Temperature and non-aromatizable androgens: a common pathway in male sex determination in a turtle with temperature-dependent sex determination?

1996 ◽  
Vol 149 (3) ◽  
pp. 457-463 ◽  
Author(s):  
D Crews ◽  
A R Cantú ◽  
J M Bergeron
Keyword(s):  
Sex Determination ◽  
Incubation Temperature ◽  
Sensitive Period ◽  
Temperature Sensitive ◽  
Temperature Dependent ◽  
Dose Response Relationship ◽  
Common Pathway ◽  
Slider Turtle ◽  
Male Sex ◽  
Incubation Temperatures

Abstract This study addressed the hypothesis that, in the red-eared slider turtle, Trachemys scripta, non-aromatizable androgens are the physiological equivalent of temperature in determining male development. In the first experiment, eggs were treated in the middle of the temperature-sensitive period with 1·0 or 10·0 μg androsterone, 5α-dihydrotestosterone, 3α-androstanediol, or 3β-androstanediol, while at an all-male, male-biased, or one of two female-biased incubation temperatures. In the second experiment, eggs were treated with the same dosages of dihydrotestosterone at different stages of embryonic development while at a male-biased, threshold, or a female-biased incubation temperature. Results of experiment one indicated that hormone-induced masculinization is specific to non-aromatizable androgens. Results of experiment two indicated that the sensitivity to dihydrotestosterone corresponds to the temperature-sensitive window during development. Further, there is a dose–response relationship but no apparent synergism between exogenous dihydrotestosterone and incubation temperature. When considered with other research, it is suggested that non-aromatizable androgens and their products are involved in the initiation of male sex determination whereas oestrogens and their aromatizable androgen precursors are involved in the initiation of female sex determination. Journal of Endocrinology (1996) 149, 457–463

Role of reductase and aromatase in sex determination in the red-eared slider (Trachemys scripta), a turtle with temperature-dependent sex determination

1994 ◽  
Vol 143 (2) ◽  
pp. 279-289 ◽  
Author(s):  
D Crews ◽  
J M Bergeron
Keyword(s):  
Sex Determination ◽  
Aromatase Inhibitors ◽  
Incubation Temperature ◽  
Combined Treatment ◽  
Female Offspring ◽  
Male Offspring ◽  
Temperature Dependent ◽  
Slider Turtle ◽  
Dose Dependent Fashion ◽  
Incubation Temperatures

Abstract In many turtles the temperature during the middle of incubation determines the gonadal sex of the hatchling. In the red-eared slider turtle (Trachemys scripta), an incubation temperature of 26 °C results in all male offspring, whereas an incubation temperature of 31 °C results in all female offspring; at temperatures intermediate to these (e.g. 29, 29·2, 29·4 °C) a mixed sex ratio is obtained. Administration of exogenous oestrogens will overcome the effects of an all-male producing incubation temperature to cause female sex determination, whereas administration of exogenous dihydrotestosterone (DHT) or testosterone to eggs incubating at an all-female temperature will have no discernible effect. Administration of DHT will cause male sex determination only if administered at intermediate incubation temperatures whereas administration of testosterone to eggs incubating at all male-producing and male-biased intermediate temperatures results in a significant number of female offspring, an effect presumably due to aromatization of testosterone to oestradiol (OE2), Since testosterone serves as the precursor to both DHT and OE2, being metabolized by reductase and aromatase respectively, three experiments were conducted to determine whether various putative reductase and aromatase inhibitors would overcome the effect of incubation temperature. First, while administration of testosterone to eggs incubating at all male-producing and male-biased intermediate temperatures produced females in a dose- and temperature-dependent manner, significant numbers of intersex individuals resulted from high dosage testosterone treatment to eggs incubating at a female-biased intermediate temperature. The reductase inhibitors 4MA and MK906 were capable of producing female offspring if administered at intermediate temperatures, but not in a dose-dependent fashion. Administration of the aromatase inhibitors CGS16949A and CGS20267 resulted in male offspring at both female-biased intermediate and at all female-producing temperatures in a dose-dependent fashion. Second, similar findings were obtained with combined doses of testosterone and reductase or aromatase inhibitors. Combined treatment of eggs at male-biased intermediate incubation temperatures with testosterone and reductase inhibitor resulted in female hatchlings, whereas combined treatment of testosterone and aromatase inhibitor at both female-biased intermediate and at all female-producing temperatures resulted in male hatchlings. Finally, treatment with reductase inhibitor and aromatase inhibitor combined resulted in only male offspring at all incubation temperatures with the exception of the all-female incubation temperature; in the latter instance almost all offspring were female. These studies indicate that in the red-eared slider turtle (i) male and female sex determination are independent cascades residing equally in each individual and regulated by incubation temperature, (ii) steroid hormones are involved in temperature-dependent sex determination, and (iii) testosterone plays a pivotal role in this process. The data also suggest that aromatase and oestrogen receptors may be involved in the initiation of an ovary determining cascade and that reductase and androgen receptors may be involved in the initiation of a testis determining cascade. Journal of Endocrinology (1994) 143, 279–289

scholarly journals Improved genome assembly of American alligator genome reveals conserved architecture of estrogen signaling

