Collaborative Research: Neuroendocrine Modulation of Circannual Rhythms in Mammals

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Predicting how species might alter their annual timing in response to rapid environmental change, including changes in climate, is constrained by insufficient knowledge of the endogenous mechanisms animals use to keep time, the cues used to adjust timing, and the extent to which programmed seasonal cycles are physiologically malleable or plastic. This project investigates the mechanisms that underlie plasticity in the seasonal induction of the neuroendocrine signals that trigger the termination of hibernation and the onset of reproduction in ground squirrels. Unlike most mammals, ground squirrels spontaneously become reproductively competent in constant darkness, without the stimulus of a changing photoperiod. As such, ground squirrels are an ideal organism for studies examining non-photoperiodic control of reproductive timing. Establishing the neuroendocrine mechanisms responsible for transitions between life-history stages will identify target genes for monitoring adaptive genetic responses to environmental change. This investigation integrates research and learning by training graduate students in ecophysiology and neurophysiology, providing opportunities for undergraduates to participate in laboratory experiments. The project also includes outreach to Alaska Native and American Indian high school students and undergraduates for inclusion in research and aims to increase K-12 students' understanding of and engagement in research by participating in Teacher Research Experience programs. In hibernating mammals, a precise integration must occur between the central nervous system signaling cascades controlling thermoregulation through the termination of torpor and the subsequent activation of the reproductive axis; however, the neuroendocrine modulators that regulate these changes and how they are integrated are unknown. In seasonally breeding, photoperiodic vertebrates, the pars tuberalis (PT) of the pituitary plays an essential role in the timing of annual cycles, as it alters hypothalamic thyroid hormone availability by secreting thyroid stimulating hormone in a light- or melatonin-sensitive manner, which acts on neighboring hypothalamic deiodinase expressing cells. The PT thyrotrophs themselves are now considered strong candidates for circannual timer cells, driving a thyroid-dependent seasonal physiology. This research tests the hypothesis that, in the absence of any photic cues, the termination of torpor and onset of reproduction are triggered by spontaneous changes in hypothalamic thyroid status driven by activation of thyrotroph cells in the PT. Additionally, the project tests the hypothesis that plasticity in timing is driven by temperature-induced changes in hypothalamic deiodinase activity and/or through effects on downstream targets of the triiodothyronine signaling pathway that occur independent of the PT.