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Ambient Temperature as a Strong Zeitgeber of Circadian Rhythms in Response to Temperature Sensitivity and Poor Heat Dissipation Abilities in Subterranean African Mole-Rats

Mammals have evolved circadian rhythms in internal biological processes and behaviors, such as locomotor activity (LA), to synchronize to the environmental conditions they experience. Photic entrainment of LA has been well established; however, non-photic entrainment, such as ambient temperature (Ta), has received much less attention. To address this dearth of knowledge, we exposed two subterranean endothermic-homeothermic African mole-rat species, the solitary Cape mole-rat (Georychus capensis [GC]) and social Mahali mole-rat (Cryptomys hottentotus mahali [CHM]), to varying Ta cycles in the absence of light. We showed that the LA rhythms of these two species entrain to Ta cycles and that the majority of LA occurred during the coolest 12-h period. LA confined to the coolest Ta periods may be the direct consequence of the poor heat dissipation abilities of African mole-rats brought about by physiological and ecological constraints. Recently, it has been hypothesized that Ta is only a strong zeitgeber for circadian rhythms in species whose thermoregulatory abilities are sensitive to changes in Ta (i.e., heterotherms and ectotherms), which previously has excluded endothermic-homeothermic mammals. However, this study demonstrates that Ta is a strong zeitgeber or entrainer for circadian rhythms of LA in subterranean endothermic-homeothermic mammals as a consequence of their sensitivity to changes in Ta brought about by their poor heat dissipation abilities. This study reinforces the intimate link between circadian rhythms and thermoregulation and conclusively, for the first time, provides evidence that Ta is a strong zeitgeber for endothermic-homeothermic mammals.