Estrogen and sex reversal in turtles: A dose-dependent phenomenon

doi:10.1016/0016-6480(91)90162-Y

General and Comparative Endocrinology

Volume 81, Issue 3, March 1991, Pages 357-364

https://doi.org/10.1016/0016-6480(91)90162-Y Get rights and content

Abstract

Exogenous estradiol benzoate (EB) or estradiol-17β (E2) caused dose-dependent gonadal feminization of slider turtle (Trachemys scripta) embryos incubated at a male-producing temperature (26°), suggesting that sex reversal requires a threshold dosage of these hormones. Even at dosages resulting in mixtures of males and females, nearly all hatchlings had normal-appearing ovaries or testes. Only 7 of 241 hatchlings had gonads that had not differentiated fully into ovaries or testes. Thus, with rare exception, estrogens exerted an “all or none” effect. The transport of hormone into the embryo varied with mode of administration and E2 was more effective than was EB at the lowest dosage used. These studies suggest either that exogenous estrogen is capable of coordinating cortical/medullary development in the gonad so that intersexes are prevented or that estrogen acts “upstream” of the developmental processes responsible for coordinating gonadal development.

References (32)

J.J. Bull et al.
Sex reversal by estradiol in three reptilian orders
Gen. Comp. Endocrinol
(1988)
D. Crews et al.
Action of sex steroid hormones on temperature-induced sex determination in the snapping turtle (Chelydra serpentina)
Gen. Comp. Endocrinol
(1989)
W.H.N. Gutzke et al.
Steroid hormones reverse sex in turtles
Gen. Comp. Endocrinol
(1986)
W.H.N. Gutzke et al.
Sensitive periods during embryogeny for hormonally induced sex in turtles
Gen. Comp. Endocrinol
(1988)
R. Maraud et al.
Structure of the right testis of sexually mature genetically female fowl experimentally masculinized during embryonic life and submitted to a post-hatching left castration
Gen. Comp. Endocrinol
(1987)
A. van Tienhoven
A method of “controlling sex” by dipping eggs in hormone solutions
Poult. Sci
(1957)
E. Witschi et al.
Steroid hormones at early development stages of vertebrates
Gen. Comp. Endocrinol
(1962)
T. Yamamoto
Hormonic factors affecting gonadal sex differentiation in fish
Gen. Comp. Endocrinol
(1962)
J. Benoit
Transformation expérimentale de sexes par ovarïectomie précoce chez la poule domestique
C.R. Acad. Sci
(1923)
J. Benoit
Differentiation sexualle chez les O seaux au cours du développement normal et de l'intersexualité experimentale par ovariectomie
Arch. Anat. Microsc. Morphol. Exp
(1950)

A.J. Billy et al.

The effects of sex steroid treatments on sexual differentiation in a unisexual lizard, Cnemidophorus uniparens (Teiidae)

J. Morphol

(1986)

J.J. Bull

Temperature-dependent sex determination in reptiles: Validity of sex diagnosis in hatchling lizards

Canad. J. Zool

(1987)

J.J. Bull et al.

Temperature-dependent sex determination in turtles

Science

(1979)

J.J. Bull et al.

Sex determining temperatures in turtles: A geographic comparison

Evolution

(1982)

R.K. Burns

Experimental reversal of sex in the gonads of the oppossum, Didelphys virginiana

R.K. Burns

Hormone vs. constitutional factors in the growth of embryonic sex primordia in the oppossum

Amer. J. Anat

(1956)

Cited by (158)

