Sex and Incubation Temperature Independently Affect Embryonic Development and Offspring Size in a Turtle with Temperature-Dependent Sex Determination

2020 ◽  
Vol 93 (1) ◽  
pp. 62-74 ◽  
Author(s):  
Daniel A. Warner ◽  
Timothy S. Mitchell ◽  
Brooke L. Bodensteiner ◽  
Fredric J. Janzen
Keyword(s):  
Embryonic Development ◽  
Sex Determination ◽  
Incubation Temperature ◽  
Offspring Size ◽  
Temperature Dependent

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 Population viability at extreme sex-ratio skews produced by temperature-dependent sex determination

2017 ◽  
Vol 284 (1848) ◽  
pp. 20162576 ◽  
Author(s):  
Graeme C. Hays ◽  
Antonios D. Mazaris ◽  
Gail Schofield ◽  
Jacques-Olivier Laloë
Keyword(s):  
Sex Determination ◽  
High Mortality ◽  
Egg Production ◽  
Incubation Temperature ◽  
Sea Turtles ◽  
Sex Ratios ◽  
Population Viability ◽  
Temperature Dependent ◽  
Population Extinction ◽  
The World

For species with temperature-dependent sex determination (TSD) there is the fear that rising temperatures may lead to single-sex populations and population extinction. We show that for sea turtles, a major group exhibiting TSD, these concerns are currently unfounded but may become important under extreme climate warming scenarios. We show how highly female-biased sex ratios in developing eggs translate into much more balanced operational sex ratios so that adult male numbers in populations around the world are unlikely to be limiting. Rather than reducing population viability, female-biased offspring sex ratios may, to some extent, help population growth by increasing the number of breeding females and hence egg production. For rookeries across the world ( n = 75 sites for seven species), we show that extreme female-biased hatchling sex ratios do not compromise population size and are the norm, with a tendency for populations to maximize the number of female hatchlings. Only at extremely high incubation temperature does high mortality within developing clutches threaten sea turtles. Our work shows how TSD itself is a robust strategy up to a point, but eventually high mortality and female-only hatchling production will cause extinction if incubation conditions warm considerably in the future.

scholarly journals Temperature-Dependent Sex Determination and Artificial Incubation of Tuatara, Sphenodon Punctatus

2021 ◽  
Author(s):  
◽  
Nicola J Nelson
Keyword(s):  
Sex Ratio ◽  
Sex Determination ◽  
Hatching Success ◽  
Conservation Management ◽  
Incubation Temperature ◽  
Management Tool ◽  
Relative Fitness ◽  
Temperature Dependent ◽  
Sphenodon Punctatus ◽  
Artificial Incubation

<p>Juveniles resulting from artificially induced and incubated eggs are often used to found or augment populations of rare reptiles, but both procedures may compromise the health of hatchlings or their fitness in natural environments. I aimed to test whether these procedures affected size or performance of juvenile tuatara, Sphenodon punctatus, New Zealand reptiles with temperature-dependent sex determination (TSD). Size and performance are phenotypic traits likely to influence fitness and eventual lifetime reproductive success, and are thus important measures of the suitability of artificial induction and incubation techniques for conservation management. I incubated 320 tuatara eggs artificially at 18, 21 and 22ºC; 52% of these were obtained by induction, the remainder were collected from natural nests. An additional 25 natural nests were left intact for investigation of TSD and effects of incubation temperature in nature. Juveniles from all incubation regimes were kept for ten months post-hatching in similar rearing conditions and sexed by laparoscopy. Induced eggs were significantly smaller than naturally laid eggs, and resulted in significantly smaller hatchlings, even when variation among clutches was accounted for. Incubation temperature did not greatly influence size at hatching, but was an important determinant of size by ten months of age; initial egg mass was the most important factor affecting size of hatchlings. Data indicate that TSD occurs in nature. The sex of hatchlings from 21 nests was investigated: 10 nests produced 100% male hatchlings, 4 nests produced 100% female hatchlings, and only 7 nests produced mixed sex ratios which ranged from 11% to 88% males. Sex of juveniles was related to temperature with a larger proportion of males produced in warmer nests. The overall percentage of male hatchlings in natural nests was 64%. Hatching success was 65% from natural nests during the 1998/99 season. Incubation temperatures throughout the year ranged from 2.9 to 34.4ºC. Global warming is likely to skew the hatchling sex ratio towards males if female tuatara are unable to select nest sites according to environmental cues. Evidence from size patterns of tuatara incubated in natural nests supports differential fitness models for the adaptive significance of TSD. The evaluation of artificial incubation as a conservation management tool demonstrated that it is a procedure that benefits conservation as it can be used reliably to produce founders; hatching success was 94% during this study. The sex ratio of artificially incubated juveniles can be easily manipulated; the pivotal temperature lies between 21 and 22ºC. Constant artificial incubation conditions resulted in larger juveniles by ten months of age than those from natural incubation. Naturally incubated juvenile tuatara, however, were faster for their size, their reaction norm to predator stimuli was to run, and they were possibly more aggressive, suggesting naturally incubated juveniles could survive better in nature. No firm conclusions can be reached on the quality of artificially incubated juvenile tuatara because further research will be required to establish the relevance of performance test results in nature and consequences of incubation regimes in the longer term with respect to relative fitness of individuals.</p>

scholarly journals Maternal provisioning and fluctuating thermal regimes enhance immune response in a reptile with temperature-dependent sex determination

2021 ◽  
pp. jeb.237016
Author(s):  
Jessica Alice Leivesley ◽  
Njal Rollinson
Keyword(s):  
Immune Response ◽  
Sex Determination ◽  
Constant Temperature ◽  
Early Life ◽  
Incubation Temperature ◽  
Experimental Studies ◽  
Egg Mass ◽  
Temperature Dependent ◽  
Bactericidal Capacity ◽  
Maternal Provisioning

