Temperature-Sensitive Period of Sex Determination in the Atlantic Silverside, Menidia menidia

1986 ◽  
Vol 43 (3) ◽  
pp. 514-520 ◽  
Author(s):  
David O. Conover ◽  
Mark H. Fleisher

We investigated the timing and duration of the temperature-sensitive period of development in the Atlantic silverside, Menidia menidia, by measuring the sex ratio in groups of larvae shifted reciprocally among low and high temperatures as development progressed. The sensitive period of sex determination was dependent on body size, rather than age, and occurred during the middle to later stages of larval development when fish were between 8 and 21 mm in total length. Sex determination was irreversibly fixed earlier in development (i.e. at 15 mm in length) at higher than at lower temperatures. Higher, male-producing temperatures therefore appear to more strongly effect sex determination than do lower, female-producing temperatures. Temperature prior to, or after, the sensitive period had no measurable effect on sex ratio. From histological examination we suggest that gonad differentiation coincided with the end of the temperature-sensitive period. The timing and duration of the temperature-sensitive period in M. menidia is generally similar to the hormone-sensitive period identified in other fishes. Both phenomena reveal a specific developmental period during which the course of primary sex differentiation in fishes is labile.

The various patterns of environmental sex determination in squamates, chelonians and crocodilians are described. High temperatures produce males in lizards and crocodiles but females in chelonians. Original experiments on the effects of incubation at 30 °C (100% females) or 33 °C (100% males) on development in Alligator mississippiensis are described. These include an investigation of the effect of exposing embryos briefly to a different incubation temperature on the sex ratio at hatching, and a study of the effects of 30 °C and 33 °C on growth and development of alligator embryos and gonads. A 7-day pulse of one temperature on the background of another was insufficient to alter the sex ratio dramatically. Incubation at 33 °C increased the rate of growth and development of alligator embryos. In particular, differentiation of the gonad at 33 °C was enhanced compared with 30 °C. A hypothesis is developed to explain the mechanism of temperature-dependent sex determination (TSD) in crocodilians. The processes of primary sex differentiation are considered to involve exposure to a dose of some male-determining factor during a specific quantum of developmental time during early incubation. The gene that encodes for the male- determining factor is considered to have an optimum temperature (33 °C). Any change in the temperature affects the expression o f this gene and affects the dose or quantum embryos are exposed to. In these cases there is production of females by default. The phylogenetic implications of TSD for crocodilians, and reptiles in particular, are related to the life history of the animal from conception to sexual maturity. Those animals that develop under optimal conditions grow fastest and largest and become male. A general association between the size of an animal and its sex is proposed for several types of vertebrate.


2016 ◽  
Author(s):  
Edward S. Rice ◽  
Satomi Kohno ◽  
John St. John ◽  
Son Pham ◽  
Jonathan Howard ◽  
...  

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.


1989 ◽  
Vol 67 (5) ◽  
pp. 1279-1284 ◽  
Author(s):  
J. Servan ◽  
P. Zaborski ◽  
M. Dorizzi ◽  
C. Pieau

Adult sex ratio in the turtle Emys orbicularis was determined in populations from seven ponds in Brenne (Indre, France). In all populations, the sex ratio was biased toward females. Among 290 captured animals, the male:female ratio was close to 0.5. Among different demographic factors that could affect the adult sex ratio, the most influential was probably the sex ratio of hatchlings. In Emys orbicularis, a ZZ male/ZW female system of genotypic sex determination has been postulated. Moreover, gonad differentiation is dependent on temperature and sex-reversed individuals can occur. To evaluate the importance of sex reversal among adult females, the blood of 78 animals was typed for the serologically detectable H-Y antigen, used as a tool to identify sexual genotype. In 73 of them, the H-Y phenotype was positive, conforming with female genotype, but in the other 5 females, it was negative (as in genotypic males), revealing that the sexual phenotype of these animals had been inverted. As the percentage of these sex-reversed genotypic males is low, the influence of temperature would appear not to be the sole cause of the observed unbalanced sex ratio. The female bias can be partly explained by the interaction of temperature with the ZZ/ZW system of genotypic sex determination. Indeed, in this system, sexual inversion under the influence of an epigenetic factor increases the ratio of genotypic females (ZW and WW) in the progeny.


2007 ◽  
Vol 28 (1) ◽  
pp. 123-128 ◽  
Author(s):  
Carlos Piña ◽  
Alejandro Larriera ◽  
Pablo Siroski ◽  
Luciano Verdade ◽  
Valentine Lance

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.


2016 ◽  
Vol 283 (1841) ◽  
pp. 20161206 ◽  
Author(s):  
Bao-Jun Sun ◽  
Teng Li ◽  
Yi Mu ◽  
Jessica K. McGlashan ◽  
Arthur Georges ◽  
...  

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.


1996 ◽  
Vol 149 (3) ◽  
pp. 457-463 ◽  
Author(s):  
D Crews ◽  
A R Cantú ◽  
J M Bergeron

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


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