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1
Yamaguchi, Toshiya, Norifumi Yoshinaga, Takashi Yazawa, Koichiro Gen, and Takeshi Kitano. "Cortisol Is Involved in Temperature-Dependent Sex Determination in the Japanese Flounder." Endocrinology 151, no. 8 (June 9, 2010): 3900–3908. http://dx.doi.org/10.1210/en.2010-0228.
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In vertebrates, sex is normally determined by genotype. However, in poikilothermal vertebrates, including reptiles, amphibians, and fishes, sex determination is greatly influenced by environmental factors, such as temperature. Little is known about the molecular mechanisms underlying environmental sex determination in these species. The Japanese flounder (Paralichthys olivaceus) is a teleost fish with an XX/XY sex determination system. However, XX flounder can be induced to develop into predominantly either phenotypic females or males, by rearing at 18 or 27 C, respectively, during the sex differentiation period. Therefore, the flounder provides an excellent model to study the molecular mechanisms underlying temperature-dependent sex determination. We previously showed that an aromatase inhibitor, an antiestrogen, and 27 C treatments cause masculinization of XX flounder, as well as suppression of mRNA expression of ovary-type aromatase (cyp19a1), a steroidogenic enzyme responsible for the conversion of androgens to estrogens in the gonads. Furthermore, estrogen administration completely inhibits masculinization by these treatments, suggesting suppression of cyp19a1 mRNA expression, and the resultant estrogen biosynthesis may trigger masculinization of the XX flounder induced by high water temperature. Here, we demonstrated that cortisol causes female-to-male sex reversal by directly suppressing cyp19a1 mRNA expression via interference with cAMP-mediated activation and that metyrapone (an inhibitor of cortisol synthesis) inhibits 27 C-induced masculinization of XX flounder. Moreover, cortisol concentrations in 27 C-reared juveniles were significantly higher than in 18 C-reared fishes during sexual differentiation. These results strongly suggest that masculinization by high water temperature is ascribable to elevation of cortisol concentration during gonadal sex differentiation in the flounder.
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Orlando, Edward F., Yoshinao Katsu, Shinichi Miyagawa, and Taisen Iguchi. "Cloning and differential expression of estrogen receptor and aromatase genes in the self-fertilizing hermaphrodite and male mangrove rivulus, Kryptolebias marmoratus." Journal of Molecular Endocrinology 37, no. 2 (October 2006): 353–65. http://dx.doi.org/10.1677/jme.1.02101.
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The mechanisms underlying sex determination and differentiation in fishes are labile in response to environmental parameters. Sex-specific phenotypes are largely regulated by sex steroids, and the inhibition or the stimulation of aromatase can reverse sex as well as alter secondary sexual characteristics in fishes. Among vertebrates, the mangrove rivulus is the only known self-fertilizing hermaphrodite. Throughout most of its range, rivulus appear to exist as clonally reproducing hermaphrodites. However, outcrossing has been documented in Belize, where up to 25% of rivulus collected are males. The direct development of (primary) males occurs when embryos are incubated at 18 °C and hermaphrodites develop into secondary males when held at 28 °C. Given the importance of sex steroids, their receptors, and aromatase in sex determination and differentiation of fishes, we cloned, sequenced, and quantified the expression of estrogen receptors (ERα, ERβ) and ovarian (AroA) and brain (AroB) aromatase genes. Hermaphrodites had increased ERα, ERβ, AroA, and AroB gene expression in the liver, gonad, gonad, and brain respectively, compared to males. These data are consistent with the gene expression data reported for other species and are reflective of the presence of ovarian tissue in the hermaphrodites. Interestingly, we show the elevated expression of brain aromatase in the hermaphrodite brain. The role of the dimorphic expression of brain aromatase in the regulation of sex-specific characteristics is intriguing and requires further research. Because of the uniqueness of its reproductive biology, rivulus is an excellent model for elucidating the mechanisms regulating vertebrate sex determination and sexual differentiation.
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Belaid, Baya, Noelle Richard-Mercier, Claude Pieau, and Mireille Dorizzi. "Sex reversal and aromatase in the European pond turtle: Treatment with letrozole after the thermosensitive period for sex determination." Journal of Experimental Zoology 290, no. 5 (2001): 490–97. http://dx.doi.org/10.1002/jez.1092.
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Kroon, Frederieke J., Philip L. Munday, David A. Westcott, Jean-Paul A. Hobbs, and N. Robin Liley. "Aromatase pathway mediates sex change in each direction." Proceedings of the Royal Society B: Biological Sciences 272, no. 1570 (June 16, 2005): 1399–405. http://dx.doi.org/10.1098/rspb.2005.3097.
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The enzyme aromatase controls the androgen/oestrogen ratio by catalysing the irreversible conversion of testosterone into oestradiol (E 2 ). Therefore, the regulation of E 2 synthesis by aromatase is thought to be critical in sexual development and differentiation. Here, we demonstrate for the first time that experimental manipulation of E 2 levels via the aromatase pathway induces adult sex change in each direction in a hermaphroditic fish that naturally exhibits bidirectional sex change. Our results demonstrate that a single enzymatic pathway can regulate both female and male sexual differentiation, and that aromatase may be the key enzyme that transduces environmental, including social, cues to functional sex differentiation in species with environmental sex determination.
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Sun, Li-Na, Xiao-Long Jiang, Qing-Ping Xie, Jing Yuan, Bao-Feng Huang, Wen-Jing Tao, Lin-Yan Zhou, Yoshitaka Nagahama, and De-Shou Wang. "Transdifferentiation of Differentiated Ovary into Functional Testis by Long-Term Treatment of Aromatase Inhibitor in Nile Tilapia." Endocrinology 155, no. 4 (April 1, 2014): 1476–88. http://dx.doi.org/10.1210/en.2013-1959.
