Association between mammalian lifespan and circadian free-running period: the circadian resonance hypothesis revisited

Abstract

Biological rhythms that oscillate with periods close to 24 h (circadian cycles) are pervasive features of mammalian physiology, facilitating entrainment to the 24 h cycle generated by the rotation of the Earth. In the absence of environmental time cues, circadian rhythms default to their endogenous period called tau, or the free-running period. This sustained circadian rhythmicity in constant conditions has been reported across the animal kingdom, a ubiquity that could imply that innate rhythmicity confers an adaptive advantage. In this study, we found that the deviation of tau from 24 h was inversely related to the lifespan in laboratory mouse strains, and in other rodent and primate species. These findings support the hypothesis that misalignment of endogenous rhythms and 24 h environmental cycles may be associated with a physiological cost that has an effect on longevity.

Figure 1.

(a) Relationship between tau-24 and lifespan (time to 75% failure, i.e. when 75% of the animals have died) in nine strains of laboratory mouse (values are mean ± s.e.m.; r² = 0.7; p < 0.01). (b) relationship between tau-24 and maximum lifespan of 13 primates (Otolemur garnettii, Aotus trivirgatus, Aotus lemurinus griseimembra, Microcebus murinus, Homo sapiens, Saimiri sciureus, Macaca mulatta, Macaca fascicularis, Callithrix jacchus, Macaca nemestrina, Aotus azarai boliviensis, Galago senegalensis, Eulemur fulvus albifrons) (r² = 0.33; p < 0.05). (c) relationship between tau-24 and maximum lifespan of 25 rodents (Mesocricetus auratus, Phodopus sungorus, Mus musculus, Rattus norvegicus, Ammospermophilus leucurus, Arvicanthis niloticus, Cryptomys damarensis, Georychus capensis, Acomys russatus, Cryptomys hottentotus, Heterocephalus glaber, Rhabdomys pumilio, Spalax ehrenbergi, Octodon degus, Peromyscus maniculatus, Dipodomys merriami, Tamiasciurus hudsonicus, Tamias striatus, Sigmodon hispidus, Glaucomys volans, Meriones unguiculatus, Peromyscus leucopus, Tamias sibiricus, Lemniscomys barbarus and Spalacopus cyanus) (r² = 0.16; p < 0.05).