Exogenous estradiol alters gonadal growth and timing of temperature sex determination in gonads of sea turtle (original) (raw)
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Seminars in Cell & Developmental Biology, 2009
The developmental processes underlying gonadal differentiation are conserved across vertebrates, but the triggers initiating these trajectories are extremely variable. The red-eared slider turtle (Trachemys scripta elegans) exhibits temperature-dependent sex determination (TSD), a system where incubation temperature during a temperature-sensitive period of development determines offspring sex. However, gonadal sex is sensitive to both temperature and hormones during this period -particularly estrogen. We present a model for temperature-based differences in aromatase expression as a critical step in ovarian determination. Localized estrogen production facilitates ovarian development while inhibiting male-specific gene expression. At male-producing temperatures aromatase is not upregulated, thereby allowing testis development.
Sexual Development, 2007
ER ␣ and AR levels spike at the female-producing temperature while ovarian sex is determined, but none of the receptors exhibited sexually dimorphic localization within the gonad prior to morphological differentiation. All three receptors respond differentially to sex-reversing treatments. When shifted to female-producing temperatures, embryos maintain ER ␣ and AR expression while ER  is reduced. When shifted to male-producing temperatures, medullary expression of all three receptors is reduced. Feminization via es tradiol (E 2 ) treatment at a male-producing temperature profoundly changed the expression patterns for all three receptors. ER ␣ and ER  redirected to the cortex in E 2 -created ovaries, while AR medullary expression was transiently reduced. Although warmer incubation temperature and estrogen result in the same endpoint (ovarian development), our results indicate different steroid signaling patterns between temperature-and estrogen-induced feminization.
Synergism between temperature and estradiol: A common pathway in turtle sex determination?
Journal of Experimental Zoology, 1991
In many reptiles, the temperature at which the eggs are incubated determines the sex of the hatchlings. Administration of estradiol will counteract the masculinizing effects of a male-producing temperature, resulting in female hatchlings. To address whether temperature and estrogen are biologically equivalent, two experiments were conducted with the red-eared slider turtle, Trachemys scripta. In the first experiment, varying dosages of estrogen were administered at Stage 17 (the middle of the temperature-sensitive window) to eggs maintained at two temperatures, 26°C (which normally produces all males) and 28.2"C (which produces mostly males but lies at the threshold of the transition from male-to female-producing temperatures). Results indicate that estrogen and temperature exert a synergistic effect on sex determination. In the second experiment, estrogen was administered at different stages of embryonic development. The results indicate an estrogen-sensitive period ranging from Stage 14 through Stage 21, a period similar to the temperature-sensitive period for this species. The results of these experiments are consistent with the hypothesis that temperature and estradiol act in a common pathway in temperature-dependent sex determination.
Differentiation, 1993
Gonadal differentiation associated with estrogen-induced female sex determination was examined in a turtle with temperature-dependent sex determination, and was compared to ovarian differentiation at a female-producing temperature. Freshly ladi eggs of the red-eared slider, Trachemys scripta, were incubated at a male-producing temperature (26 degrees C) and were experimentally manipulated at one of three embryonic stages: stage 15, 17, or 20 (i.e. early, midway, or late in the temperature-sensitive and estrogen-sensitive periods). At those developmental stages, groups of eggs were either: (1) treated with a control solution (95% ethanol) and placed back at the male-producing temperature, (2) treated with 10 micrograms of estradiol-17 beta and placed back at the male-producing temperature, or (3) shifted to a female-producing temperature (31 degrees C). Additionally, a control group of freshly laid eggs was continually incubated at 31 degrees C throughout embryonic development. To examine morphological events occurring after the treatments, a subset of embryos from each group was examined at the time of the treatment and at 1-2 stage intervals following the treatments. The results indicate that estradiol-17 beta as well as female-producing temperature may ensure female sex determination by facilitating medullary cord regression. Further, the results reveal a chronology of differentiation in which medullary cord regression temporally precedes cortical proliferation.
