Evolution Of Temperature-dependent Sex Determination Research Articles

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

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 generalizing the Charnov-Bull model across taxa. One such trait is the strength of the early-life immune response, which is strongly linked to early-life survival and fitness. Here, we manipulated 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). We found no evidence of sex-specific differences in bactericidal capacity of hatchling blood, and no evidence that mean temperature influences bactericidal capacity. However, we did find that fluctuating incubation temperature (i.e. a more naturalized incubation regime) is associated with a greater bactericidal capacity compared with constant temperature incubation. We also found 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 of 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.

A simple model for the evolution of temperature-dependent sex determination explains the temperature sensitivity of embryonic mortality in imperiled reptiles.

A 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 warm, female-producing temperatures are more stressful than cool, male-producing temperatures. Further, we find some evidence that pivotal temperatures (TPiv, the temperature that produces a 1:1 sex ratio) may 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 >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.

Incubation temperature and parental identity determine sex in the Australian agamid lizard Ctenophorus pictus.

Sex determination in Australian agamid lizards shows a complex framework of different mechanisms, varying even among closely related taxa. It is clear that discrete classification of these species as either having genetic (GSD) or environmental sex determination (ESD) does not agree with empirical data. Although many species in this group show temperature‐dependent sex determination (TSD), recent evidence suggests additional genetic or epigenetic effects. A proposed model explaining the adaptive significance and evolution of TSD in short‐lived agamids predicts that selection will favor temperature‐biased sex ratios in species with intense male‐male competition. Here, we use experimental incubation at (near) constant temperatures to test whether the sex of Australian painted dragons (Ctenophorus pictus) is influenced by temperature, building on previous research yet to have reached an agreement regarding the role of temperature in this species. In this study, incubation temperature and parental identity affected hatchling sex suggesting that environment and genetics may work in concert to determine sex in this species. Although our results are consistent with TSD, our data cannot rule out a temperature‐by‐sex effect on egg or hatchling mortality. However, our findings together with the observed differences of sex determination systems in closely related species within this genus may provide novel opportunities to address fundamental questions in the evolution of sex determination systems.

Revisiting the first report of temperature‐dependent sex determination in a vertebrate, the African redhead agama

AbstractVertebrates display a wide variety of sex‐determining mechanisms (SDMs). Identifying SDMs for different taxa is important for understanding the origins and phylogenetic history of sex‐determining mechanisms. Temperature‐dependent sex determination (TSD) is found in several vertebrate and invertebrate species, and has been studied most extensively in reptiles. The initial discovery of TSD was in a lizard, the African redhead agama (Agama agama), over 50 years ago. The original study of A. agama used only two incubation temperature treatments and had a small sample size, thus it could not fully characterize the pattern of TSD in this species. The goal of this study is to revisit this research to better characterize the pattern of TSD. We also assessed the effect of fluctuating incubation temperatures on offspring sex ratio to provide insight into how variation in offspring sex ratio is produced under natural conditions. After incubating eggs across six constant temperature treatments, we demonstrated that females are produced at relatively cool temperatures and males at warmer temperatures (30°C); fluctuating thermal regimes showed this same pattern. However, some females are again produced at even warmer temperatures, resulting in relatively balanced sex ratios toward the end of the sex‐determining reaction norm. Though the shape of the sex‐determining reaction norm shown here is unusual, it shows some similarities to that of other agamid lizards. Future studies that explore the diversity of TSD reaction norms and underlying physiological mechanisms will provide new insights into the evolution of TSD.

Seasonal sex ratios and the evolution of temperature-dependent sex determination in oviparous lizards

