Cold and hunger induce diurnality in a nocturnal mammal.

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.

Strong pituitary and hypothalamic responses to photoperiod but not to 6-methoxy-2-benzoxazolinone in female common voles (Microtus arvalis).

The annual cycle of changing day length (photoperiod) is widely used by animals to synchronise their biology to environmental seasonality. In mammals, melatonin is the key hormonal relay for the photoperiodic message, governing thyroid-stimulating hormone (TSH) production in the pars tuberalis (PT) of the pituitary stalk. TSH acts on neighbouring hypothalamic cells known as tanycytes, which in turn control hypothalamic function through effects on thyroid hormone (TH) signalling, mediated by changes in expression of the type II and III deiodinases (Dio2 and Dio3, respectively). Among seasonally breeding rodents, voles of the genus Microtus are notable for a high degree of sensitivity to nutritional and social cues, which act in concert with photoperiod to control reproductive status. In the present study, we investigated whether the TSH/Dio2/Dio3 signalling pathway of female common voles (Microtus arvalis) shows a similar degree of photoperiodic sensitivity to that described in other seasonal mammal species. Additionally, we sought to determine whether the plant metabolite 6-methoxy-2-benzoxazolinone (6-MBOA), described previously as promoting reproductive activation in voles, had any influence on the TSH/Dio2/Dio3 system. Our data demonstrate a high degree of photoperiodic sensitivity in this species, with no observable effects of 6-MBOA on upstream pituitary/hypothalamic gene expression. Further studies are required to characterise how photoperiodic and nutritional signals interact to modulate hypothalamic TH signalling pathways in mammals.