title: Cold and hunger induce diurnality in a nocturnal mammal.
abstract: 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.
authors.affiliation: Chronobiology Unit, Centre for Behaviour and Neurosciences, University of Groningen, 9747 AG, Groningen, The Netherlands; and.
authors.forename: Vincent
authors.initials: V
authors.lastname: van der Vinne
authors.affiliation: Chronobiology Unit, Centre for Behaviour and Neurosciences, University of Groningen, 9747 AG, Groningen, The Netherlands; and.
authors.forename: Sjaak J
authors.initials: SJ
authors.lastname: Riede
authors.affiliation: Chronobiology Unit, Centre for Behaviour and Neurosciences, University of Groningen, 9747 AG, Groningen, The Netherlands; and.
authors.forename: Jenke A
authors.initials: JA
authors.lastname: Gorter
authors.affiliation: Chronobiology Unit, Centre for Behaviour and Neurosciences, University of Groningen, 9747 AG, Groningen, The Netherlands; and.
authors.forename: Willem G
authors.initials: WG
authors.lastname: Eijer
authors.affiliation: Department of Biology, University of Virginia, Charlottesville, VA 22908.
authors.forename: Michael T
authors.initials: MT
authors.lastname: Sellix
authors.affiliation: Department of Biology, University of Virginia, Charlottesville, VA 22908.
authors.forename: Michael
authors.initials: M
authors.lastname: Menaker
authors.affiliation: Chronobiology Unit, Centre for Behaviour and Neurosciences, University of Groningen, 9747 AG, Groningen, The Netherlands; and.
authors.forename: Serge
authors.initials: S
authors.lastname: Daan
authors.affiliation: Chronobiology Unit, Centre for Behaviour and Neurosciences, University of Groningen, 9747 AG, Groningen, The Netherlands; and.
authors.forename: Violetta
authors.initials: V
authors.lastname: Pilorz
authors.affiliation: Chronobiology Unit, Centre for Behaviour and Neurosciences, University of Groningen, 9747 AG, Groningen, The Netherlands; and r.a.hut@rug.nl.
authors.forename: Roelof A
authors.initials: RA
authors.lastname: Hut
mesh_terms: D000818:Animals; D001522:Behavior, Animal; D002940:Circadian Rhythm / Q000502:physiology*; D003080:Cold Temperature; D004734:Energy Metabolism; D006815:Hunger; D008297:Male; D051379:Mice; D008808:Mice, Inbred CBA; D009446:Neurobiology; D009473:Neuronal Plasticity; D056950:Period Circadian Proteins / Q000378:metabolism / Q000502:physiology; D017440:Photoperiod; D013493:Suprachiasmatic Nucleus / Q000502:physiology*; D013696:Temperature
chemical_list: C513312:Per2 protein, mouse; D056950:Period Circadian Proteins
keywords: behavioral neurobiology; behavioral plasticity; chronotype ecology; circadian rhythms