Although the adaptive significance of temperature-dependent sex determination (TSD) remains a puzzle, recent models implicate a seasonal bias in offspring sex production that translates into sex-specific fitness benefits later in life. Sex-specific emergence has been linked to fitness gains in some fish, birds and reptiles, but field data supporting the occurrence of a seasonal pattern of sex ratios in oviparous lizards are lacking. We tested the hypothesis that patterns of nest site selection and seasonal temperature changes combine to inhibit the materialization of sex-biased hatching times in a population of water dragons (Intellagama lesueurii). As predicted, a seasonal increase in air and nest temperatures resulted in a sex bias by nesting date; male-producing clutches were laid 17.8 days sooner than female-producing clutches, on average. However, the seasonal ramping of nest temperatures also caused shorter relative incubation periods in the later, all-female clutches. As a consequence of this developmental ‘catch-up’, the mean hatching date for male-producing nests preceded the mean hatching date for female-producing nests by only 7.2 days. We suggest that a contracted distribution of hatching dates compared to the distribution of oviposition dates represents a general pattern for oviparous reptiles in seasonal climates, which in TSD species may largely offset the temporal disparity in nesting dates between the sexes. Although data are needed for other TSD species, such minor age differences between male and female hatchlings may not translate into fitness differences later in life, an assumption of some models for the evolution and maintenance of TSD.

Temperature, phenotype, and the evolution of temperature‐dependent sex determination: how do natural incubations compare to laboratory incubations?

Phenotypic variation is a fundamental component of the process of evolution and understanding the factors that create this variation is critical to investigations of this process. We test the hypothesis that phenotypic variation created under natural incubation conditions will differ from that created under constant laboratory conditions in a reptile species with temperature-dependent sex determination (TSD), the red-eared slider turtle (Trachemys scripta). Using a split clutch design, we demonstrate that offspring morphology, behavior, and sex differed between hatchlings incubated in the field and those from the laboratory, but immune response did not. The interactions between different phenotypic parameters will ultimately determine how natural selection acts upon offspring, and consequently our data suggest that offspring developing under these differing conditions should have different fitnesses. The relationship between offspring sex and phenotype serves as the theoretical foundation on which most investigations into the evolution of TSD are built. Thus, it may be necessary to use natural incubation conditions to accurately examine how offspring sex relates to other phenotypic parameters if we are to understand the evolution of this sex determining mechanism.

Fitness effects of the timing of hatching may drive the evolution of temperature-dependent sex determination in short-lived lizards

In several species of short-lived Australian agamid lizards, an individual’s sex is determined by the nest temperatures encountered during incubation. The adaptive significance of such systems remains unclear. Here, we explore the hypothesis that (1) the optimal timing of hatching differs between the sexes, and thus (2) temperature-dependent sex determination (TSD) enhances maternal and offspring fitness by generating seasonal shifts in offspring sex ratios. Our model predicts that TSD can indeed enhance maternal fitness returns in short-lived lizards if (1) male–male competition is intense, thus reducing mating success of newly-matured males (but not females), and (2) the nesting season is prolonged, such that seasonal effects become significant. Available data on the distribution of TSD in Australian agamid lizards broadly support these predictions. Because both the level of male–male competition and the length of nesting season can vary at small spatial and temporal scales, selective forces on sex-determining mechanisms also should vary. Hence, our model predicts extensive small-scale (intraspecific) variation in sex-determining systems within agamid lizards, as well as among species.

Temperature Sex Reversal Implies Sex Gene Dosage in a Reptile

Sex in reptiles is determined by genes on sex chromosomes or by incubation temperature. Previously these two modes were thought to be distinct, yet we show that high incubation temperatures reverse genotypic males (ZZ) to phenotypic females in a lizard with ZZ and ZW sex chromosomes. Thus, the W chromosome is not necessary for female differentiation. Sex determination is probably via a dosage-sensitive male-determining gene on the Z chromosome that is inactivated by extreme temperatures. Our data invite a novel hypothesis for the evolution of temperature-dependent sex determination (TSD) and suggest that sex chromosomes may exist in many TSD reptiles.

NO SEASONAL SEX-RATIO SHIFT DESPITE SEX-SPECIFIC FITNESS RETURNS OF HATCHING DATE IN A LIZARD WITH GENOTYPIC SEX DETERMINATION

