortly after exposure to heat. These findings were validated by analyzing the expression of genes and signaling pathways associated with sex differentiation. Our results revealed a lasting thermal effect on zebrafish gonads, suggesting new avenues for detection of functional consequences of elevated temperature in natural fish populations in a global warming scenario.A major paradox in developmental biology is the lack of conservation of sex-determining mechanisms even in closely related taxa (1). Thus, in mammals and birds, sex is genetically canalized by a chromosomal sex determination (CSD) system of male (XX/XY in mammals) or female (ZW/ZZ in birds) heterogamety, driven by the action of a master sex-determining gene: sry in mammals and dmrt1 in birds (1). In contrast, fish sex can be very plastic, with the combination of genetic and environmental influences (2). In addition to fish species with CSD, there are species with polygenic sex determination (PSD), in which sex depends on the combined action of several promale and profemale genetic factors, and species with temperature-dependent sex determination (TSD) (3). Understanding how the environment influences sex ratios in vertebrates is of fundamental importance in the study of the evolution of sex-determining mechanisms (4, 5). It is also of practical relevance in evaluating the effects of climate change and chemical pollution (6, 7).The effects of temperature on gene expression during sex differentiation have been investigated in different teleost species, including the African catfish, Clarias gariepinus (8), European sea bass, Dicentrarchus labrax (9, 10), Japanese flounder, Paralichthys olivaceus (11), pejerrey, Odontesthes...

show abstract

Section: Discussionsupporting

confidence: 78%

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

Ribas

Liew

Díaz

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

Self Cite

116

136

View full text Add to dashboard Cite

show abstract

“…Temperature and genetics contribute approximately equally to sex determination [18]–[20]. Importantly, both GSD+TE and “pure” TSD fish species have exactly the same response to high temperature: inhibition of cyp19a expression [4].…”

Section: Introductionmentioning

confidence: 99%

“…During sex differentiation, the primordial gonads, starting from a common primordium, can take two mutually exclusive different developmental pathways towards the formation of an ovary or a testis. Previous studies demonstrated that temperature effects in the European sea bass are more pronounced during the first half of the TSP, when fish are about 30 mm [20]. Interestingly, this not only occurs before morphological sex differentiation takes place (>150 dpf; ∼120 mm fish) but also even before the formation of the gonadal ridges at ∼35 dpf [26].…”

Section: Introductionmentioning

confidence: 99%

DNA Methylation of the Gonadal Aromatase (cyp19a) Promoter Is Involved in Temperature-Dependent Sex Ratio Shifts in the European Sea Bass

et al. 2011

Self Cite

View full text Add to dashboard Cite

Sex ratio shifts in response to temperature are common in fish and reptiles. However, the mechanism linking temperature during early development and sex ratios has remained elusive. We show in the European sea bass (sb), a fish in which temperature effects on sex ratios are maximal before the gonads form, that juvenile males have double the DNA methylation levels of females in the promoter of gonadal aromatase (cyp19a), the enzyme that converts androgens into estrogens. Exposure to high temperature increased the cyp19a promoter methylation levels of females, indicating that induced-masculinization involves DNA methylation-mediated control of aromatase gene expression, with an observed inverse relationship between methylation levels and expression. Although different CpGs within the sb cyp19a promoter exhibited different sensitivity to temperature, we show that the increased methylation of the sb cyp19a promoter, which occurs in the gonads but not in the brain, is not a generalized effect of temperature. Importantly, these effects were also observed in sexually undifferentiated fish and were not altered by estrogen treatment. Thus, methylation of the sb cyp19a promoter is the cause of the lower expression of cyp19a in temperature-masculinized fish. In vitro, induced methylation of the sb cyp19a promoter suppressed the ability of SF-1 and Foxl2 to stimulate transcription. Finally, a CpG differentially methylated by temperature and adjacent to a Sox transcription factor binding site is conserved across species. Thus, DNA methylation of the aromatase promoter may be an essential component of the long-sought-after mechanism connecting environmental temperature and sex ratios in vertebrate species with temperature-dependent sex determination.

show abstract

“…The current hypothesis is that high temperatures early in development (before 100 days post-fertilization, dpf) lead to decreased female rates (Piferrer et al 2005), probably through an inhibition of female differentiation (Navarro-Martin et al 2009). However long-lasting low temperatures also produce an excess of males interpreted as caused by a low growth rate precluding female orientation (Navarro-Martin et al 2009). Thus, the excess of males observed in culture would be due to the use of temperatures higher than in the wild.…”

Section: Introductionmentioning

confidence: 99%

Are sex ratios in wild European sea bass (Dicentrarchus labrax) populations biased?

Vandeputte

Quillet

Chatain

2012

Aquat. Living Resour.

View full text Add to dashboard Cite

-Sex ratios in farmed European sea bass are highly biased towards males (75 to 95%), which is problematic for aquaculture. In this mini-review, we re-analyse fisheries literature data about sex ratios in wild sea bass from 13 population samples, representing altogether 4889 individuals covering the major part of the distribution range of the species. We find that as a whole, the sex ratio of wild populations is biased towards females (59.4% females, p < 0.001), but that the sex ratio of the younger fish (<30 cm total length) is balanced (52.0% females, p = 0.15), while the sex ratio of the older fish is heavily biased towards females (69.5% females, p < 0.01). Possible causes of these differences (differential longevity, biased sampling) are discussed. When age-group sex ratios are available (three population samples out of 13), significant variation between age groups appears, part of which is most likely of environmental origin. This study shows that the excess of males in culture is not a characteristic of the species, but rather a consequence of the environments used in culture, interacting with a complex system where both environmental and genetic influences govern sex determination in sea bass.

show abstract

Balancing the effects of rearing at low temperature during early development on sex ratios, growth and maturation in the European sea bass (Dicentrarchus labrax).

Cited by 58 publications

References 46 publications

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

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

DNA Methylation of the Gonadal Aromatase (cyp19a) Promoter Is Involved in Temperature-Dependent Sex Ratio Shifts in the European Sea Bass

Are sex ratios in wild European sea bass (Dicentrarchus labrax) populations biased?

Contact Info

Product

Resources

About