Lasting effects of early exposure to temperature on the gonadal transcriptome at the time of sex differentiation in the European sea bass, a fish with mixed genetic and environmental sex determination

Díaz, Noèlia; Piferrer, Francesc

doi:10.1186/s12864-015-1862-0

Cited by 71 publications

(67 citation statements)

References 77 publications

(87 reference statements)

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“…Therefore, the result of our study in PSD confirms previous observations of environmental dependency of sexual plasticity in domesticated zebrafish. Phenotypic masculinization is also reported in many other fish species with similar SD plasticity, such as European sea bass, Dicentrarchus labrax (Díaz & Piferrer, ), medaka, Oryzias latipes (Selim, Shinomiya, Otake, Hamaguchi, & Sakaizumi, ), and Nile tilapia, Oreochromis niloticus (Rougeot, Prignon, Kengne, & Mélard, ).…”

Section: Discussionmentioning

confidence: 65%

Phenotypic plasticity induced using high ambient temperature during embryogenesis in domesticated zebrafish, Danio rerio

Hosseini

Brenig

Tetens

et al. 2018

Reprod Domestic Animals

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Contents Ambient temperature during early stages of life has a substantial effect on physiological processes, eliciting phenotypic plasticity during zebrafish developmental stages. Zebrafish are known to possess a noteworthy ability to modify their phenotype in dependence of environmental factors. However, there is a poor understanding of the effects of temperature during embryogenesis, which influences the biological functions such as survival ability and masculinization in later developmental stages. Since the middle embryonic phase (pharyngula period) is genetically the most conserved stage in embryogenesis, it is very susceptible to embryonic lethality in developmental processes of vertebrates. Here, we tested the effect of transient perturbations (heat shock) during early development (5–24 hr post‐fertilization; hpf) at 35°C compared to control group at 28°C, on survival ability of zebrafish to study the embryonic and post‐embryonic mortality. We studied the variation of heat‐induced masculinization among and across the families in response to high temperature. Furthermore, morphometric traits of adult zebrafish at different developmental time points were measured in order to estimate the temperature × sex interaction effect. We found the highest embryonic mortality around the gastrula and segmentation periods in both experimental groups, with significantly lower survival ability in the temperature‐treated group (73.30% ± 0.58% vs. 70.19% ± 0.57%, respectively). A higher hatching success was observed in the control group (71.08% ± 0.61%) compared to the heat‐induced group (67.95% ± 0.60%). A distinct reduction in survival ability was also observed in both experimental groups during the first two weeks after hatching, followed by a reduced level of changes thereafter. We found sex ratio imbalances across all families, with 25.2% more males under temperature treatment. Our study on growth performance has shown a positive effect of increased temperature on growth plasticity, with a greater impact on female fish in response to high ambient temperature.

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Section: Discussionmentioning

confidence: 65%

Phenotypic plasticity induced using high ambient temperature during embryogenesis in domesticated zebrafish, Danio rerio

Hosseini

Brenig

Tetens

et al. 2018

Reprod Domestic Animals

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“…Interestingly, hdac11 and ehmt2 expression had been upregulated with heat-induced masculinisation in European seabass [93]. The expression levels of the histone variants h2afx and h1m had been lower in MT-treated testes than ovaries, similar to reported female-biased expression in Olive flounder [147].…”

Section: Discussionmentioning

confidence: 65%

Histological and transcriptomic effects of 17α-methyltestosterone on zebrafish gonad development

et al. 2017

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BackgroundSex hormones play important roles in teleost ovarian and testicular development. In zebrafish, ovarian differentiation appears to be dictated by an oocyte-derived signal via Cyp19a1a aromatase-mediated estrogen production. Androgens and aromatase inhibitors can induce female-to-male sex reversal, however, the mechanisms underlying gonadal masculinisation are poorly understood. We used histological analyses together with RNA sequencing to characterise zebrafish gonadal transcriptomes and investigate the effects of 17α-methyltestosterone on gonadal differentiation.ResultsAt a morphological level, 17α-methyltestosterone (MT) masculinised gonads and accelerated spermatogenesis, and these changes were paralleled in masculinisation and de-feminisation of gonadal transcriptomes. MT treatment upregulated expression of genes involved in male sex determination and differentiation (amh, dmrt1, gsdf and wt1a) and those involved in 11-oxygenated androgen production (cyp11c1 and hsd11b2). It also repressed expression of ovarian development and folliculogenesis genes (bmp15, gdf9, figla, zp2.1 and zp3b). Furthermore, MT treatment altered epigenetic modification of histones in zebrafish gonads. Contrary to expectations, higher levels of cyp19a1a or foxl2 expression in control ovaries compared to MT-treated testes and control testes were not statistically significant during early gonad development (40 dpf).ConclusionOur study suggests that both androgen production and aromatase inhibition are important for androgen-induced gonadal masculinisation and natural testicular differentiation in zebrafish.Electronic supplementary materialThe online version of this article (doi:10.1186/s12864-017-3915-z) contains supplementary material, which is available to authorized users.

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“…This difference represents just a fraction (8%) of the ∼15,000 DETs that were differentially expressed between untreated females (FCT) and males (MCT), which, in turn, account for a significant part of the estimated number of protein-coding genes (>25,000) in zebrafish. In fish, masculinization by elevated temperature usually involves down-regulation of profemale genes, such as cyp19a1a and foxl2, and up-regulation of promale genes, such as dmrt1 or amh (8)(9)(10)(11)(12)(13)(14). In accordance with this general pattern, the FHT2 females with a male-like gonadal transcriptome exhibited down-regulation of both key profemale genes such as cyp19a1a and vtg5 as well as downregulation of profemale pathways such as oocyte meiosis, progesterone-mediated oocyte maturation, canonical Wnt signaling (28,53), and Fanconi anemia (26).…”

Section: Discussionmentioning

confidence: 99%

“…Regardless of the actual underlying sex-determining mechanism, a shared characteristic of all fish species in which temperature can alter sex ratios is that exposure to heat during early development upregulates the expression of genes related to testis differentiation with a concomitant down-regulation of genes related to ovarian differentiation, as assessed in several species (e.g., 9,13,[15][16][17]. This results in an increase in the proportion of males (18) and implies that some genetic females (XX or ZW females) in CSD species, or fish that otherwise would develop as females in a PSD system, end up developing as phenotypic males despite their genetic makeup.…”

mentioning

confidence: 99%

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.

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110

136

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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...

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Lasting effects of early exposure to temperature on the gonadal transcriptome at the time of sex differentiation in the European sea bass, a fish with mixed genetic and environmental sex determination

Cited by 71 publications

References 77 publications

Phenotypic plasticity induced using high ambient temperature during embryogenesis in domesticated zebrafish, Danio rerio

Phenotypic plasticity induced using high ambient temperature during embryogenesis in domesticated zebrafish, Danio rerio

Histological and transcriptomic effects of 17α-methyltestosterone on zebrafish gonad development

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

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