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Females with differentiated ovary of a gonochoristic fish, Nile tilapia, were masculinized by long-term treatment with an aromatase inhibitor (Fadrozole) in the present study. The reversed gonads developed into functional testes with fertile sperm. The longer the fish experienced sex differentiation, the longer treatment time was needed for successful sex reversal. Furthermore, Fadrozole-induced sex reversal, designated as secondary sex reversal (SSR), was successfully rescued by supplement of exogenous 17β-estradiol. Gonadal histology, immunohistochemistry, transcriptome, and serum steroid level were analyzed during SSR. The results indicated that spermatogonia were transformed from oogonia or germline stem cell-like cells distributed in germinal epithelium, whereas Leydig and Sertoli cells probably came from the interstitial cells and granulosa cells of the ovarian tissue, respectively. The transdifferentiation of somatic cells, as indicated by the appearance of doublesex- and Mab-3-related transcription factor 1 (pre-Sertoli cells) and cytochrome P450, family 11, subfamily B, polypeptide 2 (pre-Leydig cells)-positive cells in the ovary, provided microniche for the transdifferentiation of germ cells. Decrease of serum 17β-estradiol was detected earlier than increase of serum 11-ketotestosterone, indicating that decrease of estrogen was the cause, whereas increase of androgen was the consequence of SSR. The sex-reversed gonad displayed more similarity in morphology and histology with a testis, whereas the global gene expression profiles remained closer to the female control. Detailed analysis indicated that transdifferentiation was driven by suppression of female pathway genes and activation of male pathway genes. In short, SSR provides a good model for study of sex reversal in teleosts and for understanding of sex determination and differentiation in nonmammalian vertebrates.
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Lambert, Max R., Tien Tran, Andrzej Kilian, Tariq Ezaz, and David K. Skelly. "Molecular evidence for sex reversal in wild populations of green frogs (Rana clamitans)." PeerJ 7 (February 8, 2019): e6449. http://dx.doi.org/10.7717/peerj.6449.
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In vertebrates, sex determination occurs along a continuum from strictly genotypic (GSD), where sex is entirely guided by genes, to strictly environmental (ESD), where rearing conditions, like temperature, determine phenotypic sex. Along this continuum are taxa which have combined genetic and environmental contributions to sex determination (GSD + EE), where some individuals experience environmental effects which cause them to sex reverse and develop their phenotypic sex opposite their genotypic sex. Amphibians are often assumed to be strictly GSD with sex reversal typically considered abnormal. Despite calls to understand the relative natural and anthropogenic causes of amphibian sex reversal, sex reversal has not been closely studied across populations of any wild amphibian, particularly in contrasting environmental conditions. Here, we use sex-linked molecular markers to discover sex reversal in wild populations of green frogs (Rana clamitans) inhabiting ponds in either undeveloped, forested landscapes or in suburban neighborhoods. Our work here begins to suggest that sex reversal may be common within and across green frog populations, occurring in 12 of 16 populations and with frequencies of 2–16% of individuals sampled within populations. Additionally, our results also suggest that intersex phenotypic males and sex reversal are not correlated with each other and are also not correlated with suburban land use. While sex reversal and intersex are often considered aberrant responses to human activities and associated pollution, we found no such associations here. Our data perhaps begin to suggest that, relative to what is often suggested, sex reversal may be a relatively natural process in amphibians. Future research should focus on assessing interactions between genes and the environment to understand the molecular and exogenous basis of sex determination in green frogs and in other amphibians.
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Estermann, Martin Andres, and Craig Allen Smith. "Fadrozole-Mediated Sex Reversal Induces PAX2+Undifferentiated Supporting Cells in Female Chicken Gonads." Journal of the Endocrine Society 5, Supplement_1 (May 1, 2021): A765—A766. http://dx.doi.org/10.1210/jendso/bvab048.1557.
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Abstract During early embryogenesis, the undifferentiated gonad is bipotential and subsequently commits to an ovarian or testicular fate. In birds, double dose of the Z-linked gene DMRT1 is required for testicular differentiation in male embryos (genetically ZZ). In female birds, estrogen plays a key role in ovarian differentiation. 17β-estradiol (E2) induces gonadal feminization when applied to male embryos (ZZ). Conversely, inhibition of estrogen synthesis with the drug fadrozole (FAD) results in testicular development in genetically female embryos (ZW). However, activation of male markers in sex-reversed ZW embryos is typically delayed, raising the possibility that FAD-treated embryos may transition through an undifferentiated state before masculinization. Recently, PAX2 was identified as a marker of undifferentiated supporting cells in the chicken embryo, being downregulated in both sexes at the onset of gonadal sex determination. To investigate the supporting cell differentiation process in estrogen-mediated sex reversal, we injected 1 mg of fadrozole in 100µl of PBS or vehicle into embryonic day 3.5 (E3.5) chicken eggs. Eggs were incubated until E9.5, genotypically sexed (ZZ or ZW) and processed for qRT-PCR and immunofluorescence. Quantitative RT-PCR confirmed that sex reversal had occurred in FAD-treated females, showing a reduction of pre-granulosa cell markers aromatase (P<0.005) and FOXL2 (P<0.05), compared to the control. Interestingly, PAX2 mRNA expression was up-regulated (P<0.05) in sex-reversed females, suggesting an increase in undifferentiated supporting cells (n=6). To confirm this observation, immunofluorescence was used to detect aromatase, SOX9 (male marker) and PAX2. In FAD-treated females, both SOX9+ (male) and aromatase+ (female) cells co-existed in the same gonad, but in separated defined regions. Aromatase positive cells were located in the most apical region of the gonad whereas SOX9 positive cells were detected in the basal region. We detected an increase in PAX2 positive cells in the gonadal medulla between the SOX9 and aromatase positive supporting cells. No SOX9 or PAX2 positive cells were detected in control female gonads (n=3). For feminization experiments 100µl of a 1mg/ml solution of E2 or vehicle (Oil) was injected into E3.5 chicken eggs. No significant increase in PAX2 was detected by qRT-PCR (p>0.05, n=6) and no PAX2 positive cells were detected in E2 treated gonads at E9.5. These results suggest that in fadrozole-mediated masculinization (but not in estrogen-induced feminization) there is an increase in undifferentiated supporting cells. The absence of both estrogens (feminizing) and elevated DMRT1 (masculinizing) could explain why the supporting cells remain in an undifferentiated state in ZW (genetically female) embryos. Further research is required to evaluate the fate of these undifferentiated cells in gonadal sex differentiation.
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Voigt, Cornelia. "Neuroendocrine correlates of sex-role reversal in barred buttonquails." Proceedings of the Royal Society B: Biological Sciences 283, no. 1843 (November 30, 2016): 20161969. http://dx.doi.org/10.1098/rspb.2016.1969.