Higher temperatures directly increase germ cell number, promoting feminization of red-eared slider turtles
2023, Current Biology
In many reptile species, gonadal sex is affected by environmental temperature during a critical period of embryonic development—a process known as temperature-dependent sex determination (TSD).¹ The oviparous red-eared slider turtle, Trachemys scripta, has a warm-female/cool-male TSD system and is among the best-studied members of this group.² When incubated at low temperatures, the somatic cells of the bipotential gonad differentiate into Sertoli cells, the support cells of the testis, whereas at high temperatures, they differentiate into granulosa cells, the support cells of the ovary.³ Here, we report the unexpected finding that temperature independently affects the number of primordial germ cells (GCs) in the embryonic gonad at a time before somatic cell differentiation has initiated. Specifically, embryos incubated at higher, female-inducing temperatures have more GCs than those incubated at the male-inducing temperature. Furthermore, elimination of GCs in embryos incubating at intermediate temperatures results in a strong shift toward male-biased sex ratios. This is the first evidence that temperature affects GC number and the first evidence that GC number influences sex determination in amniotes. This observation has two important implications. First, it supports a new model in which temperature can impact sex determination in incremental ways through multiple cell types. Second, the findings have important implications for a major unresolved question in the fields of ecology and evolutionary biology—the adaptive significance of TSD. We suggest that linking high GC number with female development improves female reproductive potential and provides an adaptive advantage for TSD.
Effects of agricultural pesticides on the reproductive system of aquatic wildlife species, with crocodilians as sentinel species
2020, Molecular and Cellular Endocrinology
Citation Excerpt :
In this sense, several researchers have found that the administration of 17β-Estradiol (E2) during the thermosensitive period overrides the effects of the male incubation temperature, producing phenotypic females in Trachemys scripta, Alligator mississippiensis, and C. latirostris, among other species (Crain et al., 1997; Crews et al., 1996; Milnes et al., 2002; Stoker et al., 2003). This effect has been defined as sex reversal or estrogen-induced sex determination (Canesini et al., 2018; Crews et al., 1991a; Crews et al., 1991b; Holleley et al., 2016; Tousignant and Crews, 1994; Wibbels et al., 1992). The role of estrogens in sex determination is important to be evaluated because it is known that most EDCs exhibit estrogenic activity and are classified as xenoestrogens (Sonnenschein and Soto, 1998).
Agricultural pesticides represent a significant class of endocrine-disrupting chemicals (EDCs) to which non-target organisms around the world are constantly exposed. Laboratory studies have found strong evidence showing the endocrine-disruptive potential of these pesticides at environmentally relevant exposure levels. Since the field of endocrine disruption continues to grow in richness and complexity, this review aims to provide an update on the effects of two agricultural pesticides that act as EDCs: atrazine and endosulfan. We will focus mainly on the effects on crocodilians due to their worldwide occurrence in tropical and sub-tropical wetland ecosystems and their ecological and physiological features, which render them vulnerable to exposure to pesticides with endocrine-disrupting action at all life stages. The results here reviewed provide important insights into the effects of hormonally active agricultural pesticides at cellular, tissue, and organ levels in the reproductive system of crocodiles. A better understanding of the effects of exposure to environmentally relevant doses of EDCs on the reproductive system of crocodilians will contribute to protect and improve the health of both wildlife species and humans.
Mechanisms related to sexual determination by temperature in reptiles
2019, Journal of Thermal Biology
A number of strategies have emerged that appear to relate to the evolution of mechanisms for sexual determination in vertebrates, among which are genetic sex determination caused by sex chromosomes and environmental sex determination, where environmental factors influence the phenotype of the sex of an individual. Within the reptile group, some orders such as: Chelonia, Crocodylia, Squamata and Rhynchocephalia, manifest one of the most intriguing and exciting environmental sexual determination mechanisms that exists, comprising temperature-dependent sex determination (TSD), where the temperature of incubation that the embryo experiences during its development is fundamental to establishing the sex of the individual. This makes them an excellent model for the study of sexual determination at the molecular, cellular and physiological level, as well as in terms of their implications at an evolutionary and ecological level. There are different hypotheses concerning how this process is triggered and this review aims to describe any new contributions to particular TSD hypotheses, analyzing them from the “eco-evo-devo” perspective.
Learning and behavior in hatchling Trachemys scripta exposed to bisphenol-a during embryonic development
2019, Physiology and Behavior
