Seedling traits from root to shoot exhibit genetic diversity and distinct responses to environmental heterogeneity within a tree population

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.