Leaf size and venation show remarkable diversity across dicotyledons, and are key determinants of plant adaptation in ecosystems past and present. Here we present global scaling relationships of venation traits with leaf size. Across a new database for 485 globally distributed species, larger leaves had major veins of larger diameter, but lower length per leaf area, whereas minor vein traits were independent of leaf size. These scaling relationships allow estimation of intact leaf size from fragments, to improve hindcasting of past climate and biodiversity from fossil remains. The vein scaling relationships can be explained by a uniquely synthetic model for leaf anatomy and development derived from published data for numerous species. Vein scaling relationships can explain the global biogeographical trend for smaller leaves in drier areas, the greater construction cost of larger leaves and the ability of angiosperms to develop larger and more densely vascularised lamina to outcompete earlier-evolved plant lineages.

Across plant species, leaves vary enormously in their size and their venation architecture, of which one major function is to replace water lost to transpiration. The leaf hydraulic conductance (K leaf ) represents the capacity of the transport system to deliver water, allowing stomata to remain open for photosynthesis. Previous studies showed that K leaf relates to vein density (vein length per area). Additionally, venation architecture determines the sensitivity of K leaf to damage; severing the midrib caused K leaf and gas exchange to decline, with lesser impacts in leaves with higher major vein density that provided more numerous water flow pathways around the damaged vein. Because xylem embolism during dehydration also reduces K leaf , we hypothesized that higher major vein density would also reduce hydraulic vulnerability. Smaller leaves, which generally have higher major vein density, would thus have lower hydraulic vulnerability. Tests using simulations with a spatially explicit model confirmed that smaller leaves with higher major vein density were more tolerant of major vein embolism. Additionally, for 10 species ranging strongly in drought tolerance, hydraulic vulnerability, determined as the leaf water potential at 50% and 80% loss of K leaf , was lower with greater major vein density and smaller leaf size (|r| = 0.85-0.90; P , 0.01). These relationships were independent of other aspects of physiological and morphological drought tolerance. These findings point to a new functional role of venation architecture and small leaf size in drought tolerance, potentially contributing to well-known biogeographic trends in leaf size.

SummaryPopulus trichocarpa is widespread across western North America spanning extensive variation in photoperiod, growing season and climate. We investigated trait variation in P. trichocarpa using over 2000 trees from a common garden at Vancouver, Canada, representing replicate plantings of 461 genotypes originating from 136 provenance localities.We measured 40 traits encompassing phenological events, biomass accumulation, growth rates, and leaf, isotope and gas exchange-based ecophysiology traits. With replicated plantings and 29 354 single nucleotide polymorphisms (SNPs) from 3518 genes, we estimated both broad-sense trait heritability (H 2 ) and overall population genetic structure from principal component analysis.Populus trichocarpa had high phenotypic variation and moderate/high H 2 for many traits. values reflected trait correlation strength with geoclimate variables. The population genetic structure had one significant principal component (PC1) which correlated with daylength and showed enrichment for genes relating to circadian rhythm and photoperiod. Robust relationships between traits, population structure and geoclimate in P. trichocarpa reflect patterns which suggest that range-wide geographical and environment gradients have shaped its genotypic and phenotypic variability.