2016 ◽  
Author(s):  
Edward S. Rice ◽  
Satomi Kohno ◽  
John St. John ◽  
Son Pham ◽  
Jonathan Howard ◽  
...  
Keyword(s):  
Sex Determination ◽  
Genome Assembly ◽  
Critical Period ◽  
Incubation Temperature ◽  
Current Model ◽  
Alligator Mississippiensis ◽  
Estrogen Signaling ◽  
Sensitive Period ◽  
Temperature Sensitive ◽  
American Alligator

AbstractThe American alligator, Alligator mississippiensis, like all crocodilians, has temperature-dependent sex determination, in which the sex of an embryo is determined by the incubation temperature of the egg during a critical period of development. The lack of genetic differences between male and female alligators leaves open the question of how the genes responsible for sex determination and differentiation are regulated. One insight into this question comes from the fact that exposing an embryo incubated at male-producing temperature to estrogen causes it to develop ovaries. Because estrogen response elements are known to regulate genes over long distances, a contiguous genome assembly is crucial for predicting and understanding its impact.We present an improved assembly of the American alligator genome, scaffolded with in vitro proximity ligation (Chicago) data. We use this assembly to scaffold two other crocodilian genomes based on synteny. We perform RNA sequencing of tissues from American alligator embryos to find genes that are differentially expressed between embryos incubated at male-versus female-producing temperature. Finally, we use the improved contiguity of our assembly along with the current model of CTCF-mediated chromatin looping to predict regions of the genome likely to contain estrogen-responsive genes. We find that these regions are significantly enriched for genes with female-biased expression in developing gonads after the critical period during which sex is determined by incubation temperature. We thus conclude that estrogen signaling is a major driver of female-biased gene expression in the post-temperature sensitive period gonads.

The temperature-sensitive period (TSP) during incubation of broad-snouted caiman (Caiman latirostris) eggs

2007 ◽  
Vol 28 (1) ◽  
pp. 123-128 ◽  
Author(s):  
Carlos Piña ◽  
Alejandro Larriera ◽  
Pablo Siroski ◽  
Luciano Verdade ◽  
Valentine Lance
Keyword(s):  
Sex Determination ◽  
Egg Laying ◽  
Alligator Mississippiensis ◽  
Sensitive Period ◽  
Temperature Sensitive ◽  
American Alligator ◽  
Temperature Dependent ◽  
The Many

AbstractAll crocodiles studied to date exhibit temperature-dependent sex determination. During the many weeks from egg laying to hatch there is a period of 10 to 15 d in the middle third of incubation (in the American alligator) during which the sex of the embryo is irreversibly fixed, referred to as the temperature-sensitive period or TSP. In this work we investigated the TSP in Caiman latirostris eggs incubated at female-inducing and male-inducing temperatures (29° C and 33° C respectively) by switching eggs from 29° C to 33° C and vice versa at timed interval throughout incubation. Compared to Alligator mississippiensis the duration of TSP was longer, and the onset of TSP was at an earlier stage of incubation.

Sex-specific effects of developmental temperature on morphology, growth and survival of offspring in a lizard with temperature-dependent sex determination

2020 ◽  
Vol 130 (2) ◽  
pp. 320-335
Author(s):  
Ariel L Steele ◽  
Daniel A Warner
Keyword(s):  
Sex Determination ◽  
Incubation Temperature ◽  
Adaptive Significance ◽  
Similar Reaction ◽  
Temperature Dependent ◽  
Growth And Survival ◽  
Specific Effects ◽  
Offspring Sex ◽  
Males And Females ◽  
Incubation Temperatures

