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1. Differential early‐life survival underlies the adaptive significance of temperature‐dependent sex determination in a long‐lived reptile

   https://doi.org/10.1111/1365-2435.14420  

   Bock, Samantha L. ; Loera, Yeraldi ; Johnson, Josiah M. ; Smaga, Christopher R. ; Haskins, David L. ; Tuberville, Tracey D. ; Singh, Randeep ; Rainwater, Thomas R. ; Wilkinson, Philip M. ; Parrott, Benjamin B. ( September 2023 , Functional Ecology)

   Many ectotherms rely on temperature cues experienced during development to determine offspring sex. The first descriptions of temperature‐dependent sex determination (TSD) were made over 50 years ago, yet an understanding of its adaptive significance remains elusive, especially in long‐lived taxa.

   One novel hypothesis predicts that TSD should be evolutionarily favoured when two criteria are met—(a) incubation temperature influences annual juvenile survival and (b) sexes mature at different ages. Under these conditions, a sex‐dependent effect of incubation temperature on offspring fitness arises through differences in age at sexual maturity, with the sex that matures later benefiting disproportionately from temperatures that promote juvenile survival.

   The American alligator (Alligator mississippiensis) serves as an insightful model in which to test this hypothesis, as males begin reproducing nearly a decade after females. Here, through a combination of artificial incubation experiments and mark‐recapture approaches, we test the specific predictions of the survival‐to‐maturity hypothesis for the adaptive value of TSD by disentangling the effects of incubation temperature and sex on annual survival of alligator hatchlings across two geographically distinct sites.

   Hatchlings incubated at male‐promoting temperatures (MPTs) consistently exhibited higher survival compared to those incubated at female‐promoting temperatures. This pattern appears independent of hatchling sex, as females produced from hormone manipulation at MPT exhibit similar survival to their male counterparts.

   Additional experiments show that incubation temperature may affect early‐life survival primarily by affecting the efficiency with which maternally transferred energy resources are used during development.

   Results from this study provide the first explicit empirical support for the adaptive value of TSD in a crocodilian and point to developmental energetics as a potential unifying mechanism underlying persistent survival consequences of incubation temperature.

   Read the freePlain Language Summaryfor this article on the Journal blog.

    

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2. Genome‐wide DNA methylation patterns harbour signatures of hatchling sex and past incubation temperature in a species with environmental sex determination

   https://doi.org/10.1111/mec.16670  

   Bock, Samantha L. ; Smaga, Christopher R. ; McCoy, Jessica A. ; Parrott, Benjamin B. ( November 2022 , Molecular Ecology)

   Abstract Conservation of thermally sensitive species depends on monitoring organismal and population‐level responses to environmental change in real time. Epigenetic processes are increasingly recognized as key integrators of environmental conditions into developmentally plastic responses, and attendant epigenomic data sets hold potential for revealing cryptic phenotypes relevant to conservation efforts. Here, we demonstrate the utility of genome‐wide DNA methylation (DNAm) patterns in the face of climate change for a group of especially vulnerable species, those with temperature‐dependent sex determination (TSD). Due to their reliance on thermal cues during development to determine sexual fate, contemporary shifts in temperature are predicted to skew offspring sex ratios and ultimately destabilize sensitive populations. Using reduced‐representation bisulphite sequencing, we profiled the DNA methylome in blood cells of hatchling American alligators ( Alligator mississippiensis ), a TSD species lacking reliable markers of sexual dimorphism in early life stages. We identified 120 sex‐associated differentially methylated cytosines (DMCs; FDR < 0.1) in hatchlings incubated under a range of temperatures, as well as 707 unique temperature‐associated DMCs. We further developed DNAm‐based models capable of predicting hatchling sex with 100% accuracy (in 20 training samples and four test samples) and past incubation temperature with a mean absolute error of 1.2°C (in four test samples) based on the methylation status of 20 and 24 loci, respectively. Though largely independent of epigenomic patterning occurring in the embryonic gonad during TSD, DNAm patterns in blood cells may serve as nonlethal markers of hatchling sex and past incubation conditions in conservation applications. These findings also raise intriguing questions regarding tissue‐specific epigenomic patterning in the context of developmental plasticity. 

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3. Spatial and temporal variation in phenotypes and fitness in response to developmental thermal environments

   https://doi.org/10.1111/1365-2435.13910  

   Pruett, Jenna E. ; Warner, Daniel A. ( October 2021 , Functional Ecology)

   Phenotypic variation within populations is influenced by the environment via plasticity and natural selection. How phenotypes respond to the environment can vary among traits, populations and life stages in ways that can influence fitness.

   Plastic responses during early development are particularly important because they can affect components of fitness throughout an individual's life. Consequently, how natural selection shapes developmental plasticity could be influenced by fitness consequences across different life stages. Moreover, spatial variation in selection pressures could generate differences in plastic responses among populations.

   To gain insight into sources of variation in phenotypes and survival, we used a laboratory egg incubation experiment using brown anole lizardsAnolis sagreifrom mainland (ancestral) and island (descendent) populations, combined with a mark–release–recapture experiment in the field. Our study was designed to (a) quantify the effects developmental temperature on embryo development and offspring morphology, (b) assess how developmental temperature influences offspring survival across different life stages and (c) quantify how thermal reaction norms vary among ancestral and descendant populations.

