Polygenic sex determination

Moore, Emily C.; Roberts, Reade B.

doi:10.1016/j.cub.2013.04.004

Cited by 98 publications

(75 citation statements)

References 12 publications

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“…Our results on sex ratio variation among, but not within, families of domesticated zebrafish corroborate previous observations from other PSD systems (48)(49)(50), namely that at normal temperatures offspring sex ratio has a genetic component with strong influence of parental genotypes (30). These data support the earlier claims that sex determination in domesticated zebrafish is polygenic (30,31,33,51).…”

Section: Discussionsupporting

confidence: 92%

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.

120

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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Section: Discussionsupporting

confidence: 92%

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.

120

136

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show abstract

“…While mammals and well-studied species from other taxa show relatively conserved sex determination patterns characterized by gonochorism, teleost fishes exhibit a high degree of sexual plasticity [7]. Teleost fishes display temperature-dependent, heterogenic, polygenic, and socially-controlled sex determination systems [7, 8]. Even in teleost species that exhibit genotypic sex determination, sex ratios can still be heavily skewed with hormone exposure before sexual maturation [9, 10].…”

Section: Introductionmentioning

confidence: 99%

Limited sex-biased neural gene expression patterns across strains in Zebrafish (Danio rerio)

2014

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BackgroundMale and female vertebrates typically differ in a range of characteristics, from morphology to physiology to behavior, which are influenced by factors such as the social environment and the internal hormonal and genetic milieu. However, sex differences in gene expression profiles in the brains of vertebrates are only beginning to be understood. Fishes provide a unique complement to studies of sex differences in mammals and birds given that fish show extreme plasticity and lability of sexually dimorphic characters and behaviors during development and even adulthood. Hence, teleost models can give additional insight into sexual differentiation. The goal of this study is to identify neurotranscriptomic mechanisms for sex differences in the brain.ResultsIn this study we examined whole-brain sex-biased gene expression through RNA-sequencing across four strains of zebrafish. We subsequently conducted systems level analyses by examining gene network dynamics between the sexes using weighted gene coexpression network analysis. Surprisingly, only 61 genes (approximately 0.4% of genes analyzed) showed a significant sex effect across all four strains, and 48 of these differences were male-biased. Several of these genes are associated with steroid hormone biosynthesis. Despite sex differences in a display of stress-related behaviors, basal transcript levels did not predict the intensity of the behavioral display. WGCNA revealed only one module that was significantly associated with sex. Intriguingly, comparing intermodule dynamics between the sexes revealed only moderate preservation. Further we identify sex-specific gene modules.ConclusionsDespite differences in morphology, physiology, and behavior, there is limited sex-biased neural gene expression in zebrafish. Further, genes found to be sex-biased are associated with hormone biosynthesis, suggesting that sex steroid hormones may be key contributors to sexual behavioral plasticity seen in teleosts. A possible mechanism is through regulating specific brain gene networks.Electronic supplementary materialThe online version of this article (doi:10.1186/1471-2164-15-905) contains supplementary material, which is available to authorized users.

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“…In most fishes, sex is determined at fertilization by sex chromosomes with a monofactorial system often based on a XX/XY male heterogamety or less frequently a ZZ/ZW male homogamety [Devlin and Nagahama, 2002;Volff et al, 2007;Kobayashi et al, 2013;Heule et al, 2014]. Sex in some fishes as well as in a few other animal species relies upon a polyfactorial system where the sum of various independent loci determines the sexual phenotype [Kosswig, 1964;Moore and Roberts, 2013;Meisel et al, 2016]. Contrary to mammals [Graves, 2006] and birds [Takagi and Sasaki, 1974], where the sex chromosome pair can be identified by its heteromorphy with a decayed 'heterogametic sex chromosome', in most of the poikilotherm vertebrates including fish, sex chromosomes are homomorphic and poorly differentiated [Grossen et al, 2011;Heule et al, 2014, Chalopin et al, 2015.…”

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confidence: 99%

The Reversible Sex of Gonochoristic Fish: Insights and Consequences

Baroiller¹,

D'Cotta²

2016

Sex Dev

142

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Fish sex reversal is a means to understand sex determination and differentiation, but it is also used to control sex in aquaculture. This review discusses sex reversal in gonochoristic fish, with the coexistence of genetic and environmental influences. The different periods of fish sensitivity to sex reversal treatments are presented with the mechanisms implicated. The old players of sex differentiation are revisited with transcriptome data and loss of function studies following hormone- or temperature-induced sex reversal. We also discuss whether cortisol is the universal mediator of sex reversal in fish due to its implication in ovarian meiosis and 11KT increase. The large plasticity in fish for sex reversal is also evident in the brain, with a reversibility existing even in adulthood. Studies on epigenetics are presented, since it links the environment, gene expression, and sex reversal, notably the association of DNA methylation in sex reversal. Manipulations with exogenous factors reverse the primary sex in many fish species under controlled conditions, but several questions arise on whether this can occur under wild conditions and what is the ecological significance. Cases of sex reversal in wild fish populations are shown and their fitness and future perspectives are discussed.

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Polygenic sex determination

Cited by 98 publications

References 12 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

Limited sex-biased neural gene expression patterns across strains in Zebrafish (Danio rerio)

The Reversible Sex of Gonochoristic Fish: Insights and Consequences

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