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Sex differences in brain structure and behaviour are well documented among vertebrates. An excellent model exploring the neural mechanisms of sex differences in behaviour is represented by sex-role-reversed species. In the majority of bird species, males compete over access to mates and resources more strongly than do females. It is thought that the responsible brain regions are therefore more developed in males than in females. Because these behaviours and brain regions are activated by androgens, males usually have increased testosterone levels during breeding. Therefore, in species with sex-role reversal, certain areas of the female brain should be more developed or steroid hormone profiles should be sexually reversed. Here, I studied circulating hormone levels and gene expression of steroid hormone receptors and aromatase in a captive population of barred buttonquails ( Turnix suscitator ). While females performed courtship and agonistic behaviours, there was no evidence for sexually reversed hormone profiles. However, I found female-biased sex differences in gene expression of androgen receptors in several hypothalamic and limbic brain regions that were already in place at hatching. Such sex differences are not known from non-sex-role-reversed species. These data suggest that increased neural sensitivity to androgens could be involved in the mechanisms mediating sex-role-reversed behaviours.
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Zhou, Yingjie, Wei Sun, Han Cai, Haisheng Bao, Yu Zhang, Guoying Qian, and Chutian Ge. "The Role of Anti-Müllerian Hormone in Testis Differentiation Reveals the Significance of the TGF-β Pathway in Reptilian Sex Determination." Genetics 213, no. 4 (October 23, 2019): 1317–27. http://dx.doi.org/10.1534/genetics.119.302527.
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Anti-Müllerian hormone (Amh, or Müllerian-inhibiting substance, Mis), a member of TGF-β superfamily, has been well documented in some vertebrates as initiator or key regulator in sexual development, and particularly in fish. However, its functional role has not yet been identified in reptiles. Here, we characterized the Amh gene in the Chinese soft-shelled turtle Pelodiscus sinensis, a typical reptilian species exhibiting ZZ/ZW sex chromosomes. The messenger RNA of Amh was initially expressed in male embryonic gonads by stage 15, preceding gonadal sex differentiation, and exhibited a male-specific expression pattern throughout embryogenesis. Moreover, Amh was rapidly upregulated during female-to-male sex reversal induced by aromatase inhibitor letrozole. Most importantly, Amh loss of function by RNA interference led to complete feminization of genetic male (ZZ) gonads, suppression of the testicular marker Sox9, and upregulation of the ovarian regulator Cyp19a1. Conversely, overexpression of Amh in ZW embryos resulted in female-to-male sex reversal, characterized by the formation of a testis structure, ectopic activation of Sox9, and a remarkable decline in Cyp19a1. Collectively, these findings provide the first solid evidence that Amh is both necessary and sufficient to drive testicular development in a reptilian species, P. sinensis, highlighting the significance of the TGF-β pathway in reptilian sex determination.
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Sakae, Yuta, and Minoru Tanaka. "Metabolism and Sex Differentiation in Animals from a Starvation Perspective." Sexual Development 15, no. 1-3 (2021): 168–78. http://dx.doi.org/10.1159/000515281.
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Animals determine their sex genetically (GSD: genetic sex determination) and/or environmentally (ESD: environmental sex determination). Medaka (<i>Oryzias latipes</i>) employ a XX/XY GSD system, however, they display female-to-male sex reversal in response to various environmental changes such as temperature, hypoxia, and green light. Interestingly, we found that 5 days of starvation during sex differentiation caused female-to-male sex reversal. In this situation, the metabolism of pantothenate and fatty acid synthesis plays an important role in sex reversal. Metabolism is associated with other biological factors such as germ cells, HPG axis, lipids, and epigenetics, and supplys substances and acts as signal transducers. In this review, we discuss the importance of metabolism during sex differentiation and how metabolism contributes to sex differentiation.
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Richard-Mercier, Noëlle, Mireille Dorizzi, Gisèle Desvages, Marc Girondot, and Claude Pieau. "Endocrine Sex Reversal of Gonads by the Aromatase Inhibitor Letrozole (CGS 20267) in Emys orbicularis, a Turtle with Temperature-Dependent Sex Determination." General and Comparative Endocrinology 100, no. 3 (December 1995): 314–26. http://dx.doi.org/10.1006/gcen.1995.1162.
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Whiteley, Sarah L., Meghan A. Castelli, Duminda S. B. Dissanayake, Clare E. Holleley, and Arthur Georges. "Temperature-Induced Sex Reversal in Reptiles: Prevalence, Discovery, and Evolutionary Implications." Sexual Development 15, no. 1-3 (2021): 148–56. http://dx.doi.org/10.1159/000515687.
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Sex reversal is the process by which an individual develops a phenotypic sex that is discordant with its chromosomal or genotypic sex. It occurs in many lineages of ectothermic vertebrates, such as fish, amphibians, and at least one agamid and one scincid reptile species. Sex reversal is usually triggered by an environmental cue that alters the genetically determined process of sexual differentiation, but it can also be caused by exposure to exogenous chemicals, hormones, or pollutants. Despite the occurrence of both temperature-dependent sex determination (TSD) and genetic sex determination (GSD) broadly among reptiles, only 2 species of squamates have thus far been demonstrated to possess sex reversal in nature (GSD with overriding thermal influence). The lack of species with unambiguously identified sex reversal is not necessarily a reflection of a low incidence of this trait among reptiles. Indeed, sex reversal may be relatively common in reptiles, but little is known of its prevalence, the mechanisms by which it occurs, or the consequences of sex reversal for species in the wild under a changing climate. In this review, we present a roadmap to the discovery of sex reversal in reptiles, outlining the various techniques that allow new occurrences of sex reversal to be identified, the molecular mechanisms that may be involved in sex reversal and how to identify them, and approaches for assessing the impacts of sex reversal in wild populations. We discuss the evolutionary implications of sex reversal and use the central bearded dragon (<i>Pogona vitticeps</i>) and the eastern three-lined skink (<i>Bassiana duperreyi</i>) as examples of how species with opposing patterns of sex reversal may be impacted differently by our rapidly changing climate. Ultimately, this review serves to highlight the importance of understanding sex reversal both in the laboratory and in wild populations and proposes practical solutions to foster future research.
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Whiteley, Sarah L., Arthur Georges, Vera Weisbecker, Lisa E. Schwanz, and Clare E. Holleley. "Ovotestes suggest cryptic genetic influence in a reptile model for temperature-dependent sex determination." Proceedings of the Royal Society B: Biological Sciences 288, no. 1943 (January 20, 2021): 20202819. http://dx.doi.org/10.1098/rspb.2020.2819.