Abstract The developmental environment plays a pivotal role in shaping fitness-relevant phenotypes of all organisms. Phenotypes are highly labile during embryogenesis, and environmental factors experienced early in development can have profound effects on fitness-relevant traits throughout life. Many reptiles exhibit temperature-dependent sex determination (TSD), whereby temperature during embryonic development permanently determines offspring sex. The leading hypothesis for the adaptive significance of TSD posits that egg incubation temperature differentially affects the fitness of males vs. females so that each sex is produced at its optimal temperature. The goal of this research is to address this hypothesis by quantifying the sex-specific effects of incubation temperature on phenotypes and survival in a lizard (Agama picticauda) with TSD. By incubating eggs under constant and fluctuating temperatures, we demonstrated that incubation temperature affects fitness-relevant phenotypes in A. picticauda; but males and females had similar reaction norms. However, females produced from female-biased incubation temperatures had greater survival than those from male-biased temperatures, and male survival was lowest for individuals produced from a female-biased temperature. In addition, eggs incubated at male-biased temperatures hatched earlier than those incubated at female-biased temperatures, which may have sex-specific consequences later in life as predicted by models for the adaptive significance of TSD.

scholarly journals Brief exposure to warm temperatures reduces intron retention in Kdm6b in a species with temperature-dependent sex determination

2021 ◽  
Vol 17 (6) ◽  
pp. 20210167
Author(s):  
Rosario A. Marroquín-Flores ◽  
Rachel M. Bowden ◽  
Ryan T. Paitz
Keyword(s):  
Sex Determination ◽  
Incubation Temperature ◽  
Developmental Process ◽  
Intron Retention ◽  
Thermal Conditions ◽  
Temperature Sensitive ◽  
Temperature Dependent ◽  
Specific Expression ◽  
Male And Female ◽  
Thermal Variability

Animals with temperature-dependent sex determination (TSD) respond to thermal cues during early embryonic development to trigger gonadal differentiation. TSD has primarily been studied using constant temperature incubations, where embryos are exposed to constant male- or female-producing temperatures, and these studies have identified genes that display sex-specific expression in response to incubation temperature. Kdm6b , a histone demethylase gene, has received specific attention as it is among the initial genes to respond to incubation temperature and is necessary for testis development. Interestingly, Kdm6b retains an intron when eggs are incubated at a constant male-producing temperature, but the role of thermal variability in this developmental process is relatively understudied. Species with TSD regularly experience thermal cues that fluctuate between male- and female-producing temperatures throughout development but it is unclear how Kdm6b responds to such variable temperatures. In this study, we investigate temperature-sensitive splicing in Kdm6b by exposing embryos to male- and female-producing thermal conditions. We show a rapid decrease in levels of the intron retaining transcript of Kdm6b upon exposure to female-producing conditions. These results demonstrate that, under ecologically relevant conditions, temperature-sensitive splicing can differentially regulate genes critical to TSD.

scholarly journals A simple model for the evolution of temperature-dependent sex determination explains the temperature sensitivity of embryonic mortality in imperiled reptiles

2019 ◽  
Author(s):  
Lauren Lawson ◽  
Njal Rollinson
Keyword(s):  
Sex Ratio ◽  
Sex Determination ◽  
Constant Temperature ◽  
Incubation Temperature ◽  
Embryonic Mortality ◽  
Conservation Strategy ◽  
Temperature Sensitive ◽  
Temperature Dependent ◽  
High Quality ◽  
Species Specific

AbstractA common reptile conservation strategy involves artificial incubation of embryos and release of hatchlings or juveniles into wild populations. Temperature-dependent sex determination (TSD) occurs in most chelonians, permitting conservation managers to bias sex ratios towards females by incubating embryos at high temperatures, ultimately allowing the introduction of more egg-bearing individuals into populations. Here, we revisit classic sex allocation theory and hypothesize that TSD evolved in some reptile groups (specifically, chelonians and crocodilians) because male fitness is more sensitive to condition (general health, vigor) than female fitness. It follows that males benefit more than females from incubation environments that confer high-quality phenotypes, and hence high-condition individuals. We predict that female-producing temperatures, which comprise relatively high incubation temperatures in chelonians and crocodilians, are relatively stressful for embryos and subsequent life stages. We synthesize data from 28 studies to investigate how constant temperature incubation affects embryonic mortality in chelonians with TSD. We find several lines of evidence suggesting that female-producing temperatures, especially relatively warm temperatures, are more stressful than male-producing temperatures, and we find some evidence that pivotal temperatures (TPiv, the temperature that produces a 1:1 sex ratio) exhibit a correlated evolution with embryonic thermal tolerance. If patterns of temperature-sensitive embryonic mortality are also indicative of chronic thermal stress that occurs post hatching, then conservation programs may benefit from incubating eggs close to species-specific TPivs, thus avoiding high-temperature incubation. Indeed, our models predict that, on average, a sex ratio of more than 75% females can generally be achieved by incubating eggs only 1°C above TPiv. Of equal importance, we provide insight into the enigmatic evolution of TSD in chelonians, by providing support to the hypothesis that TSD evolution is related to the quality of the phenotype conferred by incubation temperature, with males produced in high-quality incubation environments.Lay summaryWe analyze data on embryonic mortality under constant-temperature incubation for 15 species of chelonians with temperature-dependent sex determination (TSD). Mortality is lowest near species-specific pivotal temperatures (Tpiv) but increases rapidly above TPiv, consistent with a theory that explains the adaptive significance of TSD. Conservation managers should incubate embryos near TPiv.

scholarly journals Is Thermal Responsiveness Affected by Maternal Estrogens in Species with Temperature-Dependent Sex Determination?