General and Comparative Endocrinology, 1997
Reptile embryos with temperature sex determination have a thermosensitive period (TSP). The finding that exogenous estradiol (E2) overcomes the effect of malepromoting temperature led to the idea that temperature may regulate estrogen concentration in the gonad during TSP. Since interspecific variations in TSP and in the effect of exogenous E2 exist, we undertook a study in the olive ridley Lepidochelys olivacea. Four parameters were correlated: the TSP (time dimension), the thermosensitive stages (rate of development), gonad development (histological aspect), and the estradiol response. Two kinds of experiments were performed: (1) Eggs were shifted once, at different stages of development, from a male-promoting temperature to a female-temperature (or vice versa) for the remainder of development. (2) Eggs at male-promoting temperature were treated once with 6 or 12 mg of estradiol (E2) at various times of incubation. Sex ratio was established around hatching in each experimental series. We found that the temporal dimension of the TSP was around 7 days (Days 20-27 of incubation) at a male-promoting or a female-promoting temperature. The rate of development of the whole embryo and gonadal growth was faster at femalepromoting temperature than at male-promoting temperature. Formation of the genital ridge began at stage 21-22 and histological differentiation of the gonads occurred around stage 26-27. Although these stages coincided with the TSP, at male-promoting temperature the thermo-sensitive stages occurred earlier (from stages 20-21 to stages 23-24) than at female-promoting temperature (from stages 23-24 to stages 26-27). Thus, at male promoting-temperature, sex was determined in embryos with incipient or undifferentiated gonads. In contrast, E2 treatment continued to feminize the gonads of embryos at a male-promoting temperature beyond the TSP up to stage 25-26, but the E2-induced ovaries were significantly smaller than temperature-induced ovaries. It is suggested that the doses of E2 used were higher than the concentration of endogenous E2 required for normal sex determination. The lack of correlation between sex determination and gonad differentiation suggests that irreversible molecular processes underlying sex determination occur earlier at male-than at female-promoting temperature. Results suggest that the male sex may be the default state and that the female condition must be imposed upon it. r 1997 Academic Press Sexual differentiation of the gonads is dependent on incubation temperature in five sea turtle species: Eretmochelys imbricata , Lepidochelys olivacea Caretta caretta Mrosovsky, 1980, 1982), Chelonia mydas Limpus, 1980, Morreale et al., 1982), and Dermochelys coriacea . Pivotal temperatures (temperature during incubation at constant temperature which gives 50% individuals of each sexual
Differentiation, 2007
Many egg-laying reptiles have temperaturedependent sex determination (TSD), where the offspring sex is determined by incubation temperature during a temperature-sensitive period (TSP) in the middle third of development. The underlying mechanism transducing a temperature cue into an ovary or testis is unknown, but it is known that steroid hormones play an important role. During the TSP, exogenous application of estrogen can override a temperature cue and produce females, while blocking the activity of aromatase (Cyp19a1), the enzyme that converts testosterone to estradiol, produces males from a female-biased temperature. The production of estrogen is a key step in ovarian differentiation for many vertebrates, including TSD reptiles, and temperature-based differences in aromatase expression during the TSP may be a critical step in ovarian determination. Steroidogenic factor-1 (Sf1) is a key gene in vertebrate sex determination and regulates many steroidogenic enzymes, including aromatase. We find that Sf1 and aromatase are differentially expressed during sex determination in the red-eared slider turtle, Trachemys scripta elegans. Sf1 is expressed at higher levels during testis development while aromatase expression increases during ovary determination. We also assayed Sf1 and aromatase response to sex-reversing treatments via temperature or the modulation of estrogen availability. Sf1 expression was redirected to low-level female-specific patterns with feminizing temperature shift or exogenous estradiol application and redirected to more intense male-specific patterns with male-producing temperature shift or inhibition of aromatase activity. Conversely, aromatase expression was redirected to more intense female-specific patterns with female-producing treatment and redirected toward diffuse low-level male-specific patterns with masculinizing sex reversal. Our data do not lend support to a role for Sf1 in the regulation of aromatase expression during slider turtle sex determination, but do support a critical role for estrogen in ovarian development.