Steroids play an integral role in orchestrating embryonic development, and they can affect a suite of phenotypic traits, including learning and behavior. Endocrine disrupting compounds (EDCs) can alter steroid-dependent phenotypic traits during embryonic development. Bisphenol-A (BPA) is an EDC that disrupts the action of estrogen, and recent work indicates that BPA can affect learning and behavior similarly to estrogen. We exposed red-eared slider turtle (Trachemys scripta) eggs to BPA during embryonic development and tested hatchlings for effects on learning and behavior in modified T-mazes over the course of two weeks. We found that behavioral patterns changed within a day and over the course of the experiment, but we found no effect of BPA treatment. Further, we found that hatchling turtles were highly consistent in their behaviors. These behaviors varied among individuals, suggesting that there are discrete behavioral types in T. scripta hatchlings. The highly repetitive nature of behaviors in the hatchlings might explain the innate biases that we observed and warrants further study.
Role for androgens in determination of ovarian fate in the common snapping turtle, Chelydra serpentina
2019, General and Comparative Endocrinology
Sex steroids are involved in sex determination in almost all vertebrates, including species with temperature-dependent sex determination (TSD). It is well established that aromatase and estrogens are involved in ovary determination in TSD species. In contrast, the role of non-aromatizable androgens in TSD is less clear. In this study, we used dihydrotestosterone (DHT) and an antagonist of the mammalian androgen receptor (flutamide) to examine the impact of androgens on sex determination in the snapping turtle. We incubated eggs at a male-producing temperature and treated embryos with drug delivery vehicle (5 L ethanol), DHT in vehicle, or flutamide in vehicle during the sex-determining period. We then measured expression of markers for ovarian and testicular development and genes involved in steroidogenesis. A subset of embryos and hatchlings were collected for histological analysis of gonad differentiation and sex determination. DHT and flutamide both induced ovarian development: 100% of vehicle-treated hatchlings had testes, while 60% of DHT-treated and 32% flutamide-treated hatchlings had ovaries. DHT and flutamide treatments also had feminizing effects on gene expression patterns and the structure of embryonic gonads. DHT treatment increased expression of FoxL2, androgen receptor, aromatase and several steroidogenic genes. Flutamide produced a similar, but weaker, pattern of gene expression. Genes involved in testis development (Sox9 and Amh) were influenced by flutamide treatment. Our findings support the hypothesis that androgens and the androgen receptor are involved in ovary determination in the common snapping turtle.
The external genitalia in juvenile Caiman latirostris differ in hormone sex determinate-female from temperature sex determinate-female
2019, General and Comparative Endocrinology
The broad-snouted caiman (Caiman latirostris) is a crocodilian species that inhabits South American wetlands. As in all other crocodilians, the egg incubation temperature during a critical thermo-sensitive window (TSW) determines the sex of the hatchlings, a phenomenon known as temperature-dependent sex determination (TSD). In C. latirostris, we have shown that administration of 17-β-estradiol (E₂) during the TSW overrides the effect of the male-producing temperature, producing phenotypic females (E₂SD-females). Moreover, the administration of E₂ during TSW has been proposed as an alternative way to improve the recovery of endangered reptile species, by skewing the population sex ratio to one that favors females. However, the ovaries of E₂SD-female caimans differ from those of TSD-females. In crocodilians, the external genitalia (i.e. clitero-penis structure or phallus) are sexually dimorphic and hormone-sensitive. Despite some morphological descriptions aimed to facilitate sexing, we found no available data on the C. latirostris phallus histoarchitecture or hormone dependence. Thus, the aims of this study were: (1) to establish the temporal growth pattern of the phallus in male and female caimans; (2) to evaluate histo-morphological features and the expression of estrogen receptor alpha (ERα) and androgen receptor (AR) in the phallus of male and female pre-pubertal juvenile caimans; and (3) to determine whether the phallus of TSD-females differs from the phallus of E₂SD-females. Our results demonstrated sexually dimorphic differences in the size and growth dynamics of the caiman external genitalia, similarities in the shape and spatial distribution of general histo-morphological compartments, and sexually dimorphic differences in innervation, smooth muscle fiber distribution, collagen organization, and ERα and AR expressions. The external genitalia of E₂SD-females differed from that of TSD-females in many histological features and in the expression of ERα and AR, resembling patterns described in males. Our results alert on the effects of estrogen agonist exposure during TSW and suggest that caution must be taken regarding the use of E₂SD as a procedure for wildlife population management.

View all citing articles on Scopus

View full text

Estrogen and sex reversal in turtles: A dose-dependent phenomenon

Abstract

Gen. Comp. Endocrinol

Gen. Comp. Endocrinol

Gen. Comp. Endocrinol

Gen. Comp. Endocrinol

Gen. Comp. Endocrinol

Poult. Sci

Gen. Comp. Endocrinol

Gen. Comp. Endocrinol

Transformation expérimentale de sexes par ovarïectomie précoce chez la poule domestique

C.R. Acad. Sci

Differentiation sexualle chez les O seaux au cours du développement normal et de l'intersexualité experimentale par ovariectomie

Arch. Anat. Microsc. Morphol. Exp

The effects of sex steroid treatments on sexual differentiation in a unisexual lizard, Cnemidophorus uniparens (Teiidae)

J. Morphol

Temperature-dependent sex determination in reptiles: Validity of sex diagnosis in hatchling lizards

Canad. J. Zool

Temperature-dependent sex determination in turtles

Science

Sex determining temperatures in turtles: A geographic comparison

Evolution

Experimental reversal of sex in the gonads of the oppossum, Didelphys virginiana

Hormone vs. constitutional factors in the growth of embryonic sex primordia in the oppossum

Amer. J. Anat