2021 ◽  
pp. 1-11
Author(s):  
Rachel M. Bowden ◽  
Ryan T. Paitz
Keyword(s):  
Sex Determination ◽  
Ovarian Development ◽  
Thermal Fluctuations ◽  
Gonadal Differentiation ◽  
Temperature Dependent ◽  
Slider Turtle ◽  
Expression Of Genes ◽  
High Responsiveness ◽  
Incubation Temperatures ◽  
Thermal Responsiveness

In species with temperature-dependent sex determination (TSD), incubation temperatures regulate the expression of genes involved in gonadal differentiation and determine whether the gonads develop into ovaries or testes. For most species, natural incubation conditions result in transient exposure to thermal cues for both ovarian and testis development, but how individuals respond to this transient exposure varies and can drive variation in the resulting sex ratios. Here, we argue that variation in the timing to respond to temperature cues, or thermal responsiveness, is a trait needing further study. Recent work in the red-eared slider turtle (<i>Trachemys scripta</i>) has found that when embryos experience transient exposure to warm conditions (i.e., heatwaves), some embryos show high responsiveness, requiring only short exposures to commit to ovarian development, while others show low responsiveness, developing testes even after more extended exposures to warm conditions. We discuss how maternal estrogens might influence thermal responsiveness for organisms that develop under thermal fluctuations. Examining the interplay of molecular responses to more subtle thermal and endocrine environments may reveal significant insights into the process of sex determination in species with TSD.

scholarly journals Molecular and Cellular Mechanisms Underlying Temperature-Dependent Sex Determination in Turtles

2021 ◽  
pp. 1-9
Author(s):  
Horacio Merchant-Larios ◽  
Verónica Díaz-Hernández ◽  
Diego Cortez
Keyword(s):  
Animal Models ◽  
Sex Determination ◽  
Incubation Temperature ◽  
State Of The Art ◽  
Current Understanding ◽  
Temperature Dependent ◽  
Cellular Mechanisms ◽  
Male Phenotype ◽  
History Of ◽  
Reptilian Species

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.

scholarly journals Effects of constant incubation regimes on eggs and hatchlings of the egg-laying skink, Oligosoma suteri

2021 ◽  
Author(s):  
◽  
Kelly Maree Hare
Keyword(s):  
Hatching Success ◽  
Incubation Temperature ◽  
Unit Length ◽  
Condition Index ◽  
Egg Laying ◽  
Maternal Influence ◽  
Temperature Dependent ◽  
Sprint Speed ◽  
Fitness Traits ◽  
Incubation Temperatures

<p>The conditions under which reptilian eggs are incubated affect survival probability and physiological attributes of the progeny. The egg-laying skink, Oligosoma suteri, is the only endemic oviparous lizard in New Zealand. No controlled laboratory incubation had previously been undertaken, and thus no information was available on the requirements for successful captive incubation. I studied the effects of incubation regime on the eggs and hatchlings of O. suteri to four months of age. Oligosoma suteri eggs (n = 174) were randomly distributed among three constant incubation temperatures (18°C, 22°C and 26°C) and two water potentials (-120 kPa and -270 kPa). Hatching success and hatchling survival were greatest at 22°C and 26°C, with hatchlings from 18°C incubation suffering from physical abnormalities. Incubation regime and maternal influence did not affect sex of individuals, with equal sex ratios occurring from each incubation treatment. Hatchlings from the 22°C and -120 kPa incubation treatments were larger, for most measurements, and warmer incubation temperatures resulted in increased growth rates. Juveniles from 22°C and 26°C and individuals with greater mass per unit length (condition index) sprinted faster over 0.25 m. Sprint speed was positively correlated with ambient temperature. At four months of age sprint speed decreased in 18°C individuals and individuals incubated at 26°C and -270 kPa compared to their performance at one month. The results suggest that the most successful captive incubation regime for O. suteri is 22°C and -120 kPa. This study also shows that temperature-dependent sex determination does not occur in O. suteri, but that fitness traits are influenced by incubation temperature.</p>

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