Natural selection against a circadian clock gene mutation in mice

TY - JOUR

T1 - Natural selection against a circadian clock gene mutation in mice

AU - Spoelstra, K.

AU - Wikelski, Martin

AU - Daan, Serge

AU - Loudon, Andrew

AU - Hau, Michaela

N1 - AnE, 6013; Data Archiving: data archived at Dataverse NL

PY - 2016

Y1 - 2016

N2 - Circadian rhythms with an endogenous period close 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 in mice bearing a short-period mutation in the enzyme casein kinase 1 (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, hetero- or 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 months, the relative frequency of the tau allele dropped from initial parity to 20%. Adult survival and recruitment of juveniles into the population contributed about 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 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.

AB - Circadian rhythms with an endogenous period close 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 in mice bearing a short-period mutation in the enzyme casein kinase 1 (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, hetero- or 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 months, the relative frequency of the tau allele dropped from initial parity to 20%. Adult survival and recruitment of juveniles into the population contributed about 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 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.

KW - circadian rhythms

KW - survival

KW - reproduction

KW - resonance

KW - tau mutation

KW - international

UR - http://hdl.handle.net/10411/20660

U2 - 10.1073/pnas.1516442113

DO - 10.1073/pnas.1516442113

M3 - Article

SN - 0027-8424

VL - 113

SP - 686

EP - 691

JO - Proceedings of the National Academy of Sciences of the United States of America

JF - Proceedings of the National Academy of Sciences of the United States of America

IS - 3

ER -