Embryonic Temperature Affects Metabolic Compensation and Thyroid Hormones in Hatchling Snapping Turtles

Abstract

Temperature acclimation of adult vertebrates typically induces changes in metabolic physiology. During early development, such metabolic compensation might have profound consequences, yet acclimation of metabolism is little studied in early life stages. We measured the effect of egg incubation temperature on resting metabolic rate (RMR) and blood thyroid hormone levels of hatchling snapping turtles (Chelydra serpentina). Like many reptiles, snapping turtles have temperature-dependent sex determination (TSD), in which embryonic temperature determines sex. Therefore, we designed the experiments to separately measure effects of temperature and of sex on the response variables. We incubated eggs in the laboratory at 21. 5 degrees, 24.5 degrees, 27.5 degrees, and 30.5 degrees C, producing both sexes, all males, both sexes, and all females, respectively. Hatchling RMR, when measured at a common temperature (either 25 degrees or 31 degrees C), was negatively correlated with egg temperature in both males and females, such that RMR of turtles from 21.5 degrees C-incubated eggs averaged 160% that of turtles from 30.5 degrees C-incubated eggs. These results indicate that egg temperatures induced positive metabolic compensation in both sexes. Thyroid hormone levels of hatchlings showed similar correlations with egg temperature; thyroxine level of turtles from 21.5 degrees C-incubated eggs averaged 220% that of turtles from 30.5 degrees C-incubated eggs. To examine the possibility that thyroid hormones contribute to positive metabolic compensation, we added triiodothyronine to eggs during mid-incubation. RMR of hatchlings from these treated eggs averaged 131% that of controls, consistent with the previous possibility. Moreover, the effects of embryonic temperature on metabolic physiology, in combination with effects on sex, can result in differences in RMR and thyroid hormone levels between male and female hatchling turtles. Such differences may be important to the ecology and evolution of TSD.

Physiological and morphological correlates of among-individual variation in standard metabolic rate in the leopard frog Rana pipiens

“…Thyroxine supplementation (both T3 and T4) certainly stimulates ectotherm standard metabolic rates (Gupta and Thapliyal, 1991;Joos and John-Alder, 1990). More importantly, however, metabolic rate appears to correlate with endogenous variation of thyroxine levels in both endotherms Stenlof et al, 1993;Toubro et al, 1996) and ectotherms (O'Steen and Janzen, 1999). In the latter study, thyroxine levels of neonatal snapping turtles from different egg incubation temperatures correlated with mean SMR.…”

Embryonic communication in the nest: metabolic responses of reptilian embryos to developmental rates of siblings

“…TH influences tissue accretion and differentiation in a foetus through both metabolic and non-metabolic mechanisms [33]. Critically, TH affects a variety of metabolic pathways, especially energy metabolism, and also plays a role in mammalian and reptilian metabolic responses to temperature acclimation [34]. TH is a key regulator of postnatal growth and the complex process of transition from allantoic to pulmonary respiration [35,36], yet the thyroid also is one of the earliest endocrine organs to differentiate and the metabolic adjustment in our experimental groups may lie with changes in TH.…”

Control of the development of the pulmonary surfactant system in the saltwater crocodile,Crocodylus porosus

“…Forty-eight and twentyfour hours before the sampling day, the embryos were pretreated with water-soluble Dex (2 ϫ 50 g, Sigma, Sydney, Australia), T3 (2 ϫ 5 g, Sigma), or a combination of both hormones (Dex ϩ T3). The doses were based on hormone pretreatment of snapping turtle (40) and chicken eggs (13,68) and scaled up according to the differences in body weights. Dex was dissolved directly in isotonic saline, whereas the T 3 was dissolved in a small volume of 0.1 M NaOH before diluting in isotonic saline.…”