Sex allocation theory predicts that mothers should adjust their sex-specific reproductive investment in relation to the predicted fitness returns from sons versus daughters. Sex allocation theory has proved to be successful in some invertebrate taxa but data on vertebrates often fail to show the predicted shift in sex ratio or sex-specific resource investment. This is likely to be partly explained by simplistic assumptions of vertebrate life-history and mechanistic constraints, but also because the fundamental assumption of sex-specific fitness return on investment is rarely supported by empirical data. In short-lived species, the time of hatching or parturition can have a strong impact on the age and size at maturity. Thus, if selection favors adult sexual-size dimorphism, females can maximize their fitness by adjusting offspring sex over the reproductive season. We show that in mallee dragons, Ctenophorus fordi, date of hatching is positively related to female reproductive output but has little, if any, effect on male reproductive success, suggesting selection for a seasonal shift in offspring sex ratio. We used a combination of field and laboratory data collected over two years to test if female dragons adjust their sex allocation over the season to ensure an adaptive match between time of hatching and offspring sex. Contrary to our predictions, we found no effect of laying date on sex ratio, nor did we find any evidence for within-female between-clutch sex-ratio adjustment. Furthermore, there was no differential resource investment into male and female offspring within or between clutches and sex ratios did not correlate with female condition or any partner traits. Consequently, despite evidence for selection for a seasonal sex-ratio shift, female mallee dragons do not seem to exercise any control over sex determination. The results are discussed in relation to potential constraints on sex-ratio adjustment, alternative selection pressures, and the evolution of temperature-dependent sex determination.

Egg mass determines hatchling size, and incubation temperature influences post‐hatching growth, of tuatara Sphenodon punctatus

AbstractThe size of reptile hatchlings can be phenotypically plastic in response to incubation temperature, and size is a trait likely to influence fitness – i.e. hatchling size is proposed as an indicator of quality. The parental and incubation temperature effects on the size of one of New Zealand's most biologically significant reptile species, the tuatara Sphenodon punctatus are investigated. Artificial incubation at constant temperatures is used to produce founders for new captive and wild populations of tuatara and to augment existing rare populations. We compare size of hatchling tuatara from artificial and natural incubation treatments. The relationship of hatchling size with incubation temperature and sex is examined, and we investigate whether our results support differential fitness models for the evolution of temperature‐dependent sex determination in tuatara. Initial egg mass is the most important factor affecting size of hatchling tuatara and is still an important influence at 10 months of age. Incubation temperature does not greatly influence size of hatchlings, but significantly influences size by 10 months of age. Constant artificial incubation conditions result in larger, but possibly less aggressive, juveniles than those from more variable natural incubation conditions by 10 months of age. Evidence from size patterns of tuatara incubated in natural nests supports differential fitness models for the adaptive significance of temperature‐dependent sex determination. Thermal variation has little effect on size of male hatchlings, but female embryos that develop in more stable thermal conditions, in more reliable sites for hatching, are bigger and have longer jaws.

Embryonic temperature affects metabolic compensation and thyroid hormones in hatchling snapping turtles.

Temperature acclimation of adult vertebrates typically induces changes in metabolic physiology. During early development, such metabolic compensation might have profound consequences, yet acclimation of metabolism is little studied in early life stages. We measured the effect of egg incubation temperature on resting metabolic rate (RMR) and blood thyroid hormone levels of hatchling snapping turtles (Chelydra serpentina). Like many reptiles, snapping turtles have temperature-dependent sex determination (TSD), in which embryonic temperature determines sex. Therefore, we designed the experiments to separately measure effects of temperature and of sex on the response variables. We incubated eggs in the laboratory at 21. 5 degrees, 24.5 degrees, 27.5 degrees, and 30.5 degrees C, producing both sexes, all males, both sexes, and all females, respectively. Hatchling RMR, when measured at a common temperature (either 25 degrees or 31 degrees C), was negatively correlated with egg temperature in both males and females, such that RMR of turtles from 21.5 degrees C-incubated eggs averaged 160% that of turtles from 30.5 degrees C-incubated eggs. These results indicate that egg temperatures induced positive metabolic compensation in both sexes. Thyroid hormone levels of hatchlings showed similar correlations with egg temperature; thyroxine level of turtles from 21.5 degrees C-incubated eggs averaged 220% that of turtles from 30.5 degrees C-incubated eggs. To examine the possibility that thyroid hormones contribute to positive metabolic compensation, we added triiodothyronine to eggs during mid-incubation. RMR of hatchlings from these treated eggs averaged 131% that of controls, consistent with the previous possibility. Moreover, the effects of embryonic temperature on metabolic physiology, in combination with effects on sex, can result in differences in RMR and thyroid hormone levels between male and female hatchling turtles. Such differences may be important to the ecology and evolution of TSD.

