Cold and hunger induce diurnality in a nocturnal mammal

• Published in: Proceedings of the National Academy of Sciences - PNAS Vol. 111; no. 42; pp. 15256 - 15260
• Main Authors: van der Vinne, Vincent, Riede, Sjaak J., Gorter, Jenke A., Eijer, Willem G., Sellix, Michael T., Menaker, Michael, Daan, Serge, Pilorz, Violetta, Hut, Roelof A.
• Format: Journal Article
• Language: English
• Published: United States National Academy of Sciences 21-10-2014; National Acad Sciences
• Subjects: Animal nesting; Animals; Behavior, Animal; Biological rhythms; Biological Sciences; Circadian rhythm; Circadian Rhythm - physiology; Cold Temperature; Energy Metabolism; Gene expression; Genotype & phenotype; Hunger; Male; Mammals; Metabolism; Mice; Mice, Inbred CBA; Neurobiology; Neuronal Plasticity; Period Circadian Proteins - metabolism; Period Circadian Proteins - physiology; Phenotypes; Photoperiod; Simulation; Suprachiasmatic Nucleus - physiology; Surface temperature; Temperature; Workloads; chronotype ecology; behavioral neurobiology; behavioral plasticity; circadian rhythms
• ISSN: 0027-8424; 1091-6490
• DOI: 10.1073/pnas.1413135111

Significance The circadian system drives daily rhythms in physiology and behavior. Mammals in nature can change their daily activity rhythms, but causes and consequences of this behavioral plasticity are unknown. Here we show that nocturnal mice become diurnal when challenged by cold or hunger. Negative energy balance changes hormonal, physiological and behavioral rhythms without modifying the rhythm of the circadian pacemaker in the suprachiasmatic nucleus. This response is adaptive because activity during daytime warmth and resting in a buffered environment during the cold nighttime generally reduces energy expenditure. This mechanism may explain why nighttime activity in humans generally evokes higher energy uptake and subsequent obesity and metabolic syndrome, as seen in late chronotypes and night shift workers.
The mammalian circadian system synchronizes daily timing of activity and rest with the environmental light–dark cycle. Although the underlying molecular oscillatory mechanism is well studied, factors that influence phenotypic plasticity in daily activity patterns (temporal niche switching, chronotype) are presently unknown. Molecular evidence suggests that metabolism may influence the circadian molecular clock, but evidence at the level of the organism is lacking. Here we show that a metabolic challenge by cold and hunger induces diurnality in otherwise nocturnal mice. Lowering ambient temperature changes the phase of circadian light–dark entrainment in mice by increasing daytime and decreasing nighttime activity. This effect is further enhanced by simulated food shortage, which identifies metabolic balance as the underlying common factor influencing circadian organization. Clock gene expression analysis shows that the underlying neuronal mechanism is downstream from or parallel to the main circadian pacemaker (the hypothalamic suprachiasmatic nucleus) and that the behavioral phenotype is accompanied by phase adjustment of peripheral tissues. These findings indicate that nocturnal mammals can display considerable plasticity in circadian organization and may adopt a diurnal phenotype when energetically challenged. Our previously defined circadian thermoenergetics hypothesis proposes that such circadian plasticity, which naturally occurs in nocturnal mammals, reflects adaptive maintenance of energy balance. Quantification of energy expenditure shows that diurnality under natural conditions reduces thermoregulatory costs in small burrowing mammals like mice. Metabolic feedback on circadian organization thus provides functional benefits by reducing energy expenditure. Our findings may help to clarify relationships between sleep–wake patterns and metabolic phenotypes in humans.