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 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.

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 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>

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

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 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 Unexpected resilience of species with temperature-dependent sex determination at the Cretaceous–Palaeogene boundary

2010 ◽  
Vol 7 (2) ◽  
pp. 295-298 ◽  
Author(s):  
Sherman Silber ◽  
Jonathan H. Geisler ◽  
Minjin Bolortsetseg
Keyword(s):  
Climate Change ◽  
Sex Ratio ◽  
Sex Determination ◽  
Volcanic Eruptions ◽  
Egg Laying ◽  
Molecular Clocks ◽  
Temperature Dependent ◽  
Hell Creek Formation ◽  
Male Preponderance ◽  
Genotypic Sex Determination

It has been suggested that climate change at the Cretaceous–Palaeogene (K–Pg) boundary, initiated by a bolide impact or volcanic eruptions, caused species with temperature-dependent sex determination (TSD), including dinosaurs, to go extinct because of a skewed sex ratio towards all males. To test this hypothesis, the sex-determining mechanisms (SDMs) of Cretaceous tetrapods of the Hell Creek Formation (Montana, USA) were inferred using parsimony optimizations of SDMs on a tree, including Hell Creek species and their extant relatives. Although the SDMs of non-avian dinosaurs could not be inferred, we were able to determine the SDMs of 62 species; 46 had genotypic sex determination (GSD) and 16 had TSD. The TSD hypothesis for extinctions performed poorly, predicting between 32 and 34 per cent of survivals and extinctions. Most surprisingly, of the 16 species with TSD, 14 of them survived into the Early Palaeocene. In contrast, 61 per cent of species with GSD went extinct. Possible explanations include minimal climate change at the K–Pg, or if climate change did occur, TSD species that survived had egg-laying behaviour that prevented the skewing of sex ratios, or had a sex ratio skewed towards female rather than male preponderance. Application of molecular clocks may allow the SDMs of non-avian dinosaurs to be inferred, which would be an important test of the pattern discovered here.

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.

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