Sex or candy? Neuroendocrine regulation of the seasonal transition from courtship to feeding behavior in male red-sided garter snakes (Thamnophis sirtalis parietalis)

Seasonal modulation of glucocorticoids plays an important role in supporting critical life-history events, and probably facilitates transitions between different life-history stages. In a well-studied population of red-sided garter snakes (Thamnophis sirtalis parietalis), glucocorticoids are elevated during the mating season, but males dispersing to summer feeding grounds have significantly lower baseline glucocorticoids than courting males at the den. We tested the hypothesis that decreased plasma glucocorticoids mediate the behavioral switch between reproduction and foraging in this species. Using a two-choice Y-maze paradigm, we demonstrate that males treated with the glucocorticoid synthesis inhibitor metyrapone (1 and 3 mg implants) prefer feeding cues (worm trail) over reproductive cues (female pheromone trail) significantly earlier than control-treated snakes. The metyrapone-induced changes in appetitive feeding behavior were independent of changes in plasma androgens and body mass loss. Metyrapone-treated males continued to court females at levels similar to those of control-treated snakes, suggesting that appetitive reproductive and ingestive behaviors are not mutually exclusive during this life-history transition. Consistent with this hypothesis, metyrapone treatment did not alter the number of arginine vasotocin-immunoreactive cells in any brain region, while it significantly increased neuropeptide Y-immunoreactive cell number in both the cortex and nucleus sphericus (homologues of the mammalian hippocampus and amygdala, respectively). Our results suggest that male red-sided garter snakes have the potential to maximize reproductive opportunities by continuing to court females they encounter even as they disperse from the den in search of food. Taken together, these data have important implications for understanding the neuroecology of seasonal life-history transitions.