Hummingbird torpor recapitulates key molecular signatures of hibernation without large-scale transcriptomic remodelling

Abstract

Torpor is a physiological strategy used by which some species conserve energy by lowering metabolic rates and body temperatures. While mammalian hibernation is well-studied, the molecular mechanisms governing the rapid entry into avian torpor remain poorly understood. This study represents the first multi-tissue whole-transcriptomic analysis of torpor entry in an avian system. By combining real-time thermal imaging and respirometry with transcriptomic profiling across seven tissues, we identified the key molecular pathways orchestrating this transition in Anna's hummingbirds (Calypte anna). Our results reveal that avian torpor entry is characterised by a subtle transcriptomic change (<5% of the genome differentially expressed across tissues) compared to mammalian hibernation (10%-60%). Most of these genes are differentially expressed before torpor entry is complete, rather than tracking body temperature linearly. This indicates that active transcriptional reprogramming precedes and potentially drives the transition. Thus, hummingbird torpor entry is not a passive shutdown, but a highly regulated, tissue-specific process. Vital organs, such as the heart and lungs, remain transcriptionally stable to maintain essential functions, while the liver and gut exhibit extensive metabolic rewiring. We found evidence of global transcriptional and translational suppression, and cell-cycle arrest: the three major contributors to cellular energy budgets. We hypothesise that avian torpor entry is orchestrated through an arrest of apoptosis, a metabolic switch from carbohydrate to lipid utilisation, coupled with alterations in alternative splicing and circadian rhythm regulation. Finally, the counterintuitive upregulation of genes involved in mitochondrial metabolism suggests a preparation for rapid arousal despite the depressed metabolic state.