The Journal of Experimental Zoology, 1998
Although temperature sex determination is well known in several reptile species, the physiological mechanism underlying this process remains to be elucidated. In the current work, we analyzed the levels of testosterone (T) and estradiol (E2) in the gonads; two brain regions-telencephalon (Te) and diencephalon/mesencephalon (Di)-and the serum of developing embryos of the olive ridley Lepidochelys olivacea incubated at male-or female-promoting temperatures. Conversion of pregnenolone (P5) to T and T to E2 were studied in the gonads and brain. The analyses were performed during three periods: the thermosensitive period (TSP), histologically undifferentiated gonads (UDG), and differentiated gonads (DG). In the gonads, serum, and brain, T concentrations were higher at the female-promoting temperature during the three periods, whereas in the gonads and serum, E2 levels were similar at the female and male-promoting temperature. In Di, the concentration of E2 was significantly higher at the female-promoting temperature. Biotransformation of P5 to T in gonadal tissues were slightly higher at the femalepromoting temperature in TSP and increased during UDG and DG. Conversion of T to E2, however, was similar at the two temperatures during the three periods. In the brain, the Di showed a higher efficiency for transforming T to E2 at the female-promoting temperature. Our present results do not allow us to decide whether the diencephalon is the cause or the effect, but they conclusively demonstrate that, in L. olivacea, this region of the brain senses temperature during sex determination.
KEYWORDS Estradiol, gonad development, temperature sex determination, turtle, fadrozole, fulvestrant HIGHLIGHTS 1. Estradiol levels regulate cell proliferation pattern of the medullary cords. 2. Fadrozole and fulvestrant delay the remodeling of the medullary cords in ovary 3. Estrogen levels are involved in the sex fate of medullary cords ABSTRACT In turtles undergoing temperature sex determination (TSD), bipotential gonads express Sox9 in medullary cords at both female-(FPT) and male-producing temperatures (MPT). Subsequently, when the sex fate of medullary cords becomes dimorphic, at FPT, Sox9 is downregulated, whereas at MPT, its expression is maintained. Medullary cords in the ovary turn into ovarian lacuna, whereas in the testis they differentiate as seminiferous cords. When embryos of Lepidochelys olivacea sea turtle are incubated at MPT and treated with estradiol, Sox9 expression persists in the medullary cords in the form of tiny ovotestis-like formations. The perturbed development of the treated gonads is due to a significant decrease in the number of proliferating cells. This suggests that the disturbed effect caused by exogenous estradiol may be due to a conflict between the gene networks regulated by temperature and the increased level of endogenous estrogens, induced by the treatment. Here, we decided to use fadrozole and fulvestrant, an aromatase inhibitor and an estrogen-receptor antagonist, respectively, to provide insights into the role played by endogenous estrogens in regulating the cell proliferation of the two main gonadal compartments: the medullary cords and the cortex. Comparing cell proliferation patterns, our current results suggest that the endogenous estrogens are involved in determining the sex fate of medullary cords, by repressing proliferation.
Molecular and Cellular Mechanisms Underlying Temperature-Dependent Sex Determination in Turtles
Sexual Development, 2021
The discovery in mammals that fetal testes are required in order to develop the male phenotype inspired research efforts to elucidate the mechanisms underlying gonadal sex determination and differentiation in vertebrates. A pioneer work in 1966 that demonstrated the influence of incubation temperature on sexual phenotype in some reptilian species triggered great interest in the environment’s role as a modulator of plasticity in sex determination. Several chelonian species have been used as animal models to test hypotheses concerning the mechanisms involved in temperature-dependent sex determination (TSD). This brief review intends to outline the history of scientific efforts that corroborate our current understanding of the state-of-the-art in TSD using chelonian species as a reference.
Correlation among Thermosensitive Period, Estradiol Response, and Gonad …
General and …, 1997
Reptile embryos with temperature sex determination have a thermosensitive period (TSP). The finding that exogenous estradiol (E2) overcomes the effect of male-promoting temperature led to the idea that temperature may regulate estrogen concentration in the gonad during ...