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Sex determination and differentiation in reptiles is complex. Temperature-dependent sex determination (TSD), genetic sex determination (GSD) and the interaction of both environmental and genetic cues (sex reversal) can drive the development of sexual phenotypes. The jacky dragon ( Amphibolurus muricatus ) is an attractive model species for the study of gene–environment interactions because it displays a form of Type II TSD, where female-biased sex ratios are observed at extreme incubation temperatures and approximately 50 : 50 sex ratios occur at intermediate temperatures. This response to temperature has been proposed to occur due to underlying sex determining loci, the influence of which is overridden at extreme temperatures. Thus, sex reversal at extreme temperatures is predicted to produce the female-biased sex ratios observed in A. muricatus . The occurrence of ovotestes during development is a cellular marker of temperature sex reversal in a closely related species Pogona vitticeps . Here, we present the first developmental data for A. muricatus , and show that ovotestes occur at frequencies consistent with a mode of sex determination that is intermediate between GSD and TSD. This is the first evidence suggestive of underlying unidentified sex determining loci in a species that has long been used as a model for TSD.
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Sun, Bao-Jun, Teng Li, Yi Mu, Jessica K. McGlashan, Arthur Georges, Richard Shine, and Wei-Guo Du. "Thyroid hormone modulates offspring sex ratio in a turtle with temperature-dependent sex determination." Proceedings of the Royal Society B: Biological Sciences 283, no. 1841 (October 26, 2016): 20161206. http://dx.doi.org/10.1098/rspb.2016.1206.
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The adaptive significance of temperature-dependent sex determination (TSD) has attracted a great deal of research, but the underlying mechanisms by which temperature determines the sex of a developing embryo remain poorly understood. Here, we manipulated the level of a thyroid hormone (TH), triiodothyronine (T 3 ), during embryonic development (by adding excess T 3 to the eggs of the red-eared slider turtle Trachemys scripta , a reptile with TSD), to test two competing hypotheses on the proximate basis for TSD: the developmental rate hypothesis versus the hormone hypothesis . Exogenous TH accelerated embryonic heart rate (and hence metabolic rate), developmental rate, and rates of early post-hatching growth. More importantly, hyperthyroid conditions depressed expression of Cyp19a1 (the gene encoding for aromatase) and levels of oestradiol, and induced more male offspring. This result is contrary to the direction of sex-ratio shift predicted by the developmental rate hypothesis , but consistent with that predicted by the hormone hypothesis . Our results suggest an important role for THs in regulating sex steroid hormones, and therefore, in affecting gonadal sex differentiation in TSD reptiles. Our study has implications for the conservation of TSD reptiles in the context of global change because environmental contaminants may disrupt the activity of THs, and thereby affect offspring sex in TSD reptiles.
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Piferrer, Francesc, and Dafni Anastasiadi. "Do the Offspring of Sex Reversals Have Higher Sensitivity to Environmental Perturbations?" Sexual Development 15, no. 1-3 (2021): 134–47. http://dx.doi.org/10.1159/000515192.
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Sex determination systems in vertebrates vary along a continuum from genetic (GSD) to environmental sex determination (ESD). Individuals that show a sexual phenotype opposite to their genotypic sex are called sex reversals. Aside from genetic elements, temperature, sex steroids, and exogenous chemicals are common factors triggering sex reversal, a phenomenon that may occur even in strict GSD species. In this paper, we review the literature on instances of sex reversal in fish, amphibians, reptiles, birds, and mammals. We focus on the offspring of sex-reversed parents in the instances that they can be produced, and show that in all cases studied the offspring of these sex-reversed parents exhibit a higher sensitivity to environmental perturbations than the offspring of non-sex-reversed parents. We suggest that the inheritance of this sensitivity, aside from possible genetic factors, is likely to be mediated by epigenetic mechanisms such as DNA methylation, since these mechanisms are responsive to environmental cues, and epigenetic modifications can be transmitted to the subsequent generations. Species with a chromosomal GSD system with environmental sensitivity and availability of genetic sex markers should be employed to further test whether offspring of sex-reversed parents have greater sensitivity to environmental perturbations. Future studies could also benefit from detailed whole-genome data in order to elucidate the underlying molecular mechanisms. Finally, we discuss the consequences of such higher sensitivity in the context of global climate change.
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Goikoetxea, Alexander, Erica V. Todd, and Neil J. Gemmell. "Stress and sex: does cortisol mediate sex change in fish?" Reproduction 154, no. 6 (December 2017): R149—R160. http://dx.doi.org/10.1530/rep-17-0408.
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Cortisol is the main glucocorticoid (GC) in fish and the hormone most directly associated with stress. Recent research suggests that this hormone may act as a key factor linking social environmental stimuli and the onset of sex change by initiating a shift in steroidogenesis from estrogens to androgens. For many teleost fish, sex change occurs as a usual part of the life cycle. Changing sex is known to enhance the lifetime reproductive success of these fish and the modifications involved (behavioral, gonadal and morphological) are well studied. However, the exact mechanism behind the transduction of the environmental signals into the molecular cascade that underlies this singular process remains largely unknown. We here synthesize current knowledge regarding the role of cortisol in teleost sex change with a focus on two well-described transformations: temperature-induced masculinization and socially regulated sex change. Three non-mutually exclusive pathways are considered when describing the potential role of cortisol in mediating teleost sex change: cross-talk between GC and androgen pathways, inhibition of aromatase expression and upregulation ofamh(the gene encoding anti-Müllerian hormone). We anticipate that understanding the role of cortisol in the initial stages of sex change will further improve our understanding of sex determination and differentiation across vertebrates, and may lead to new tools to control fish sex ratios in aquaculture.
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Wedekind, Claus. "Demographic and genetic consequences of disturbed sex determination." Philosophical Transactions of the Royal Society B: Biological Sciences 372, no. 1729 (July 31, 2017): 20160326. http://dx.doi.org/10.1098/rstb.2016.0326.
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During sex determination, genetic and/or environmental factors determine the cascade of processes of gonad development. Many organisms, therefore, have a developmental window in which their sex determination can be sensitive to, for example, unusual temperatures or chemical pollutants. Disturbed environments can distort population sex ratios and may even cause sex reversal in species with genetic sex determination. The resulting genotype–phenotype mismatches can have long-lasting effects on population demography and genetics. I review the theoretical and empirical work in this context and explore in a simple population model the role of the fitness v yy of chromosomally aberrant YY genotypes that are a consequence of environmentally induced feminization. Low v yy is mostly beneficial for population growth. During feminization, low v yy reduces the proportion of genetic males and hence accelerates population growth, especially at low rates of feminization and at high fitness costs of the feminization itself (i.e. when feminization would otherwise not affect population dynamics much). When sex reversal ceases, low v yy mitigates the negative effects of feminization and can even prevent population extinction. Little is known about v yy in natural populations. The available models now need to be parametrized in order to better predict the long-term consequences of disturbed sex determination. This article is part of the themed issue ‘Adult sex ratios and reproductive decisions: a critical re-examination of sex differences in human and animal societies’.
