Sex and Incubation Temperature Independently Affect Embryonic Development and Offspring Size in a Turtle with Temperature-Dependent Sex Determination

Warner, Daniel A.; Mitchell, Timothy S.; Bodensteiner, Brooke L.; Janzen, Fredric J.

doi:10.1086/706786

Cited by 11 publications

(4 citation statements)

References 68 publications

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“…Although we found no evidence for sex effects on hatching success and post-hatching survival in this study, we see a cumulative reduction in fitness for females across all three stages (Table 2). Sexspecific differences in survival have been documented in other turtle species (e.g., Steyermark and Spotila, 2001b;Freedberg et al, 2001Freedberg et al, , 2004, as well as a range of other traits in painted turtles (Warner et al, 2020). In species with TSD, sex and temperature effects on lifehistory traits are often confounded, and the absence of statistically Frontiers in Physiology frontiersin.org significant sex effects on survival at each stage in this study may be due to the thermal variance incorporated through temperature switches, which could have produced intermediate phenotypes and thus blurred group distinctions.…”

Section: Discussionmentioning

confidence: 97%

Developmental asynchrony might not reduce fitness in early life in painted turtles

2022

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Synchronous hatching and emergence of turtles from nests may be adaptive in predator avoidance during dispersal. However, little is known about the phenotypic consequences of such synchrony or the generality of predator avoidance in driving the evolution of this trait. Colbert et al. (2010) found that less advanced embryos hatched early in the presence of more advanced sibs, sustaining a persistent reduction in neuromuscular function. In this study, we experimentally assessed the influence of such accelerated embryonic development on hatching success, winter survival, and survival during terrestrial dispersal from the nest. Although we predicted that shortened incubation periods would reduce survival, early-hatching individuals suffered no detectable fitness costs at any stage considered in this study. Incubation temperature did not affect hatching success, and offspring sex did not affect survival across treatment groups. Incubation regime influenced offspring body size and was negatively correlated with dispersal time, however, there was no effect on survival during winter or terrestrial dispersal. Lack of a detectable fitness cost in these key early-life stages associated with hatching synchrony is consistent with a single, predator avoidance origin for this trait and retention in C. picta and other derived turtles via phylogenetic inertia.

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Section: Discussionmentioning

confidence: 97%

Developmental asynchrony might not reduce fitness in early life in painted turtles

2022

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“…However, in contrast to the results presented here, the same study showed that turtle hatchlings from the lower, MPT exhibited increased survival relative to their male counterparts incubated under intermediate temperatures promoting the development of both sexes (Janzen, 1995). Clearly, additional studies examining the extent to which incubation temperature influences juvenile survival under field conditions (Janzen, 1995; Warner et al, 2020) and the directionality of this relationship with respect to sex biases in age at maturity are needed to generalize across reptiles exhibiting TSD.…”

Section: Discussionmentioning

confidence: 99%

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

Bock,

Loera,

Johnson

et al. 2023

Functional Ecology

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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.

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“…In addition, the non-linear relationship explains studies where exogenous application of E 2 has unexpectedly produced male hatchlings (e.g. 43,44 ). In such cases, E 2 application, combined with existing maternal contributions, may have resulted in shifting the E 2 :T ratio within the eggs closer to one, forcing male development.…”

Section: Discussionmentioning

confidence: 99%

“…Interestingly, the effects of these hormones on sex determination vary by experiment and species, likely as the results of adaptation to local nesting conditions (e.g. 43,44 ). However, here we show that in sea turtles, a clutch specific threshold exist for feminisation that is the product of an interaction between temperature and maternal hormone transfer.…”

Section: Discussionmentioning

confidence: 99%

Maternally derived sex steroid hormones impact sex ratios of loggerhead sea turtles

Reischig²,

Eizaguirre

2020

Preprint

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An optimal sex ratio is arguably one of the most important demographic traits of species. Rising global temperatures threaten temperature-dependent sex determination (TSD) species with extreme sex ratio bias and ultimately extinction. Because sex steroid hormones can impact sex determination in TSD reptiles, variation in their maternal transfer within the egg yolk may form a buffer mechanism against raising temperatures. We tested this hypothesis by quantifying the effect of maternal oestradiol (E2) and testosterone (T) on offspring sex in a threatened TSD population of loggerhead sea turtles (Caretta caretta). Circulating levels of E2 and T in nesting females, in egg yolks at oviposition and in neonates were measured. Immediately after oviposition, nests were relocated into an in situ experimental hatchery where temperatures were controlled by standardising the incubation depth. We used affinity propagation clustering on hormone profiles guided by incubation duration, to sex individuals from these nests in a non-lethal manner, offering a novel conservation tool for this endangered species. Despite standardised temperatures, we found a large level of variation in the sex ratio of clutches, which correlated in a non-linear manner with maternal investment of the E2:T ratio in egg yolks. Males were produced at equal levels of E2 and T and females were produced on either side of this optimum. Modelling sex ratios for the coming century, we show that maternally-derived hormones form a trans-generational mechanism of TSD plasticity that adjusts offspring sex ratios in endangered sea turtles.

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Sex and Incubation Temperature Independently Affect Embryonic Development and Offspring Size in a Turtle with Temperature-Dependent Sex Determination

Cited by 11 publications

References 68 publications

Developmental asynchrony might not reduce fitness in early life in painted turtles

Developmental asynchrony might not reduce fitness in early life in painted turtles

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

Maternally derived sex steroid hormones impact sex ratios of loggerhead sea turtles

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