Circadian Rhythms and Reproductive Phenology Covary in a Natural Plant Population

The circadian clock is a molecular timekeeper that matches endogenous rhythms in diverse traits with 24-h cycles in the external environment. Although a lack of clock resonance to the environment is detrimental to performance, clock phenotypes in wild populations nevertheless deviate substantially from the predicted optimal cycle length of 24 h, and significant genetic variation exists for circadian parameters. Here, we describe covariation between 2 traits considered to reflect adaptation to different aspects of temporal environmental heterogeneity, circadian rhythms (adaptation to daily environmental cycles) and flowering time (adaptation to seasonal cycles), in a Rocky Mountain population of the mustard Boechera stricta, a North American relative of Arabidopsis thaliana. We found that 18 families that differ in circadian period in leaf movement by 3.5 h expressed genetic diversity in first-year growth, reproductive phenology, vegetative size at reproduction, and starch concentration following vernalization. The families exhibited a large (~90-day) range in mean flowering time, even though the spatial scale of population sampling covered only a few hundred meters. Circadian period covaried with other traits such that longer-period families flowered earlier and at a larger size, a trait combination predicted to yield a fitness benefit in the wild. Circadian clock research in model systems has previously shown that mutations in clock genes influence phenology. Our results widen the scope of this research by illustrating a link between naturally segregating clock variation and reproductive phenology among wild genotypes, suggesting that the causes of genetic diversity in the clock lie partly in adaptation to seasonal environmental heterogeneity.