Genetic variation in circadian period follows an elevational
gradient in the Rocky Mountains
We detected limited spatial autocorrelation in our data, indicating that
in rare cases spatially adjacent populations exhibited similar
population averages or ranges of within-population genetic variation. On
the whole, we found evidence for a moderate negative association between
elevation and population averages of circadian period in our sample.
This trend may be an outcome of populations sampled close to and above
3000 m exhibiting averages below 24 h while for instance at ca. 2700 m
the full range of among-population genetic variation was evident.
Similarly, the range of within-population genetic variation decreased
towards higher elevations, which agrees with the results of Salmela et
al. (2016) and which may result from more intense selection in marginal
habitats with long winters and limited growing seasons and resources.
We estimated home site conditions of the populations using the WorldClim
data (Fick and Hijmans 2017) and found evidence for pronounced
temperature and precipitation gradients along the 800-m elevational
range, with estimates of average annual temperature varying from ca. +4
°C at 2500 m to ca. −1 °C at 3400 m. This pattern denotes that growing
seasons begin at different timepoints and photoperiods depending on the
elevation: by June, the two highest-elevation sites may have yet to
reach a monthly mean of +5 °C. On the other hand, average precipitation
was estimated to increase towards higher elevations, while soil pH was
lower at higher elevations. Although we found that elevation explained a
larger proportion of genetic diversity in circadian period (22 %) than
did latitude in A. thaliana (Michael et al. 2003, Rees et al.
2021), variation was still largely residual, suggesting that complex
spatial gradients are behind the observed levels of diversity.
Contrastingly, in M. laciniatus in the California Sierra Nevada,
circadian period was not linearly related to elevation although the
WorldClim data indicated a strong association between elevation and
temperature conditions (Leinonen et al. 2020). Importantly, the
WorldClim data provide model-based estimates for a given location with a
1 × 1 km grid, which may mask substantial micro-environmental
heterogeneity in complex mountainous landscapes. When a species is found
in highly divergent environments, it is possible that different
environmental factors drive local adaptation even across adjacent
populations. This has been noted for instance in M. guttatus in
California, where coastal and inland populations seem to be influenced
by divergent selective agents (Popovic and Lowry 2020). Such
differentiation might give rise to large-scale spatial clines in
quantitative traits with consequential levels of unexplained variation.
A population-level survey on reproductive phenology in this species has
yet to be conducted, but in the study by Anderson and Gezon (2014),
which sampled one maternal family of B. stricta per location in
Colorado at 2800−3700 m, higher-elevation genotypes tended to flower
earlier in common garden. Consequently, selection on photoperiodic
responses could be a contributing factor to the diversity of circadian
period among populations. Beside the circadian clock, other traits will
need to be investigated in the same genetic origins to understand
adaptation in this species more comprehensively and to uncover the
mechanisms that help maintain significant genetic diversity within
populations. A limitation of the WorldClim data is that it does not
provide information on the extent of potential among-year variation in
temperature conditions in the region. However, weather station data from
the Rocky Mountains reveal long-term annual variability for instance in
spring temperatures and timing of snowmelt, which in turn are correlated
with timing of flowering in nearby plant populations (Anderson et al.
2012). Genetic variation in the circadian clock might be sustained
across short spatial distances within populations if selection on
circadian period – or on a closely correlated trait − varied in
strength or direction in response to such environmental fluctuations.
Causes of very spatially localized genetic diversity in nature are often
poorly understood (e.g., Delph and Kelly 2014), but in A.
thaliana on the Iberian Peninsula, spatially and temporally replicated
field experiments provide evidence that fluctuating natural selection
could preserve genetic variation for instance in phenology within
populations (Exposito-Alonso et al. 2018).