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Li, Hong, Clare E. Holleley, Melanie Elphick, Arthur Georges, and Richard Shine. "The behavioural consequences of sex reversal in dragons." Proceedings of the Royal Society B: Biological Sciences 283, no. 1832 (June 15, 2016): 20160217. http://dx.doi.org/10.1098/rspb.2016.0217.
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Sex differences in morphology, physiology, and behaviour are caused by sex-linked genes, as well as by circulating sex-steroid levels. Thus, a shift from genotypic to environmental sex determination may create an organism that exhibits a mixture of male-like and female-like traits. We studied a lizard species (Central Bearded Dragon, Pogona vitticeps ), in which the high-temperature incubation of eggs transforms genetically male individuals into functional females. Although they are reproductively female, sex-reversed dragons (individuals with ZZ genotype reversed to female phenotype) resemble genetic males rather than females in morphology (relative tail length), general behaviour (boldness and activity level), and thermoregulatory tactics. Indeed, sex-reversed ‘females’ are more male-like in some behavioural traits than are genetic males. This novel phenotype may impose strong selection on the frequency of sex reversal within natural populations, facilitating rapid shifts in sex-determining systems. A single period of high incubation temperatures (generating thermally induced sex reversal) can produce functionally female individuals with male-like (or novel) traits that enhance individual fitness, allowing the new temperature-dependent sex-determining system to rapidly replace the previous genetically based one.
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Xiong, Yang, Shuai Wang, Jian-Fang Gui, and Jie Mei. "Artificially induced sex-reversal leads to transition from genetic to temperature-dependent sex determination in fish species." Science China Life Sciences 63, no. 1 (November 28, 2019): 157–59. http://dx.doi.org/10.1007/s11427-019-1568-7.
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Driscoll, Rose M. H., Josh J. Faber-Hammond, Cynthia F. O'Rourke, Peter L. Hurd, and Suzy C. P. Renn. "Epigenetic regulation of gonadal and brain aromatase expression in a cichlid fish with environmental sex determination." General and Comparative Endocrinology 296 (September 2020): 113538. http://dx.doi.org/10.1016/j.ygcen.2020.113538.
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Kitano, T., K. Takamune, T. Kobayashi, Y. Nagahama, and SI Abe. "Suppression of P450 aromatase gene expression in sex-reversed males produced by rearing genetically female larvae at a high water temperature during a period of sex differentiation in the Japanese flounder (Paralichthys olivaceus)." Journal of Molecular Endocrinology 23, no. 2 (October 1, 1999): 167–76. http://dx.doi.org/10.1677/jme.0.0230167.
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The phenotypic sex of many teleost fishes including flounders can be experimentally altered by treating embryos or larvae with varied temperatures or sex-steroid hormones. To analyse the sex determination mechanism, especially the role of cytochrome P450 aromatase (P450arom), an enzyme that catalyses the conversion of androgens to estrogens, in temperature-dependent gonadal sex differentiation in the Japanese flounder, we generated two populations of larvae, both having XX (genetic females) but each growing up to display all phenotypic females or males, by rearing the larvae at normal (18 degrees C) or high (27 degrees C) water temperatures from days 30 to 100 after hatching respectively. The larvae (XX) were produced artificially by mating normal females (XX) with gynogenetic diploid males (XX) which had been sex-reversed to phenotypic males by 17alpha-methyltestosterone. To study the role of P450arom in sex determination in the flounder, we first isolated a P450arom cDNA containing the complete open reading frame from the ovary. RT-PCR showed that P450arom mRNA was highly expressed in the ovary and spleen but weakly in the testis and brain. Semi-quantitative analyses of P450arom mRNA in gonads during sex differentiation showed that there was no difference in the levels of P450arom mRNA between the female and male groups when the gonad was sexually indifferent (day 50 after hatching). However, after the initiation of sex differentiation (day 60), the mRNA levels increased rapidly in the female group, whereas they decreased slightly in the male group. Similarly, estradiol-17beta levels rose remarkably in the female group, yet remained constant in the male group. These results suggest that induction of sex reversal of genetically female larvae to phenotypic males by rearing them at a high water temperature caused a suppression of P450arom gene expression. Furthermore, we suggest that the maintenance of P450arom mRNA at very low levels is a prerequisite for testicular differentiation, while the increased levels are indispensable for ovarian differentiation.
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Veyrunes, Frederic, Pascale Chevret, Josette Catalan, Riccardo Castiglia, Johan Watson, Gauthier Dobigny, Terence J. Robinson, and Janice Britton-Davidian. "A novel sex determination system in a close relative of the house mouse." Proceedings of the Royal Society B: Biological Sciences 277, no. 1684 (December 9, 2009): 1049–56. http://dx.doi.org/10.1098/rspb.2009.1925.
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Therian mammals have an extremely conserved XX/XY sex determination system. A limited number of mammal species have, however, evolved to escape convention and present aberrant sex chromosome complements. In this study, we identified a new case of atypical sex determination in the African pygmy mouse Mus minutoides , a close evolutionary relative of the house mouse. The pygmy mouse is characterized by a very high proportion of XY females (74%, n = 27) from geographically widespread Southern and Eastern African populations. Sequencing of the high mobility group domain of the mammalian sex determining gene Sry , and karyological analyses using fluorescence in situ hybridization and G-banding data, suggest that the sex reversal is most probably not owing to a mutation of Sry , but rather to a chromosomal rearrangement on the X chromosome. In effect, two morphologically different X chromosomes were identified, one of which, designated X*, is invariably associated with sex-reversed females. The asterisk designates the still unknown mutation converting X*Y individuals into females. Although relatively still unexplored, such an atypical sex chromosome system offers a unique opportunity to unravel new genetic interactions involved in the initiation of sex determination in mammals.
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McCoy, Jessica A., Benjamin B. Parrott, Thomas R. Rainwater, Phillip M. Wilkinson, and Louis J. Guillette. "Incubation history prior to the canonical thermosensitive period determines sex in the American alligator." REPRODUCTION 150, no. 4 (October 2015): 279–87. http://dx.doi.org/10.1530/rep-15-0155.
