Hummingbird torpor recapitulates key molecular signatures of hibernation without large-scale transcriptomic remodelling
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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.
Significance Statement
Torpor allows animals to dramatically reduce energy expenditure during periods of energetic deficit, yet its molecular regulation in non-mammals remains poorly understood. Using multi-tissue transcriptomics, we examined the transition from normothermy to deep torpor in Anna’s hummingbirds. Surprisingly, tissues undergo limited transcriptomic remodeling (1–4% of genes differentially expressed per tissue), unlike mammalian hibernators (∼15–60%). Hummingbirds regulate key pathways shared with mammals—arresting translation, transcription, and the cell cycle while priming mitochondrial metabolism for rapid arousal—but achieve them with minimal transcriptomic reorganization. The degree of transcriptomic changes observed, despite these interesting findings, suggest that avian torpor may rely more heavily on post-transcriptional and post-translational regulation than previously appreciated and provides a molecular framework for understanding the evolution of dormancy across vertebrates.
