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

Abstract

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 free Plain Language Summary for this article on the Journal blog.

Fauna Associated with American Alligator (Alligator mississippiensis) Nests in Coastal South Carolina, USA

“…Fiddler crab burrows are known to aerate marsh sediments and influence sediment oxygen dynamics [70]. This raises interesting questions regard-ing the potential effects of fiddler crab burrows constructed in alligator nests on internal gas flux and thermal dynamics and, subsequently, alligator egg incubation temperatures, hatchling sex ratios, and neonatal survival associated with those nests [71]. Overall, except for ants, virtually nothing is known regarding the invertebrate fauna of crocodilian nest mounds despite the potential of these large heaps of decomposing vegetation as an ideal, albeit ephemeral, habitat for a variety of species.…”

The influence of incubation temperature on offspring traits varies across northern and southern populations of the American alligator (Alligator mississippiensis)

“…Recent reports demonstrate that temperature-sensitive traits, including body mass index (BMI) and snout-vent length (SVL), are associated with higher juvenile survival at MPT in the alligator (Bock et al, 2023;Johnson et al, 2023). However, these appear to be context dependent as the relationship between phenotypic traits and survival varies across years (Bock et al, 2023). Nonetheless, given that warmer, MPT appears to be the optimum developmental temperature in this species, we hypothesize that northern populations, presumably exposed to cooler temperatures, will show compensatory responses to incubation temperature.…”

“…Specifically, incubations at warmer, male-promoting temperatures (MPT) reduce developmental costs, producing larger hatchlings with greater residual yolk reserves when compared to incubations at cooler female-promoting temperatures (FPT, Allsteadt & Lang, 1995;Bock et al, 2023. Recent reports demonstrate that temperature-sensitive traits, including body mass index (BMI) and snout-vent length (SVL), are associated with higher juvenile survival at MPT in the alligator (Bock et al, 2023;Johnson et al, 2023). However, these appear to be context dependent as the relationship between phenotypic traits and survival varies across years (Bock et al, 2023).…”

“…Like many turtles and some lizards, alligators display temperature-dependent sex determination (TSD), in which thermal signals experienced during a discrete developmental window determine sex, along with additional phenotypic traits (Allsteadt & Lang, 1995;Bock et al, 2021;Kohno et al, 2014;McCoy et al, 2016). Specifically, incubations at warmer, male-promoting temperatures (MPT) reduce developmental costs, producing larger hatchlings with greater residual yolk reserves when compared to incubations at cooler female-promoting temperatures (FPT, Allsteadt & Lang, 1995;Bock et al, 2023. Recent reports demonstrate that temperature-sensitive traits, including body mass index (BMI) and snout-vent length (SVL), are associated with higher juvenile survival at MPT in the alligator (Bock et al, 2023;Johnson et al, 2023).…”