Adaptations That Track Environmental Temperature Cues in Hibernation: Insights From Time-Series Transcriptomic...

Organisms can use environmental temperature cues to time life-history events and coordinate necessary adaptive physiological adjustments to synchronize with seasonal environmental changes. However, our knowledge about the adaptations that track environmental temperature cues in life-history events remains limited. Hibernation is an important life-history strategy for many animal groups to survive seasonal cold and food scarcity. This study explored the match between physiological adaptations during hibernation and environmental temperature cues by analyzing monthly hepatic transcriptomic profiles in the Chinese three-keeled pond turtle Mauremys reevesii juveniles throughout field hibernation in relation to water temperature change patterns. We illustrated the transcriptomic dynamics indicative of the onset of hibernation, deep hibernation, and the gradual end of hibernation in M. reevesii corresponding to phases of rapid temperature reduction, low temperatures, and temperature rise, respectively. During these stages, in hibernating M. reevesii, we revealed the substantial upregulation of genes involved in protective mechanisms, including anti-apoptotic processes, autophagy, and mRNA stability regulation prior to the coldest period; a coordinated transcriptional suppression of immune-related genes during deep hibernation; and a pre-activation of genes involved in translational processes before emergence when water temperature began to rise. These results suggested active adaptive regulations that track environmental temperature cues in hibernating M. reevesii, rather than merely passive effects of temperature changes. This study provides insights into the adaptations underlying synchronization between life-history events and environmental changes, a process fundamental to phenology, and offers a crucial mechanistic framework for further understanding of the potential effects of climate change on hibernation processes.