Natural variation in circadian period is associated with diverse phenological measures in Boechera stricta

The circadian clock is a time-keeping mechanism that detects and responds to temporal environmental changes. Despite functional hypotheses of circadian resonance, in which the match between endogeneous circadian rhythms and exogenous environmental cycles is presumed to be adaptive, considerable genetic variation is observed in clock parameters. The circadian parameter of period length, for instance, exhibits significant segregating genetic variation within and among populations along an elevational cline in Boechera stricta. This variation might reflect variable selection on circadian timing of biological functions and clock outputs across environmental microsites. Reproductive timing is an important clock output, and selection might favour accelerated or delayed phenology.

We performed a 3 year common garden field study with the short-lived perennial B. stricta (Brassicaceae) to quantify differences in life history. We studied individuals from 20 populations along an elevational gradient and from 20 maternal families derived from a single population. We measured days to bolting and later life-history transitions, such as days to flowering; in the same genotypes, we measured circadian period and assessed correlations between phenology and clock traits.

The timing of all life-history transitions varied among growing seasons, suggesting adaptive life-history evolution to local climate conditions. Life-history transitions after bolting were associated with circadian period, such that lengthened period was correlated with delayed life-history transitions. Structural equation modelling indicated that indirect selection via days to flowering and fruit production favoured lengthened clock period in the low-elevation common garden site.

We found a direct, directional effect of the environment on phenology, and indirect selection on the circadian clock through phenology. Our results suggest that selection on phenology could explain the evolution of variable circadian periods observed among populations from differing environments.