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Despite the widespread occurrence of environmental sex determination (ESD) among vertebrates, our knowledge of the temporal dynamics by which environmental factors act on this process remains limited. In many reptiles, incubation temperature determines sex during a discrete developmental window just prior to and coincident with the differentiation of the gonads. Yet, there is substantial variation in sex ratios among different clutches of eggs incubated at identical temperatures during this period. Here, we test the hypothesis that temperatures experienced prior to the reported thermosensitive period for alligators (Alligator mississippiensis) can impact how the sex determination system responds to thermal cues later in development. Temperature shift experiments on eggs collected from the field within 24 h of oviposition were employed to decouple various maternal influences from thermal effects, and results demonstrate a previously undefined window of thermosensitivity occurring by stage 15 of embryonic development, six stages earlier than previously reported. We also examine the intrasexual expression of several male- and female-biased genes and show that while male-biased genes display no intrasexual differences, ovarian CYP19A1 (aromatase) transcript abundance differs by approximately twofold depending on thermal exposures experienced at early stages of embryonic development. These findings expand our understanding of the ESD in the alligator and provide the rationale for reevaluation of the temporal dynamics of sex determination in other crocodilians.
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Brown, A. Ross, Stewart F. Owen, James Peters, Yong Zhang, Marta Soffker, Gregory C. Paull, David J. Hosken, M. Abdul Wahab, and Charles R. Tyler. "Climate change and pollution speed declines in zebrafish populations." Proceedings of the National Academy of Sciences 112, no. 11 (March 2, 2015): E1237—E1246. http://dx.doi.org/10.1073/pnas.1416269112.
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Endocrine disrupting chemicals (EDCs) are potent environmental contaminants, and their effects on wildlife populations could be exacerbated by climate change, especially in species with environmental sex determination. Endangered species may be particularly at risk because inbreeding depression and stochastic fluctuations in male and female numbers are often observed in the small populations that typify these taxa. Here, we assessed the interactive effects of water temperature and EDC exposure on sexual development and population viability of inbred and outbred zebrafish (Danio rerio). Water temperatures adopted were 28 °C (current ambient mean spawning temperature) and 33 °C (projected for the year 2100). The EDC selected was clotrimazole (at 2 μg/L and 10 μg/L), a widely used antifungal chemical that inhibits a key steroidogenic enzyme [cytochrome P450(CYP19) aromatase] required for estrogen synthesis in vertebrates. Elevated water temperature and clotrimazole exposure independently induced male-skewed sex ratios, and the effects of clotrimazole were greater at the higher temperature. Male sex ratio skews also occurred for the lower clotrimazole exposure concentration at the higher water temperature in inbred fish but not in outbred fish. Population viability analysis showed that population growth rates declined sharply in response to male skews and declines for inbred populations occurred at lower male skews than for outbred populations. These results indicate that elevated temperature associated with climate change can amplify the effects of EDCs and these effects are likely to be most acute in small, inbred populations exhibiting environmental sex determination and/or differentiation.
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Ribas, Laia, Woei Chang Liew, Noèlia Díaz, Rajini Sreenivasan, László Orbán, and Francesc Piferrer. "Heat-induced masculinization in domesticated zebrafish is family-specific and yields a set of different gonadal transcriptomes." Proceedings of the National Academy of Sciences 114, no. 6 (January 23, 2017): E941—E950. http://dx.doi.org/10.1073/pnas.1609411114.
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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.
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Listyasari, Nurin Aisyiyah, Ardy Santosa, and Achmad Zulfa Juniarto. "SRY-negative in 46, XX Male Testicular DSD: a case report." Journal of Biomedicine and Translational Research 6, no. 3 (December 23, 2020): 97–100. http://dx.doi.org/10.14710/jbtr.v6i3.9088.
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Background: The sex determination process requires distinct signaling pathways to generate either testis or ovaries from the same precursor structures, the primordial gonad. Deviations of this signaling mechanism may result in disorders/differences of sex development (DSD). The 46, XX testicular DSD is a rare genetic condition identified by a discrepancy between genetic and phenotypic sex caused sex reversal syndrome. Case Presentation: We describe the case of a 5 years-old 46, XX boy with ambiguous genitalia. On physical examination he had severe hypospadias, bifid scrotum, micropenis and palpable bilateral testes. Cytogenetic analysis of patient reveals a 46, XX karyotype. Hormonal assay showed low level of FSH, LH and Testosterone and there was no evidence of Mullerian structures based on pelvic imaging. The histopathology of gonadal tissue showed a Leydig cell hyperplasia which gives the impression of Sertoli cell nodule. Polymerase chain reaction (PCR) analysis failed to identify the presence of SRY gene, therefore a diagnosis of 46, XX Testicular DSD with SRY-negative was established. Conclusion: This report presents a rare case of SRY-negative 46, XX Testicular DSD in a boy with ambiguous genitalia. A comprehensive management including clinical, cytogenetic and molecular analyses have indicated that undiscovered genetic or environmental factors needs to be elucidated. It is important to carry out further molecular testing to establish precise diagnosis of DSD and to provide appropriate genetic counseling for patients and their family.
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Jin, Kai, Qisheng Zuo, Jiuzhou Song, Yani Zhang, Guohong Chen, and Bichun Li. "CYP19A1 (aromatase) dominates female gonadal differentiation in chicken (Gallus gallus) embryos sexual differentiation." Bioscience Reports 40, no. 10 (October 2020). http://dx.doi.org/10.1042/bsr20201576.
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Abstract Cytochrome P450 Family 19 SubFamily A member 1 (CYP19A1) gene encodes an aromatase which regulates the sexual differentiation in vertebrates by initiating and maintaining 17β-Estradiol (E2) synthesis. Here, we described the spatiotemporal expression pattern of CYP19A1 and its functional role in the embryonic gonad development in amphoteric chickens (Gallus gallus). Results showed that CYP19A1 exhibited a sexually dimorphic expression pattern in female gonads early at embryonic day 5.5 (HH 28) and robustly expressed within the cytoplasm in ovarian medullas. Most importantly, we induced the gonadal sex reversal by ectopically delivering the aromatase inhibitor (AI) or estradiol (E2) into chicken embryos. To further explore the role of CYP19A1 in chicken embryonic sexual differentiation, we successfully developed an effective method to deliver lentiviral particles with CYP19A1 manipulation into chicken embryos via embryonic intravascular injection. The analysis of interference and overexpression of CYP19A1 provided solid evidences that CYP19A1 is both necessary and sufficient to initiate sex differentiation toward female in chicken embryos. Collectively, this work demonstrates that CYP19A1 is a crucial sex differentiation gene in the embryonic development, which provides a foundation for understanding the mechanism of sex determination and differentiation in chickens.
