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Phenotypic diversity within plant species is crucial to shaping evolutionary responses of populations and interactions among species, yet intraspecific genetic variability notably in roots has attracted little attention. Further, evidence for the root–shoot trait synchronisation remains inconclusive, narrowing our understanding of the role that belowground traits play in local adaptation. We applied broad ‘top‐to‐toe’ phenotyping to a model system whose native environmental conditions were simulated in experimental settings. Fifteen maternal families of Norway spruce Picea abies from southern Finland grew in six combinations of two simulated growing seasons and three soil treatments. We scored variation in 25 functional traits, including size, architecture and morphology of intact root systems, and shoot growth and phenology. Careful phenotyping of roots uncovered five trait dimensions, with root size, architecture and morphology forming the three largest axes of variation. Dimensions varied in their treatment responses. We observed among‐family differences in all trait dimensions, marking substantial within‐population genetic diversity. For example, average total root length varied almost twofold among families, but family × soil interactions indicated treatment‐specific estimates of genetic variance. Mirroring root traits, phenotypic plasticity and genetic variation characterised shoot growth and phenology. In all, the complete phenotypic dataset yielded six trait dimensions, with assorted measures of root system and shoot size composing the main axis of variation. Although plastic and genetically variable, root architecture and morphology were not associated with shoot growth in any treatment. Also phenology and root‐to‐shoot ratio were detached from the primary axis of trait variability. Our results demonstrate that complex within‐species patterns of trait covariation can be observed even locally and that phenotypic variation in independent trait dimensions reflecting divergent growth strategies is under genetic control. More accurate predictions of population and species responses to changes in the environment can be achieved when such intraspecific diversity is taken into account.

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.

Circadian clocks have evolved independently in all three domains of life, and fitness benefits of a functional clock have been demonstrated in experimental genotypes in controlled conditions. Still, little is known about genetic variation in the clock and its fitness consequences in natural populations from heterogeneous environments. Using Wyoming populations of the Arabidopsis relative Boechera stricta as our study system, we demonstrate that genetic variation in the clock can occur at multiple levels: means of circadian period among populations sampled at different elevations differed by less than 1 h, but means among families sampled within populations varied by as much as 3.5 h. Growth traits also varied among and within populations. Within the population with the most circadian variation, we observed evidence for a positive correlation between period and growth and a negative correlation between period and root-to-shoot ratio. We then tested whether performance tradeoffs existed among families of this population across simulated seasonal settings. Growth rankings of families were similar across seasonal environments, but for root-to-shoot ratio, genotype × environment interactions contributed significantly to total variation. Therefore, further experiments are needed to identify evolutionary mechanisms that preserve substantial quantitative genetic diversity in the clock in this and other species.

Spatial heterogeneity in environmental conditions has led to adaptive genetic differentiation and the development of home-site fitness advantage (local adaptation) among populations of many widespread plant species such as forest trees. Although its overall patterns have been well characterised, earlier studies on adaptation have predominantly used long-term averages of environmental variables to describe local climates. Subsequently, only little is currently known about more complex patterns of variation in potential selective forces and how they affect adaptive processes. Furthermore, we also lack a good understanding of why adaptive traits often vary within populations despite clear evidence of local selection. Because the capacity of a population to respond to changes in its home environment depends on the amount of genetic variation that it contains, an understanding of these patterns is fundamental to predicting how extant populations will cope with climate change. In this paper, I call attention to these two issues and discuss adaptation in heterogeneous environments using studies mainly on Finnish populations of Scots pine ( Pinus sylvestris L.) as an example. In this geographic area, population means in growth cessation are closely related to the latitude at the population’s home site, indicating adaptation to local environments. Yet the trait varies considerably also within populations, with the highest levels of phenotypic variation found in the central part of the latitudinal gradient. Increased variation further north may have a significant genetic component. In stable local environments this would indicate that populations with less variation are more optimally adapted to their home site environments. On the other hand, climate data show that growing season temperature conditions within Finland become temporally more variable towards the north which might contribute to different levels of trait variation. Collectively, these findings demonstrate the weaknesses of focusing only on long-term averages of environmental variables or trait means when examining adaptation in natural populations. Moreover, better integrated analyses of both genetic and environmental variation might help in disentangling the mechanisms that maintain adaptive genetic diversity and adaptive capacity in natural populations of perennial species under changing environmental conditions.