The Charnov-Bull model of differential fitness is often used to explain the evolution and maintenance of temperature-dependent sex determination (TSD). Most tests of the model focus on morphological proxies of fitness, such as size traits, whereas early life physiological traits that are closely related to lifetime fitness might provide a framework for generalising the Charnov-Bull model across taxa. One such trait is the strength of early life immune response, which is strongly linked to early life survival and fitness. Here, we manipulate temperature, variance in temperature, and sex to test the Charnov-Bull model using a physiological trait, immune system strength, in the snapping turtle (Chelydra serpentina L. 1758). We find no evidence of sex-specific differences in bactericidal capacity of hatchling blood, and no evidence that mean temperature influences bactericidal capacity. However, we find that fluctuating incubation temperature (i.e., a more naturalized incubation regime) is associated with a greater bactericidal capacity compared to constant temperature incubation. We also find that egg mass, a proxy for maternal provisioning, is positively associated with bactericidal capacity. Our findings suggest that the evolution of temperature-dependent sex determination in reptiles is unrelated to our measure early-life innate immunity. Our study also underlines how immune response is condition-dependent in early life, and questions the biological relevance of constant temperature incubation in experimental studies on ectotherm development.

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

Intraspecific genome size variation in a turtle (Trachemys scripta) exhibiting temperature-dependent sex determination

1991 ◽  
Vol 69 (9) ◽  
pp. 2306-2310 ◽  
Author(s):  
Samuel F. Lockwood ◽  
Brenden S. Holland ◽  
John W. Bickham ◽  
Brian G. Hanks ◽  
James J. Bull
Keyword(s):  
Sex Ratio ◽  
Sex Determination ◽  
Genome Size ◽  
Incubation Temperature ◽  
Size Variation ◽  
Developmental Rate ◽  
Trachemys Scripta ◽  
Temperature Dependent ◽  
Genome Size Variation ◽  
Different Temperatures

Variation in genome size within and among populations of the pond slider, Trachemys scripta, a species with temperature-dependent sex determination, was investigated. Because genome size has been shown to affect developmental rate in various organisms, as does incubation temperature, it was hypothesized that genome size could influence sex determination in species with environmental sex determination. Significant variation in DNA content was found between geographic populations and among clutches. No significant differences in mean genome size were observed among samples incubated at different temperatures or between sexes of turtles hatched at a temperature that yields a mixed sex ratio. Thus, it appears that sex determination in T. scripta is accomplished in the absence of sex-specific and incubation-temperature-specific differences in genome size. Preliminary data from two populations, however, suggest that genome size may be significantly correlated with the threshold incubation temperature at which a mixed sex ratio is produced.

Absence of temperature-dependent sex determination in northern populations of two cyprinodontid fishes

1991 ◽  
Vol 69 (2) ◽  
pp. 530-533 ◽  
Author(s):  
D. O. Conover ◽  
S. B. DeMond
Keyword(s):  
Sex Ratio ◽  
Sex Determination ◽  
Life Histories ◽  
Laboratory Experiments ◽  
Fundulus Heteroclitus ◽  
Incubation Temperature ◽  
Effect Of Temperature ◽  
Temperature Dependent ◽  
Young Of The Year ◽  
Embryonic And Larval Development

We tested for an effect of temperature during embryonic and larval development on the sex ratio of offspring in two cyprinodontid fishes (Fundulus heteroclitus and Cyprinodon variegatus) having life histories in which temperature-dependent sex determination might be expected to occur. In both species, field collections showed that as young of the year recruited to the population, the sex ratio did not vary over time, nor did it deviate from 1:1. In laboratory experiments, there was no influence of incubation temperature on sex ratio in either species and sex ratios were near unity in all treatments. Although there was no evidence of temperature-dependent sex determination in the populations we studied, this result should be confirmed on other populations before it is generalized to the species level.

scholarly journals Inheritance of nesting behaviour across natural environmental variation in a turtle with temperature-dependent sex determination

2009 ◽  
Vol 277 (1685) ◽  
pp. 1219-1226 ◽  
Author(s):  
Suzanne E. McGaugh ◽  
Lisa E. Schwanz ◽  
Rachel M. Bowden ◽  
Julie E. Gonzalez ◽  
Fredric J. Janzen
Keyword(s):  
Sex Determination ◽  
Vegetation Cover ◽  
Incubation Temperature ◽  
Additive Genetic Variance ◽  
Thermal Conditions ◽  
Evolutionary Change ◽  
Temperature Dependent ◽  
Painted Turtles ◽  
Julian Date ◽  
Nesting Behaviour

Nesting behaviour is critical for reproductive success in oviparous organisms with no parental care. In organisms where sex is determined by incubation temperature, nesting behaviour may be a prime target of selection in response to unbalanced sex ratios. To produce an evolutionary change in response to sex-ratio selection, components of nesting behaviour must be heritable. We estimated the field heritability of two key components of nesting behaviour in a population of painted turtles ( Chrysemys picta ) with temperature-dependent sex determination by applying the ‘animal model’ to a pedigree reconstructed from genotype data. We obtained estimates of low to non-detectable heritability using repeated records across all environments. We then determined environment-specific heritability by grouping records with similar temperatures for the winter preceding the nesting season, a variable known to be highly associated with our two traits of interest, nest vegetation cover and Julian date of nesting. The heritability estimates of nest vegetation cover and Julian date of nesting were qualitatively highest and significant, or nearly so, after hot winters. Additive genetic variance for these traits was not detectable after cold winters. Our analysis suggests that the potential for evolutionary change of nesting behaviour may be dependent on the thermal conditions of the preceding winter, a season that is predicted to be especially subject to climate change.

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