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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. Incubation temperature as a constraint on clutch size evolution

   https://doi.org/10.1111/1365-2435.13764  

   Hope, Sydney F. ; DuRant, Sarah E. ; Hallagan, John J. ; Beck, Michelle L. ; Kennamer, Robert A. ; Hopkins, William A. ; Williams, ed., Tony ( February 2021 , Functional Ecology)

   Elucidating factors that limit the number of offspring produced is fundamental to understanding life‐history evolution. Here, we examine the hypothesis that parental ability to maintain an optimal physical developmental environment for all offspring constrains clutch size via effects on offspring quality.

   Experimental laboratory studies of birds have shown that a <1°C difference in average incubation temperature has diverse effects on fitness‐related post‐hatching offspring phenotypes. Thus, the inability of parents to maintain optimal incubation temperatures could constrain clutch sizes.

   A fundamental question that has not been sufficiently addressed is whether larger clutch sizes lead towithinnest variation in egg temperature that is large enough to produce offspring with different phenotypes within a brood. This could lead to differential survival among offspring, and could create a trade‐off between offspring number and quality.

   We manipulated clutch size in nests of free‐living wood ducks and measured incubation temperature among and within clutches using multiple temperature loggers.

   As clutch size increased, average incubation temperatures were lower and more variable, and eggs took longer to hatch. Notably, the range inaverageincubation temperature among eggswithinnests increased with clutch size and exceeded 1°C in large clutches. Clutch size did not affect hatch success.

   In conjunction with our companion laboratory studies that used artificial incubation to document the effects of temperature variation on fitness‐related traits in this species, our work suggests that suboptimal incubation temperatures could be a factor that limits clutch size through diminishing returns on post‐hatch offspring quality.

   A freeplain language summarycan be found within the Supporting Information of this article.

    

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3. Thermal sensitivity of lizard embryos indicates a mismatch between oxygen supply and demand at near‐lethal temperatures

   https://doi.org/10.1002/jez.2359  

   Hall, Joshua M. ; Warner, Daniel A. ( April 2020 , Journal of Experimental Zoology Part A: Ecological and Integrative Physiology)

   Aspects of global change create stressful thermal environments that threaten biodiversity. Oviparous, non‐avian reptiles have received considerable attention because eggs are left to develop under prevailing conditions, leaving developing embryos vulnerable to increases in temperature. Though many studies assess embryo responses to long‐term (i.e., chronic), constant incubation temperatures, few assess responses to acute exposures which are more relevant for many species. We subjected brown anole (Anolis sagrei) eggs to heat shocks, thermal ramps, and extreme diurnal fluctuations to determine the lethal temperature of embryos, measure the thermal sensitivity of embryo heart rate and metabolism, and quantify the effects of sublethal but stressful temperatures on development and hatchling phenotypes and survival. Most embryos died at heat shocks of 45°C or 46°C, which is ~12°C warmer than the highest constant temperatures suitable for successful development. Heart rate and O₂consumption increased with temperature; however, as embryos approached the lethal temperature, heart rate and CO₂production continued rising while O₂consumption plateaued. These data indicate a mismatch between oxygen supply and demand at high temperatures. Exposure to extreme, diurnal fluctuations depressed embryo developmental rates and heart rates, and resulted in hatchlings with smaller body size, reduced growth rates, and lower survival in the laboratory. Thus, even brief exposure to extreme temperatures can have important effects on embryo development, and our study highlights the role of both immediate and cumulative effects of high temperatures on egg survival. Such effects must be considered to predict how populations will respond to global change.

    

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4. Adaptive variation in the development of extraembryonic membranes of gekkotan embryos: A meta‐analytical approach

   https://doi.org/10.1002/jmor.21345  

   Andrews, Robin M. ( March 2021 , Journal of Morphology)

   Highly mineralized rigid‐shelled eggs characterize one lineage of gekkotans. In contrast, poorly mineralized flexible‐shelled eggs characterize basal lineages of gekkotans and all other squamates. Low oxygen permeability of rigid‐shelled eggs is associated with small eggs and hatchlings, and long incubation lengths compared to flexible‐shelled gekkotan eggs. These features represent a demographic cost for species with rigid‐shelled eggs. This cost is offset, at least in part, because mortality due to desiccation and predation is reduced for rigid‐shelled eggs relative to flexible‐shelled eggs. Developmental traits may also compensate for the low oxygen permeability of rigid‐shelled eggs. Oviposition, for example, occurs at earlier developmental stages for gekkotans with rigid‐ versus flexible‐shelled eggs. Such early oviposition facilitates development because eggs move from the relatively hypoxic oviduct to the much better oxygenated nest environment. In this study, I tested the hypothesis that the growth of the yolk sac (YS) and chorioallantoic membrane (CAM) of gekkotans with rigid‐shelled eggs is initiated and completed earlier than those of gekkotans with flexible‐shelled eggs. I measured the surface area of eggs covered by the YS and CAM from oviposition to hatching and determined which of four nonlinear models provide the best fit for growth curves. I also compiled a data set on embryonic metabolism of gekkotans and other lizards in order to place growth of the YS and CAM in the context of energy utilization of lizard embryos overall. Growth of the YS and CAM of gekkotans with rigid‐shelled eggs is accelerated relative to that of gekkotans with flexible‐shelled eggs and may serve to separate the cost of YS and CAM development from that of the embryo itself. Adaptive variation in YS and CAM development may extend to birds, crocodilians, and turtles as they also exhibit life history variation that affects oxygen availability to embryos during development.

    

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5. Incubation Temperature and Maternal Resource Provisioning, but Not Contaminant Exposure, Shape Hatchling Phenotypes in a Species with Temperature-Dependent Sex Determination

   https://doi.org/10.1086/714572  

   Bock, Samantha L. ; Hale, Matthew D. ; Rainwater, Thomas R. ; Wilkinson, Philip M. ; Parrott, Benjamin B. ( April 2021 , The Biological Bulletin)

   null (Ed.)

   The environment experienced during embryonic development is a rich source of phenotypic variation, as environmental signals have the potential to both inform adaptive plastic responses and disrupt normal developmental programs. Environment-by-embryo interactions are particularly consequential for species with temperature-dependent sex determination, a mode of sex determination common in non-avian reptiles and fish, in which thermal cues during a discrete period of development drive the formation of either an ovary or a testis. Here we examine the impact of thermal variation during incubation in combination with developmental exposure to a common endocrine-disrupting contaminant on fitness-related hatchling traits in the American alligator (Alligator mississippiensis), a species with temperature-dependent sex determination. Using a factorial design, we exposed field-collected eggs to five thermal profiles (three constant temperatures, two fluctuating temperatures) and two environmentally relevant doses of the pesticide metabolite dichlorodiphenyldichloroethylene; and we quantified incubation duration, sex ratios, hatchling morphometric traits, and growth (9–10 days post-hatch). Whereas dichlorodiphenyldichloroethylene exposure did not generally affect hatchling traits, constant and fluctuating temperatures produced diverse phenotypic effects. Thermal fluctuations led to subtle changes in incubation duration and produced shorter hatchlings with smaller heads when compared to the constant temperature control. Warmer, male-promoting incubation temperatures resulted in larger hatchlings with more residual yolk reserves when compared to cooler, female-promoting temperatures. Together, these findings advance our understanding of how complex environmental factors interact with developing organisms to generate phenotypic variation and raise questions regarding the mechanisms connecting variable thermal conditions to responses in hatchling traits and their evolutionary implications for temperature-dependent sex determination. 

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