Maternally derived sex steroid hormones impact sex ratios of loggerhead sea turtles (original) (raw)

Incubation Temperature Influences Sex-Steroid Levels in Juvenile Red-Eared Slider Turtles, Trachemys scripta, a Species with Temperature-Dependent Sex Determination1

Biology of Reproduction, 1999

Incubation temperature determines gonadal sex in the redeared slider turtle, Trachemys scripta. However, little is known about the long-term effects of incubation temperature on traits other than gonadal sex in this species. To investigate the hypothesis that incubation temperature (independent of gonadal sex) influences sex steroid levels after hatching, we incubated eggs of the red-eared slider turtle at three temperatures (26, 28.6, and 31؇C). We then measured plasma levels of dihydrotestosterone, estradiol, progesterone, and testosterone in 6-wkold males from 26؇C and 28.6؇C eggs, and in 6-wk-old females from 28.6؇C and 31؇C eggs. We found that dihydrotestosterone levels were not influenced by incubation temperature or gonadal sex. However, progesterone levels were significantly higher in males from 26؇C eggs than in males from 28.6؇C eggs. In contrast, testosterone levels did not differ between males from 26؇C versus males from 28.6؇C eggs, but they were significantly higher in females from 28.6؇C than in females from 31؇C eggs. Progesterone and testosterone levels did not differ between males and females from 28.6؇C eggs. Temperature also influenced estradiol levels in both sexes, but the effects were enigmatic. We conclude that incubation temperature has lasting effects on sex steroid levels even after hatching.

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.

Key parameters describing temperature-dependent sex determination in the southernmost population of loggerhead sea turtles

All marine turtles have temperature-dependent sex determination (TSD), and there is mounting evidence that climate change has increased sand temperatures at some rookeries, leading to pronounced biases in hatchling sex ratios. Quantification of the variation in the key parameters that describe TSD will be essential to our ability to predict the adaptive capacity of marine turtles, and for implementing conservation programs where necessary. Here we integrate field and laboratory data on the embryonic development of a little-studied population of loggerhead turtles (Caretta caretta, Linnaeus 1758) from Western Australia, which is home to a large rookery at the southernmost limit of the species' global range. We determined that the pivotal temperature that produces an equal sex ratio was 29.0°C, centred within a transitional range of temperatures of 0.67°C where both sexes are produced. For the first time for a marine turtle, embryonic development rates were modelled with a nonlinear function, and were used to define the start and end of the thermosensitive period, where bipotential gonads differentiate into testes or ovaries. The period where gonads were sensitive to a masculinizing trigger occurred between 33 and 64% of development. In general, the TSD parameters for this southernmost population of C. caretta were similar to those estimated for other loggerhead populations, reinforcing previous findings that sex determination thresholds and processes are highly conserved.

Estimating sex ratios in Caribbean hawksbill turtles: testosterone levels and climate effects

Aquatic Biology, 2013

Evolutionary theory predicts that male and female offspring should be produced at a 1:1 ratio, but this may rarely be the case for species in which sex is determined during incubation by temperature, such as marine turtles. Estimates of primary sex ratio suggest that marine turtle sex ratios are highly skewed, with up to 9 females per male. We captured juvenile hawksbill turtles Eretmochelys imbricata in waters around Anegada, British Virgin Islands, a regionally important foraging aggregation, and analysed concentrations of plasma testosterone and oestradiol-17β from 62 turtles to estimate sex ratio. There were 2.4 to 7.7 times more females than males. Testosterone concentrations correlated with sampling date and sea surface temperature (SST), with higher con centrations in the late summer when SST was highest, suggesting that assigning sex through threshold values of sex hormones must be carried out cautiously. The sex ratio in the juvenile foraging aggregation around Anegada is more male biased than at other locations, suggesting that turtles at Anegada have resilience against feminising effects of climate change. Future work should (1) integrate the relative contributions of different genetic stocks to foraging aggregations and (2) investigate the annual and seasonal cycles of sex hormones, and differences among individuals and life history stages.