Environment-driven genetic differentiation among populations is a common feature among forest trees, and an understanding of how populations have adapted to their home site conditions is essential for management and conservation practices. In Scotland, 84 native Scots pine ( Pinus sylvestris L.) woodlands are recognised by the Forestry Commission and they occupy highly diverse environments from the maritime west coast to continental sites in eastern Scotland. However, it is not known whether adaptations to local environments along sharp temperature and rainfall gradients have occurred in different populations and as a result, the seed transfer guidelines of the species are based only on data from isozymes and monoterpenes. In this study of an outdoor common-garden trial, we used chlorophyll fluorescence to examine whether seedlings from 32 open-pollinated families and eight populations from sites experiencing contrasting annual temperature regimes differed in their response to variation in natural outdoor temperatures between September 2009 and May 2010. In addition, growth initiation in spring was recorded. Photochemical capacity at photosystem II F v /F m showed a distinct seasonal trend and remained at relatively high levels (∼0.7) until November. Following a period of over 2 weeks with temperatures below or close to 0 °C, F v /F m started decreasing towards its minimum values recorded in early March when population means varied between 0.35 and 0.45. By early May and along with rising temperatures, photochemical capacity had recovered to the same level as observed in early November. Populations were found to respond differently to the cold period starting in December. The largest drop in photochemical capacity was observed in seedlings from a low-altitude population located in the maritime western Scotland, while in seedlings from higher-altitude locations in the cooler eastern Scotland, the response was smaller. In March, the recovery of photochemical capacity was slowest in seedlings from the mildest and coolest sites. Evidence of adaptive genetic differentiation was also found in spring phenology. Initiation of shoot elongation and needle flush were earlier in families from higher altitudes (cooler areas), but population differences were not significant at the α = 0.05 level. These results suggest that adaptation to the spatially heterogeneous environment in Scotland has taken place in Scots pine and that in order to minimise the risk of planting maladapted seed stock, the patterns of environmental and adaptive genetic variation should be taken into account in the management of genetic resources in this species.

Understanding the present-day distribution of molecular variation requires knowledge about the history of the species. Past colonization routes and locations of refugia of Scots pine (Pinus sylvestris) were inferred from variation in mitochondrial DNA in material collected from 37 populations located in countries within, and immediately adjacent to the continent of Europe. Two mitochondrial regions, nad1 intron (exon B/C) and nad7 intron 1, were included in the study. Differentiation in maternally inherited mitochondria was high (G ST′ = 0.824). Two new haplotypes were found at the nad7 intron 1. The occurrence of a 5-bp indel variant was restricted to the Turkish Kalabak population and a 32 bp only found in Central, Eastern, and Northern Europe. The complete absence of the 32-bp indel from the Mediterranean peninsulas supports the view that coniferous forests existed outside these areas during the last glacial maximum, and these populations contributed to the subsequent colonization of the northern parts of Europe. P. sylvestris shares features of its glacial and postglacial history with two other northern, cold-tolerant tree species, Picea abies and Betula sp. These three species differ from many other European trees for which pollen core and molecular evidence indicate colonization from southern refugia after the last glacial period.

Nucleotide polymorphism at 12 nuclear loci was studied in Scots pine populations across an environmental gradient in Scotland, to evaluate the impacts of demographic history and selection on genetic diversity. At eight loci, diversity patterns were compared between Scottish and continental European populations. At these loci, a similar level of diversity (θ(sil)= ~0.01) was found in Scottish vs mainland European populations, contrary to expectations for recent colonization, however, less rapid decay of linkage disequilibrium was observed in the former (ρ=0.0086±0.0009, ρ=0.0245±0.0022, respectively). Scottish populations also showed a deficit of rare nucleotide variants (multi-locus Tajima's D=0.316 vs D=-0.379) and differed significantly from mainland populations in allelic frequency and/or haplotype structure at several loci. Within Scotland, western populations showed slightly reduced nucleotide diversity (π(tot)=0.0068) compared with those from the south and east (0.0079 and 0.0083, respectively) and about three times higher recombination to diversity ratio (ρ/θ=0.71 vs 0.15 and 0.18, respectively). By comparison with results from coalescent simulations, the observed allelic frequency spectrum in the western populations was compatible with a relatively recent bottleneck (0.00175 × 4N(e) generations) that reduced the population to about 2% of the present size. However, heterogeneity in the allelic frequency distribution among geographical regions in Scotland suggests that subsequent admixture of populations with different demographic histories may also have played a role.