Incubation Temperature and Sex Affect Mass and Energy Reserves of Hatchling Snapping Turtles, Chelydra serpentina

Temperature during embryonic development irreversibly determines gonadal sex in many oviparous reptiles. Although embryonic temperature also influences a number of other traits in these species, it is unclear whether such effects are primarily due to incubation temperature or to gonadal sex. Here we dissociated these normally confounding effects via hormonal manipulations of snapping turtle embryos (Chelydra serpentina), a species with temperature-dependent sex determination. We then ascertained temperature and sex effects on residual yolk mass, abdominal fat body mass, and total mass in neonates shortly after hatching or after one month without feeding. Yolk mass was initially affected by incubation temperature, clutch identity. and their interaction, but not gonadal sex. Yolk mass was not influenced by any of these variables 30 d after hateching. Fat mass was initially affected by temperature and clutch, but not sex. Gonadal sex did, however, affect fat mass at 30 d of age as did temperature and clutch. Incubation temperature affected total mass in a complex manner. There were significant clutch by temperature interactions initially, but no main effect of temperature. These effects changed so that the temperature effect was significant but interaction effects were not detected at 30 d of age. Repeated measures analysis of total mass after hatching and at 30 d of age indicated that turtles from lower temperatures lost more mass than turtles from higher incubation temperatures. and that females lost more mass than males. These data indicate that some hatchling traits were influenced directly by incubation temperature, whereas others were independently affected by gonadal sex. These results are consistent with a leading hypothesis for the evolution of temperature-dependent sex determination.

Sex differences in optimal incubation temperatures in a scincid lizard species.

Most theoretical models for the evolution of temperature-dependent sex determination (TSD) rely upon differential fitness of male and female offspring incubated under different thermal regimes. However, there are few convincing data on this topic. We studied incubation effects in a lizard species (Bassiana duperreyi, Scincidae) with genotypic sex determination, so that we could separate effects due to incubation temperatures from those due to offspring gender. We incubated eggs under two different fluctuating-temperature regimes that simulated hot and cold natural nest-sites. The effects of our incubation treatments on phenotypes of the hatchling lizards (morphology and locomotor performance) differed between the sexes. Females emerging from eggs exposed to the "hot nest" treatment (diel cycling, 23-31°C) were larger, and ran faster, than did their sisters from the "cold nest" treatment (16-24°C). Males showed a smaller and less consistent phenotypic response than females. These incubation-induced responses were relatively stable during the first few weeks of life post-hatching, at least in captive lizards maintained under laboratory conditions. These kinds of sex differences in the phenotypic responses of hatchling reptiles to incubation conditions provide a plausible basis for the evolution of temperature-dependent sex determination in reptiles.

Embryonic Temperature Influences Juvenile Temperature Choice And Growth Rate In Snapping Turtles Chelydra Serpentina

Snapping turtles (Chelydra serpentina) demonstrate temperature-dependent sex determination (TSD): intermediate egg incubation temperatures (23-27 degreesC) produce males, while extreme temperatures produce females. Snapping turtles are also sexually dimorphic: adult males are typically larger than females. Previous researchers hypothesized that male-producing egg temperatures enhanced the growth rate of juvenile turtles, resulting in the adult dimorphism and potentially providing an adaptive benefit for TSD. In reptiles, the choice of ambient temperature can also influence growth. I measured the effect of egg incubation temperature on juvenile growth rate and water temperature choice of C. serpentina. Eggs were incubated in the laboratory at 21.5, 24.5, 27.5 or 30.5 degreesC to produce both sexes, all males, both sexes or all females, respectively. Egg temperature was linearly and negatively correlated with growth rate of both male and female juveniles. Thus, growth was enhanced, but not maximized, by male-producing egg temperatures. Egg temperature was also negatively correlated with juvenile temperature choice such that, on average, turtles from 21.5 degreesC eggs selected 28 degreesC water, while turtles from 30.5 degreesC eggs chose 24.5 degreesC water. Additionally, these temperature choices were highly repeatable, even following a 6 month hibernation period at 7 degreesC. Thus, while male egg temperatures do not directly maximize growth, multiple effects of embryonic temperature may combine to create long-lasting differences in the behavioral physiology of male and female C. serpentina. Such differences could be important to the ecology and evolution of TSD.