Thyroid hormone modulates offspring sex ratio in a turtle with temperature-dependent sex determination

Proceedings. Biological sciences, 2016

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 (T3), during embryonic development (by adding excess T3 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 consis...

A review of how the biology of male sea turtles may help mitigate female-biased hatchling sex ratio skews in a warming climate

Marine Biology

In a warming climate, male sea turtles may become increasingly rare due to temperature-dependent sex determination with females being produced at warmer temperatures. Hence there is widespread concern that a lack of adult males may impact population viability. However, there is controversy over this scenario and here we review aspects of the biology of male sea turtles that will help mitigate female-biased hatchling sex ratios. In particular, there is strong evidence that males generally breed more frequently than females (i.e. have a shorter remigration interval) and that individual breeding males actively search for females and may mate with multiple females from different nesting sites. These aspects of the biology of male turtles will cause female-biased hatchling sex ratios to translate into more balanced adult sex ratios on the breeding grounds (i.e. operational sex ratios). Sexual dimorphism is widespread with adult male turtles generally being smaller than females. In freshw...

Embryonic sex steroid hormones accumulate in the eggshell of loggerhead sea turtle (Caretta caretta

Steroids hormones such as estradiol-17b (E2) and testosterone (T) are involved in gonadal differentiation of oviparous animals with temperature-dependent sex determination (TSD), and are greatly distributed. This hypothesizes that these embryonic steroid hormones probably accumulate in the eggshell throughout blood or/and chorioallantoic fluid in sea turtle species with TSD, producing females at higher temperature. To demonstrate this hypothesis, concentrations of E2 and T in the blood plasma from the hatchling loggerhead sea turtle (Caretta caretta) and in their eggshells were measured by radioimmunoassay. In the present study we propose that both concentrations of E2 and T in the blood plasma are correlated with amounts of these sex steroids in the eggshell. Moreover, contents of E2 in the eggshell showed a significant positive correlation with mean incubation temperatures during a thermosensitive period in the experimental nests, whereas T contents in the eggshell did not. Taken together, these findings indicated that embryonic E2 and T that accumulated in the eggshell can be extracted and measured. Furthermore, the present study suggested that contents of E2 in the eggshell may differ between male and female, and monitoring of these steroids is a useful method to identify the sex of loggerhead sea turtle hatchling.

Sex-determining potencies vary among female incubation temperatures in a turtle

Journal of Experimental Zoology, 1990

Reptiles whose sex is determined by incubation temperature typically exhibit all-male or all-female sex ratios over a wide range of incubation temperatures. The question arises as to whether the various all-female temperatures (or the various all-male temperatures) are equivalent in their “potency,” or capacity to effect female determination. In map turtles, warm incubation temperatures produce all females and cool ones produce all males. We compared sex determining potencies of two all-female temperatures, 31°C and 32.5°C, by incubating eggs first at a male-producing temperature (26°C) and then shifting them to the warm temperatures. The resulting sex ratio was significantly more male biased in the 26°C31°C shift than in the 26°C32.5°C shift, indicating that 32.5°C has the greater female potency. These results point to the possibility that sex determination depends on a quantitative rather than qualitative level of gene expression.

Temperature-dependent sex determination in the Kemp’s ridley sea turtle: effects of incubation temperatures on sex ratios

Endangered Species Research, 2012

This study provides the most comprehensive evaluation to date of the temperature range that produces mixed sex ratios as well as the temperature that produces a 1:1 sex ratio (denoted 1:1 temperature in the following) in the Kemp's ridley sea turtle Lepidochelys kempii. We analyzed temperature data from Padre Island National Seashore (PAIS), Texas (USA). Using 2006 to 2008 PAIS sex ratio data sorted by mean temperature, which fluctuated minimally in this study, we found a 1:1 temperature of 30.0°C utilizing the Hill distribution model. The upper limit of the temperature range that was estimated to produce mixed sex ratios was 32.5°C; the lower end could not be determined. These values are in the upper range of those reported for other sea turtle species, except the olive ridley. The Kemp's ridley temperature-dependent sex determination parameters described here can be used to predict sex ratios from nests with known incubation temperatures in order to help manage the recovery of this species.