Energy homeostasis in an extreme vertebrate: Relationships between life-history status and the molecular stress response in red-sided garter snakes

Vertebrates experience diverse and unique life-history events, many of which are annual and energetically taxing. Energy is a limited resource and thus its careful budgeting is critical for successful transitions between life-history states and across the lifetime of a species. Glucocorticoids (GCs) regulate vertebrate energetics via partitioning of energy use and storage in metabolic tissues (liver, fat, muscle) and exert their effects through activation of two main receptor types, the glucocorticoid receptor (GR), responsible for mobilization of energy from storage tissues, and the mineralocorticoid receptor (MR), responsible for ion balance and osmotic homeostasis. Species adapted to extreme environments carefully balance expression of these two receptors to manage their energy allocation as they transition through demanding events such as mating and migration. A vertebrate with extreme annual life-history is the red-sided garter snake (Thamnophis sirtalis parietalis). In the northern extent of their range (Inwood, Manitoba, Canada), individual red-sided garter snakes emerge after an eight-month dormancy and engage in a short but explosive breeding event followed by a demanding migration, all while in a non-feeding state. To prioritize reproduction, behavioral sensitivity to capture stress and subsequent elevation of glucocorticoids is suppressed during the mating season but is restored upon transition to feeding. The brain-based mechanisms involved are partially characterized; however, peripheral endocrine processes, namely GC receptor expression in metabolic tissues, are understudied. To test the hypothesis that GR and MR work in concert to regulate energy budgets in red-sided garter snakes, I first observed expression of both receptors in spring at two mating dens and along the migratory transition. I then administered low and high doses of GCs to male garter snakes in a summer feeding state to experimentally modulate receptor expression. I found sex- and location-specific differences in expression of GR but not MR. Females had higher expression levels of liver GR compared to males, and females overwintering in at the Middle Den had higher GR expression and lower body condition compared to conspecifics from the Main Den. Administration of GCs showed no significant dose-specific effects in liver GR, possibly indicating that energy use is localized to other parts of the male body such as muscle. This is the first study to characterize GR and MR in the red-sided garter snake, and results from this study illuminate intimate but complex relationships between life-history, overwintering locations, and molecular energy budgeting with implications that may extend to other vertebrate systems demonstrating extreme adaptations.

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