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Proc Natl Acad Sci U S A. 2016 Jan 19;113(3):686-91. doi: 10.1073/pnas.1516442113. Epub 2015 Dec 29.

Natural selection against a circadian clock gene mutation in mice.

Author information

1
Department of Ecology and Evolutionary Biology, Princeton University, Princeton, NJ 08544; Department of Migration and Immuno-Ecology, Max Planck Institute for Ornithology, D-78315 Radolfzell, Germany; K.Spoelstra@nioo.knaw.nl.
2
Department of Ecology and Evolutionary Biology, Princeton University, Princeton, NJ 08544; Department of Migration and Immuno-Ecology, Max Planck Institute for Ornithology, D-78315 Radolfzell, Germany; Department of Biology, University of Konstanz, D-78457 Konstanz, Germany;
3
Unit of Chronobiology, Institute of Evolutionary Life Sciences, University of Groningen, 9747 AG Groningen, The Netherlands;
4
Faculty of Life Sciences, University of Manchester, Manchester M13 9PL, United Kingdom;
5
Department of Ecology and Evolutionary Biology, Princeton University, Princeton, NJ 08544; Department of Biology, University of Konstanz, D-78457 Konstanz, Germany; Evolutionary Physiology Group, Max Planck Institute for Ornithology, D-82319 Seewiesen, Germany.

Abstract

Circadian rhythms with an endogenous period close to or equal to the natural light-dark cycle are considered evolutionarily adaptive ("circadian resonance hypothesis"). Despite remarkable insight into the molecular mechanisms driving circadian cycles, this hypothesis has not been tested under natural conditions for any eukaryotic organism. We tested this hypothesis in mice bearing a short-period mutation in the enzyme casein kinase 1ε (tau mutation), which accelerates free-running circadian cycles. We compared daily activity (feeding) rhythms, survivorship, and reproduction in six replicate populations in outdoor experimental enclosures, established with wild-type, heterozygous, and homozygous mice in a Mendelian ratio. In the release cohort, survival was reduced in the homozygote mutant mice, revealing strong selection against short-period genotypes. Over the course of 14 mo, the relative frequency of the tau allele dropped from initial parity to 20%. Adult survival and recruitment of juveniles into the population contributed approximately equally to the selection for wild-type alleles. The expression of activity during daytime varied throughout the experiment and was significantly increased by the tau mutation. The strong selection against the short-period tau allele observed here contrasts with earlier studies showing absence of selection against a Period 2 (Per2) mutation, which disrupts internal clock function, but does not change period length. These findings are consistent with, and predicted by the theory that resonance of the circadian system plays an important role in individual fitness.

KEYWORDS:

circadian rhythms; reproduction; resonance; survival; tau mutation

PMID:
26715747
PMCID:
PMC4725470
DOI:
10.1073/pnas.1516442113
[Indexed for MEDLINE]
Free PMC Article

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