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Dissanayake, Duminda S. B., Clare E. Holleley, and Arthur Georges. "Effects of natural nest temperatures on sex reversal and sex ratios in an Australian alpine skink." Scientific Reports 11, no. 1 (October 11, 2021). http://dx.doi.org/10.1038/s41598-021-99702-1.
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AbstractAltered climate regimes have the capacity to affect the physiology, development, ecology and behaviour of organisms dramatically, with consequential changes in individual fitness and so the ability of populations to persist under climatic change. More directly, extreme temperatures can directly skew the population sex ratio in some species, with substantial demographic consequences that influence the rate of population decline and recovery rates. In contrast, this is particularly true for species whose sex is determined entirely by temperature (TSD). The recent discovery of sex reversal in species with genotypic sex determination (GSD) due to extreme environmental temperatures in the wild broadens the range of species vulnerable to changing environmental temperatures through an influence on primary sex ratio. Here we document the levels of sex reversal in nests of the Australian alpine three-lined skink (Bassiana duperreyi), a species with sex chromosomes and sex reversal at temperatures below 20 °C and variation in rates of sex reversal with elevation. The frequency of sex reversal in nests of B. duperreyi ranged from 28.6% at the highest, coolest locations to zero at the lowest, warmest locations. Sex reversal in this alpine skink makes it a sensitive indicator of climate change, both in terms of changes in average temperatures and in terms of climatic variability.
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Ehl, Jan, Marie Altmanová, and Lukáš Kratochvíl. "With or Without W? Molecular and Cytogenetic Markers are Not Sufficient for Identification of Environmentally-Induced Sex Reversal in the Bearded Dragon." Sexual Development, March 23, 2021, 1–10. http://dx.doi.org/10.1159/000514195.
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Transitions from environmental sex determination (ESD) to genotypic sex determination (GSD) require an intermediate step of sex reversal, i.e., the production of individuals with a mismatch between the ancestral genotypic and the phenotypic sex. Among amniotes, the sole well-documented transition in this direction was shown in the laboratory in the central bearded dragon, Pogona vitticeps, where very high incubation temperatures led to the production of females with the male-typical (ZZ) genotype. These sex-reversed females then produced offspring whose sex depended on the incubation temperature. Sex-reversed animals identified by molecular and cytogenetic markers were also reported in the field, and their increasing incidence was speculated as a climate warming-driven transition in sex determination. We show that the molecular and cytogenetic markers normally sex-linked in P. vitticeps are also sex-linked in P. henrylawsoni and P. minor, which points to quite ancient sex chromosomes in this lineage. Nevertheless, we demonstrate, based on a crossing experiment with a male bearded dragon who possesses a mismatch between phenotypic sex and genotype, that the used cytogenetic and molecular markers might not be reliable for the identification of sex reversal. Sex reversal should not be considered as the only mechanism causing a mismatch between genetic sex-linked markers and phenotypic sex, which can emerge also by other processes, here most likely by a rare recombination between regions of sex chromosomes which are normally sex-linked. We warn that sex-linked, even apparently for a long evolutionary time, and sex-specific molecular and cytogenetic markers are not a reliable tool for the identification of sex-reversed individuals in a population and that sex reversal has to be verified by other approaches, particularly by observation of the sex ratio of the progeny.
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Dai, Shengfei, Shuangshuang Qi, Xueyan Wei, Xingyong Liu, Yibing Li, Xin Zhou, Hesheng Xiao, Baoyue Lu, Deshou Wang, and Minghui Li. "Germline sexual fate is determined by the antagonistic action of dmrt1 and foxl3/foxl2 in tilapia." Development 148, no. 8 (April 15, 2021). http://dx.doi.org/10.1242/dev.199380.
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ABSTRACT Germline sexual fate has long been believed to be determined by the somatic environment, but this idea is challenged by recent studies of foxl3 mutants in medaka. Here, we demonstrate that the sexual fate of tilapia germline is determined by the antagonistic interaction of dmrt1 and foxl3, which are transcriptionally repressed in male and female germ cells, respectively. Loss of dmrt1 rescued the germ cell sex reversal in foxl3Δ7/Δ7 XX fish, and loss of foxl3 partially rescued germ cell sex reversal but not somatic cell fate in dmrt1Δ5/Δ5 XY fish. Interestingly, germ cells lost sexual plasticity in dmrt1Δ5/Δ5 XY and foxl3Δ7/Δ7 XX single mutants, as aromatase inhibitor (AI) and estrogen treatment failed to rescue the respective phenotypes. However, recovery of germ cell sexual plasticity was observed in dmrt1/foxl3 double mutants. Importantly, mutation of somatic cell-specific foxl2 resulted in testicular development in foxl3Δ7/Δ7 or dmrt1Δ5/Δ5 mutants. Our findings demonstrate that sexual plasticity of germ cells relies on the presence of both dmrt1 and foxl3. The existence of dmrt1 and foxl3 allows environmental factors to influence the sex fate decision in vertebrates.
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Castañeda-Cortés, Diana Carolina, and Juan Ignacio Fernandino. "Stress and sex determination in fish: from brain to gonads." International Journal of Developmental Biology 52 (2020). http://dx.doi.org/10.1387/ijdb.200072jf.
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Fish present remarkable malleability regarding gonadal sex fate. This phenotypic plasticity enables an organism to adapt changes in the environment by responding with different phenotypes. The gonad and the brain present this extraordinary plasticity. These organs are involved in the response to environmental stressors to direct the gonadal fate, inducing sex change or sex reversal in hermaphroditic and gonochoristic fish, respectively. The presence of such molecular and endocrine plasticity gives this group a large repertoire of possibilities against a continuously changing environment, resulting in the highest radiation of reproduction strategies described in vertebrates. In this review, we provide a broad and comparative view of tremendous radiation of sex determination mechanisms to direct gonadal fate. New results have established that the driving mechanism involves early response to environmental stressors by the brain plus high plasticity of gonadal differentiation and androgens as by-products of stress inactivation. In addition to the stress axis, another two major axes – the hypothalamic-pituitary-gonadal axis and the hypothalamic-pituitary-thyroid axis, which are well known to participate in the regulation of reproduction – have been proposed as reinforcing the brain-gonadal interrelationships in the fate of the gonad.
