Long-Term Resilience of Primary Sex Ratios in a Species with Temperature-Dependent Sex Determination after Decades of Climate Warming.

AbstractSpecies with environmental sex determination (ESD) have persisted through deep time, despite massive environmental perturbation in the geological record. Understanding how species with temperature-dependent sex determination (TSD), a type of ESD, persist through climate change is particularly timely given the current climate crisis, as highly biased sex ratios and extinction are predicted. Since 1982, we have studied primary sex ratios of a reptile with TSD (Chelydra serpentina). Primary sex ratios remained unchanged over time, despite warming in the environment. Resilience of the primary sex ratio occurred via a portfolio effect, realized through remarkable intra-annual variation in nest-level sex ratios, leading to a relatively consistent mean annual sex ratio. Intra-annual variation in nest-level sex ratios was related to variation in egg burial depth coupled with large clutch sizes, creating thermal gradients in the nest and promoting mixed-sex clutches. Furthermore, both locally and globally, sustained increases in nighttime air temperature contribute more to warming than increases in daily maximum temperature, but development rate was affected more strongly by maximum daily air temperature, conferring additional resilience to overall warming. Our study suggests that some TSD species may be resilient to warming and provides an example of how ESD may persist under environmental change.

A new method of estimating thermal performance of embryonic development rate yields accurate prediction of embryonic age in wild reptile nests.

Temperature has a strong effect on ectotherm development rate. It is therefore possible to construct predictive models of development that rely solely on temperature, which have applications in a range of biological fields. Here, we leverage a reference series of development stages for embryos of the turtle Chelydra serpentina, which was described at a constant temperature of 20 °C. The reference series acts to map each distinct developmental stage onto embryonic age (in days) at 20 °C. By extension, an embryo taken from any given incubation environment, once staged, can be assigned an equivalent age at 20 °C. We call this concept "Equivalent Development", as it maps the development stage of an embryo incubated at a given temperature to its equivalent age at a reference temperature. In the laboratory, we used the concept of Equivalent Development to estimate development rate of embryos of C. serpentina across a series of constant temperatures. Using these estimates of development rate, we created a thermal performance curve measured in units of Equivalent Development (TPCED). We then used the TPCED to predict developmental stage of embryos in several natural turtle nests across six years. We found that 85% of the variation of development stage in natural nests could be explained. Further, we compared the predictive accuracy of the model based on the TPCED to the predictive accuracy of a degree-day model, where development is assumed to be linearly related to temperature and the amount of accumulated heat is summed over time. Information theory suggested that the model based on the TPCED better describes variation in developmental stage in wild nests than the degree-day model. We suggest the concept of Equivalent Development has several strengths and can be broadly applied. In particular, studies on temperature-dependent sex determination may be facilitated by the concept of Equivalent Development, as development age maps directly onto the developmental series of the organism, allowing critical periods of sex determination to be delineated without invasive sampling, even under fluctuating temperature.