   Developmental temperature influenced offspring morphology, but thermal reaction norms of embryos showed little variation among populations. Developmental temperature influenced offspring survival, but the patterns differed between embryo and hatchling stages; the optimal temperature for embryos was about 5℃ lower than that for hatchlings. High temperatures were thermally stressful to embryos, but they reduced incubation duration and led to early hatching. In turn, earlier hatching increased the probability of survival to adulthood. Moreover, the effect of developmental temperature on hatchling survival was most pronounced for offspring that hatched late in the season.

   The difference in optimal developmental temperatures between life stages may be driven by physiological tolerance for embryos and by ecological factors for hatchlings. Moreover, the fitness consequences of the developmental environment depend on the phenology of hatching. Overall, these results highlight how the developmental environment can differentially affect fitness across life stages and show that temporal thermal heterogeneity can influence survival of embryos, but the consequences on post‐hatching stages may vary at different times of the season.

   A freePlain Language Summarycan be found within the Supporting Information of this article.

    

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4. Breadth of the thermal response captures individual and geographic variation in temperature‐dependent sex determination

   https://doi.org/10.1111/1365-2435.13410  

   Carter, Anna L. ; Bodensteiner, Brooke L. ; Iverson, John B. ; Milne‐Zelman, Carrie L. ; Mitchell, Timothy S. ; Refsnider, Jeanine M. ; Warner, Daniel A. ; Janzen, Fredric J. ; White, ed., Craig ( August 2019 , Functional Ecology)

   Population‐scale responses of key ecological traits to local environmental conditions provide insight into their adaptive potential. In species with temperature‐dependent sex determination (TSD), short‐term, individual developmental responses to the incubation environment have long‐term consequences for populations.

   We took a model‐based approach to study within‐ and among‐population variation in the physiological components of TSD in 12 populations of painted turtles (Chrysemys picta). We used laboratory and field incubation data to quantify variation in thermal reaction norms at both population and clutch scales, focusing on the pivotal temperature that produces a 1:1 sex ratio (P) and the transitional range of incubation temperatures (TRTs) that produce mixed sex ratios.

   Defying theoretical expectations, among‐population variation inPwas not convincingly explained by geography or local thermal conditions. However, within some populations,Pvaried by >5°C at the clutch scale, indicating that the temperature sensitivity of gonadal differentiation can vary substantially among individual nesting females. In addition, the TRT was wider at lower latitudes, suggesting responsiveness to local incubation conditions.

   Our results provide a potential explanation for discrepancies observed between constant‐temperature experimental results and outcomes of fluctuating incubation conditions experienced in natural nests, exposing important knowledge gaps in our understanding of local adaptation in TSD and identifying shortcomings of traditional laboratory studies. Understanding individual variation and the timing of gonadal differentiation is likely to be far more useful in understanding local adaptation than previously acknowledged.

   A freePlain Language Summarycan be found within the Supporting Information of this article.

    

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5. Post-Transcriptional Mechanisms Respond Rapidly to Ecologically Relevant Thermal Fluctuations During Temperature-Dependent Sex Determination

   https://doi.org/10.1093/iob/obaa033  

   Bock, Samantha L ; Hale, Matthew D ; Leri, Faith M ; Wilkinson, Philip M ; Rainwater, Thomas R ; Parrott, Benjamin B ( January 2020 , Integrative Organismal Biology)

   null (Ed.)

   Synopsis An organism’s ability to integrate transient environmental cues experienced during development into molecular and physiological responses forms the basis for adaptive shifts in phenotypic trajectories. During temperature-dependent sex determination (TSD), thermal cues during discrete periods in development coordinate molecular changes that ultimately dictate sexual fate and contribute to patterns of inter- and intra-sexual variation. How these mechanisms interface with dynamic thermal environments in nature remain largely unknown. By deploying thermal loggers in wild nests of the American alligator (Alligator mississippiensis) over two consecutive breeding seasons, we observed that 80% of nests exhibit both male- and female-promoting thermal cues during the thermosensitive period, and of these nests, all exhibited both male- and female-promoting temperatures within the span of a single day. These observations raise a critical question—how are opposing environmental cues integrated into sexually dimorphic transcriptional programs across short temporal scales? To address this question, alligator embryos were exposed to fluctuating temperatures based on nest thermal profiles and sampled over the course of a daily thermal fluctuation. We examined the expression dynamics of upstream genes in the temperature-sensing pathway and find that post-transcriptional alternative splicing and transcript abundance of epigenetic modifier genes JARID2 and KDM6B respond rapidly to thermal fluctuations while transcriptional changes of downstream effector genes, SOX9 and DMRT1, occur on a delayed timescale. Our findings reveal how the basic mechanisms of TSD operate in an ecologically relevant context. We present a hypothetical hierarchical model based on our findings as well as previous studies, in which temperature-sensitive alternative splicing incrementally influences the epigenetic landscape to affect the transcriptional activity of key sex-determining genes. 

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