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Catanach, Andrew, Mike Ruigrok, Deepa Bowatte, Marcus Davy, Roy Storey, Noémie Valenza-Troubat, Elena López-Girona, et al. "The genome of New Zealand trevally (Carangidae: Pseudocaranx georgianus) uncovers a XY sex determination locus." BMC Genomics 22, no. 1 (November 2, 2021). http://dx.doi.org/10.1186/s12864-021-08102-2.
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Abstract Background The genetic control of sex determination in teleost species is poorly understood. This is partly because of the diversity of mechanisms that determine sex in this large group of vertebrates, including constitutive genes linked to sex chromosomes, polygenic constitutive mechanisms, environmental factors, hermaphroditism, and unisexuality. Here we use a de novo genome assembly of New Zealand silver trevally (Pseudocaranx georgianus) together with sex-specific whole genome sequencing data to detect sexually divergent genomic regions, identify candidate genes and develop molecular makers. Results The de novo assembly of an unsexed trevally (Trevally_v1) resulted in a final assembly of 579.4 Mb in length, with a N50 of 25.2 Mb. Of the assembled scaffolds, 24 were of chromosome scale, ranging from 11 to 31 Mb in length. A total of 28,416 genes were annotated after 12.8 % of the assembly was masked with repetitive elements. Whole genome re-sequencing of 13 wild sexed trevally (seven males and six females) identified two sexually divergent regions located on two scaffolds, including a 6 kb region at the proximal end of chromosome 21. Blast analyses revealed similarity between one region and the aromatase genes cyp19 (a1a/b) (E-value < 1.00E-25, identity > 78.8 %). Males contained higher numbers of heterozygous variants in both regions, while females showed regions of very low read-depth, indicative of male-specificity of this genomic region. Molecular markers were developed and subsequently tested on 96 histologically-sexed fish (42 males and 54 females). Three markers amplified in absolute correspondence with sex (positive in males, negative in females). Conclusions The higher number of heterozygous variants in males combined with the absence of these regions in females support a XY sex-determination model, indicating that the trevally_v1 genome assembly was developed from a male specimen. This sex system contrasts with the ZW sex-determination model documented in closely related carangid species. Our results indicate a sex-determining function of a cyp19a1a-like gene, suggesting the molecular pathway of sex determination is somewhat conserved in this family. The genomic resources developed here will facilitate future comparative work, and enable improved insights into the varied sex determination pathways in teleosts. The sex marker developed in this study will be a valuable resource for aquaculture selective breeding programmes, and for determining sex ratios in wild populations.
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Zheng, Shuqing, Wenjing Tao, Haowen Yang, Thomas D. Kocher, Zhijian Wang, Zuogang Peng, Li Jin, Deyong Pu, Yaoguang Zhang, and Deshou Wang. "Identification of sex chromosome and sex-determining gene of southern catfish ( Silurus meridionalis ) based on XX, XY and YY genome sequencing." Proceedings of the Royal Society B: Biological Sciences 289, no. 1971 (March 16, 2022). http://dx.doi.org/10.1098/rspb.2021.2645.
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Teleosts are important models to study sex chromosomes and sex-determining (SD) genes because they present a variety of sex determination systems. Here, we used Nanopore and Hi-C technologies to generate a high-contiguity chromosome-level genome assembly of a YY southern catfish ( Silurus meridionalis ). The assembly is 750.0 Mb long, with contig N50 of 15.96 Mb and scaffold N50 of 27.22 Mb. We also sequenced and assembled an XY male genome with a size of 727.2 Mb and contig N50 of 13.69 Mb. We identified a candidate SD gene through comparisons to our previous assembly of an XX individual. By resequencing male and female pools, we characterized a 2.38 Mb sex-determining region (SDR) on Chr24. Analysis of read coverage and comparison of the X and Y chromosome sequences showed a Y specific insertion (approx. 500 kb) in the SDR which contained a male-specific duplicate of amhr2 (named amhr2y ). amhr2y and amhr2 shared high-nucleotide identity (81.0%) in the coding region but extremely low identity in the promotor and intron regions. The exclusive expression in the male gonadal primordium and loss-of-function inducing male to female sex reversal confirmed the role of amhr2y in male sex determination. Our study provides a new example of amhr2 as the SD gene in fish and sheds light on the convergent evolution of the duplication of AMH/AMHR2 pathway members underlying the evolution of sex determination in different fish lineages.
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Zerpa-Catanho, Dessireé, Jennifer Wai, Ming Li Wang, Li’ang Yu, Julie Nguyen, and Ray Ming. "Differential gene expression among three sex types reveals a MALE STERILITY 1 (CpMS1) for sex differentiation in papaya." BMC Plant Biology 19, no. 1 (December 2019). http://dx.doi.org/10.1186/s12870-019-2169-0.
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Abstract Background Carica papaya is a trioecious plant species with a genetic sex-determination system defined by sex chromosomes. Under unfavorable environmental conditions male and hermaphrodite exhibit sex-reversal. Previous genomic research revealed few candidate genes for sex differentiation in this species. Nevertheless, more analysis is still needed to identify the mechanism responsible for sex flower organ development in papaya. Results The aim of this study was to identify differentially expressed genes among male, female and hermaphrodite flowers in papaya during early (pre-meiosis) and later (post-meiosis) stages of flower development. RNA-seq was used to evaluate the expression of differentially expressed genes and RT-qPCR was used to verify the results. Putative functions of these genes were analyzed based on their homology with orthologs in other plant species and their expression patterns. We identified a Male Sterility 1 gene (CpMS1) highly up-regulated in male and hermaphrodite flower buds compared to female flower buds, which expresses in small male flower buds (3–8 mm), and that might be playing an important role in male flower organ development due to its homology to MS1 genes previously identified in other plants. This is the first study in which the sex-biased expression of genes related to tapetum development in the anther developmental pathway is being reported in papaya. Besides important transcription factors related to flower organ development and flowering time regulation, we identified differential expression of genes that are known to participate in ABA, ROS and auxin signaling pathways (ABA-8-hydroxylases, AIL5, UPBEAT 1, VAN3-binding protein). Conclusions CpMS1 was expressed in papaya male and hermaphrodite flowers at early stages, suggesting that this gene might participate in male flower organ development processes, nevertheless, this gene cannot be considered a sex-determination gene. Due to its homology with other plant MS1 proteins and its expression pattern, we hypothesize that this gene participates in anther development processes, like tapetum and pollen development, downstream gender specification. Further gene functional characterization studies in papaya are required to confirm this hypothesis. The role of ABA and ROS signaling pathways in papaya flower development needs to be further explored as well.