Circadian period manifests genetic diversity among and within
natural plant populations
As hypothesized, we found that populations of B. stricta along an
800-m elevational gradient were genetically differentiated in circadian
period of leaf movement, with population averages varying between 21.9 h
and 24.9 h. Thus, the broad-ranging regional population sample in this
study expanded the among-population range of variation by approximately
2 h from that previously described by Salmela et al. (2016) with a
smaller elevational gradient. The only other study to estimate
among-population genetic differentiation in circadian period found that
in Mimulus laciniatus in the California Sierra Nevada, population
averages varied by 1.6 h within ca. 100 km and along an elevational
range of 1000−2600 m (Leinonen et al. 2020). The current 3-h range among
population means accounts for approximately 46 % of the genetic
variation documented among 150 A. thaliana accessions sampled
across the Northern hemisphere (Michael et al. 2003), and for 68 % of
the variation among 191 A. thaliana accessions sampled in Sweden
(Rees et al. 2021). These contrasts are notable because we restricted
our sampling to a considerably narrower geographic range.
Although a high degree of self-fertilization in species like B.
stricta is often expected to erode genetic diversity on a fine spatial
scale (e.g., Wright et al. 2013), a significant effect of maternal
family nested within population showed that genetic variation in
circadian period was present locally, i.e., on a scale of only a few
hundred meters. Further, we observed that the magnitude of
within-population genetic diversity was variable, with eight populations
expressing a genetic range in period length that exceeded four hours.
Variance components indicated that among-population genetic differences
accounted for a slightly larger proportion of total variation in
circadian period than did among-family differences within populations,
but overall, the amounts of genetic diversity at these two levels were
similar. This finding agrees with Song et al. (2006) who found that up
to 40 % of molecular marker diversity segregated within and up to 47 %
segregated among populations in B. stricta , but it differs from
the study by Salmela et al. (2016) in which within-population genetic
diversity in circadian period exceeded that found among populations. The
difference most likely arises from a greater number of populations
sampled in the current study. The 3.5-h within-population range in
genotypic means found by Salmela et al. (2016) is in agreement with the
current results. In M. laciniatus in the Sierra Nevada,
among-population genetic differences explained ca. 12 % of total
variation in circadian period while genetic variation within populations
contributed only ca. 2 % (Leinonen et al. 2020). This interspecific
difference may stem from the contrasting life histories of the two
species: M. laciniatus is a small annual plant with a very rapid
life and a limited distribution in the Sierra Nevada, whereas B.
stricta is a short-lived perennial found across North America. In the
widely distributed M. guttatus in western North America,
within-population genetic variation in circadian period was large
compared to the magnitude of among-population differentiation (Greenham
et al. 2017).
In considering variation in biological rhythms, it is worth reviewing
the observed range of natural genetic variation in circadian rhythms
from the perspective of the classical circadian resonance theory, which
postulates a fitness advantage to endogenous circadian periods whose
length matches that of the exogenous environmental cycle (Dodd et al.
2005, Ouyang et al. 1998, Pittendrigh and Minis 1972, Woelfle et al.
2004). We detected a wide range of genetic variation in circadian period
in natural populations that have experienced only 24-h diel cycles in
their native habitats. This raises the possibility of weak
daylength-imposed natural selection on the trait, which in recent animal
studies has been proposed to explain the considerable variation detected
in period length of locomotor activity within and among three spider
species and in mouse lemurs (Hozer et al. 2020, Mah et al. 2019).
Indeed, these parallel observations across plant and animal species
provide evidence that 24-h exogenous cycles do not select just for
endogenous cycling patterns of a matching length. Considering that
variation in circadian period is not manifested under 24-h environmental
cycles, it is possible that the trait is influenced by selection
indirectly via its association with another circadian trait like phase
that is relevant in a naturally oscillating environment. Indeed,
circadian period and phase are correlated in some (Rees et al. 2021,
Rubin et al. 2017) but not all datasets (Michael et al. 2003) inA. thaliana . Genetic variation in the clock could be affected by
selection on genetically related phenological traits like flowering
time: Salmela et al. (2018) found that maternal families from a single
population of B. stricta that had longer circadian periods tended
to flower earlier and at a larger size after vernalization, and
experimental progeny from controlled crosses of A. thaliana andBrassica rapa accessions indicate that clock traits covary with
shoot growth patterns (Rubin et al. 2018) and photosynthetic traits
(Edwards et al. 2011, Yarkhunova et al. 2019). To identify environmental
factors that may select for natural genetic variation in circadian
period in B. stricta , it is necessary to investigate
among-population differences in relation to the steep spatial
environmental gradients that characterize the study area in the Rocky
Mountains.