Correlation among Thermosensitive Period, Estradiol Response, and Gonad … (original) (raw)
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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
Developmental Biology, 2015
Temperature sex determining species offer a model for investigating how environmental cues become integrated to the regulation of patterning genes and growth, among bipotential gonads. Manipulation of steroid hormones has revealed the important role of aromatase in the regulation of the estrogen levels involved in temperature-dependent sex determination. Estradiol treatment counteracts the effect of male-promoting temperature, but the resulting ovarian developmental pattern differs from that manifested with the female-promoting temperature. Hypoplastic gonads have been reported among estradiol-treated turtles; however the estradiol effect on gonadal size has not been examined. Here we focused on the sea turtle Lepidochelys olivacea, which develops hypoplastic gonads with estradiol treatment. We studied the effect of estradiol on cell proliferation and on candidate genes involved in ovarian pattern. We found this effect is organ specific, causing a dramatic reduction in gonadal cell proliferation during the temperature-sensitive period. Although the incipient gonads resembled tiny ovaries, remodeling of the medullary cords and down-regulation of testicular factor Sox9 were considerably delayed. Contrastingly, with ovarian promoting temperature as a cue, exogenous estradiol induced the upregulation of the ovary factor FoxL2, prior to the expression of aromatase. The strong expression of estrogen receptor alpha at the time of treatment suggests that it mediates estradiol effects. Overall results indicate that estradiol levels required for gonadal growth and to establish the female genetic network are delicately regulated by temperature.
Journal of Herpetology, 2007
Estrogens and estrogen mimics can affect offspring sex ratios in a wide variety of animal species including Leopard Geckos, Eublepharis macularius, a species with temperature-dependent sex determination (TSD). Estrogens can disrupt effects of temperature on sex determination by feminizing or sex-reversing embryos incubated at male-producing temperatures. Estrogens may have paradoxical effects at different incubation temperatures and in different concentrations. In this study, E. macularius eggs were exposed to ethanol, estradiol benzoate, or estradiol 17b at the beginning of the thermosensitive period when sex determination occurs. Eggs were treated and incubated at each of three incubation temperatures known to produce varying primary sex ratios. At a male-producing incubation temperature, estrogen-treated groups produced more females than negative control groups. This result has been reported in other TSD reptiles. In our study, we showed that at a female-producing incubation temperature, estrogen-treated groups produced significantly more males than negative control groups. This is the first report of its kind in which a TSD reptile was shown to produce significantly more males at a female-producing temperature. Our results suggest a complex feedback relationship between aromatase and cofactors during the thermosensitive period of egg incubation in E. macularius. Expected effects of exogenous estrogens on contaminant-exposed wildlife populations may differ depending on nest-site temperatures.
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.
Journal of Experimental Zoology Part A: Ecological Genetics and Physiology, 2009
A brief review of our current understanding (or lack of understanding) of the molecular basis of temperature-dependent sex determination (TSD) in reptiles is presented. Current theories are discussed: yolk steroids as sex determinants, the brain as the driver for TSD and the enzyme aromatase and estrogen production as the possible determinants of sex. There is little evidence to support the first two theories, but enough evidence to keep the third theory in play. As yet, however, we have no molecular understanding of how a two-degree difference in temperature during the temperature-sensitive phase of egg incubation can initiate the molecular cascade that determines whether the indifferent gonad develops as an ovary or a testis.
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.
General and comparative …, 1996
triol treatment also resulted in cranially hypertrophied In many turtles the temperature during the middle of oviducts at all incubation temperatures in a dose-depenincubation determines the gonadal sex of the hatchling. dent manner, whereas animals treated with estradiol-Sex steroid hormones have been implicated in tempera-17b and estrone had normal oviducts. These results supture-dependent sex determination in the red-eared slider port the hypothesis that estrogens are involved in the turtle, Trachemys scripta; nonaromatizable androgens final common pathway of female sex determination in are involved in male sex determination and estrogens this species. ᭧ 1996 Academic Press, Inc. and aromatizable androgens in female sex determination. Administration of exogenous estradiol-17b to eggs incubating at a temperature that normally produces only In many reptiles gonadal sex is determined by the males can overcome the effect of temperature and result temperature of the incubating egg, a process known as in all offspring being female. Further, estradiol-17b and temperature-dependent sex determination (TSD). In the incubation temperature synergize to produce a greater red-eared slider turtle (Trachemys scripta), incubation of feminizing effect at intermediate incubation temperaeggs at relatively low temperatures (e.g., 20 -28.6Њ) retures that produce mixed sex ratios. This study demonsults in only male hatchlings, whereas relatively high strates that, in the red-eared slider, there is a complex temperatures (e.g., 29.6 -35Њ) results in only female interaction between incubation temperature, different hatchlings; when eggs are incubated at temperatures estrogens, and the dosage effect of each hormone. There intermediate to these, varying sex ratios are produced are changes in potency of different estrogens with incu- . Sex steroid hormones appear to be bation temperature such that estriol is more potent than the physiological equivalent of incubation temperature estrone and estradiol-17b at 26Њ (an all-male producing and both male-and female-producing incubation temincubation temperature), estrone and estriol are equipoperatures and exogenous steroids exert their effects tent to each other and more potent than estradiol-17b at during the mid-trimester of development (Crews et al., . Estrogens and aromatizable biased sex ratio), and estradiol-17b is more potent than androgens induce female sex determination, whereas estrone and estriol at 29Њ (an incubation temperature nonaromatizable androgens induce male sex determithat produced equal numbers of males and females).
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.
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.