Temperature-induced Activation of the Reproductive Axis through Melatonin-mediated Changes in Thyrotropin

An animal\u27s ability to synchronize life-history events or stages with optimal environmental conditions is paramount to successfully reproducing and maximizing fitness. Additional events including migration, foraging, rearing of young, and emergence from hibernation are all examples of processes under environmental control in one species or another. An exciting new mechanism involving neural thyroid hormone metabolism has been elucidated that links environmental control to the neuroendocrine reproductive axis. In birds and mammals with seasonal breeding cycles, this neuroendocrine pathway is activated by photoperiod-induced changes in thyroid stimulating hormone (TSH, also known as thyrotropin) production within the pars tuberalis region of the pituitary. Thyrotropin then alters neural thyroid hormone metabolism in the hypothalamus to stimulate the release of gonadatropin-releasing hormone (GnRH). Melatonin, the primary hormone produced by the pineal gland, has long been known as the primary transducer of photoperiod and thermoperiod in seasonally breeding animals. It is possible that this mechanism is conserved across all seasonally breeding vertebrates and that the mechanism itself is directly linked to reproductive physiological changes. Through melatonin manipulation we experimented to see if melatonin directly mediates the effects of thermoperiod on hypothalamic thyroid hormone metabolism the same way it mediates the effects of photoperiod in seasonal breeding vertebrates. In this study we used the red-sided garter snake (Thamnophis sirtalis parietalis), an ectothermic vertebrate that is known to be a temperature-activated seasonal breeder, to investigate changes in thyrotropin stimulating hormone (TSH) and courtship behavior at different hibernation temperatures (4°C or 12°C) and with different melatonin treatments: the melatonin precursor 5-hydroxytryptophan (5-HTP) or the melatonin receptor antagonist luzindole. Males that hibernated at the ecologically relevant temperature of 4°C exhibited a significant decrease in TSH immunoreactivity within the median eminence area of the hypothalamus, an effect that was reversed in males treated with the melatonin precursor 5-HTP. Additionally, males hibernated at 4°C and treated with 5-HTP had significantly lower courtship intensity. Males hibernated at a warmer 12°C temperature, with or without luzindole treatment, did not show any difference in TSH immunoreactivity or mating behavior. These results suggest that while changes in melatonin may be necessary for transducing the effects of low-temperature exposure on the reproductive axis, melatonin is not sufficient in overriding the influence of elevated hibernation temperatures. Together, these results indicate that more research is needed if we are to understand the mechanisms by which increases in environmental temperature will impact physiology and behavior