Is the torpor-arousal cycle of hibernation controlled by a non-temperature-compensated circadian clock?

Abstract

During the hibernation season, mammalian hibernators alternate between prolonged bouts of torpor with a reduced body temperature (Tb) and short arousals with a return to euthermy. Evidence is presented here to show that this metabolic-and also physiological and neuroanatomical-rhythm is controlled by a clock, the torpor-arousal (TA) clock. The temperature dependence of torpor bout duration in 3 species of Spermophilus (published data) may be described by assuming that the TA clock is a circadian clock (probably not the suprachiasmatic clock) that has lost its temperature compensation. This loss might result either from a permanent deletion, or more likely from a seasonal epigenetic control at the level of the clock gene machinery. This hypothesis was verified over the full Tb range on published data from 5 other species (a monotreme, a marsupial, and 3 placental mammals). In a hibernation season, instantaneous subjective time of the putative TA clock was summated over each torpor bout. For each animal, torpor bout length (TBL) was accurately predicted as a constant fraction of a subjective day, for actual durations in astronomical time varying between 4 and 13 to 20 days. The resulting temperature dependence of the interval between arousals predicts that energy expenditure over the hibernation season will be minimal when Tb is as low as possible without eliciting cold thermogenesis.