Evolving the structure: climatic and developmental constraints on the evolution of plant architecture. A case study in Euphorbia.

Plant architecture strongly influences ecological performance, yet its role in plant evolution has been weakly explored. By testing both phylogenetic and environmental signals, it is possible to separate architectural traits into four categories: development constraints (phylogenetic signal only); convergences (environmental correlation only); key innovations to the environmental driver (both); unknown (neither).

We analysed the evolutionary history of the genus Euphorbia, a model clade with both high architectural diversity and a wide environmental range. We conducted comparative analysis of 193 Euphorbia species taken worldwide using 73 architectural traits, a dated phylogeny, and climate data.

We identified 14 architectural types in Euphorbia based on trait combinations. We found 26 traits and 3 types representing convergences under climate groups; 16 traits and 4 types showing phylogenetic signal but no relation to climate; and 31 traits and 5 types with both climate and phylogenetic signals.

Major drivers of architectural trait evolution probably include water stress in deserts (selected for succulence, continuous branching), frost disturbance in temperate systems (selected for simple, prostrate, short-lived shoots) and light competition (selected for arborescence). Simple architectures allowed resilience to disturbance, and frequent transitions into new forms. Complex architectures with functional specialisation developed under stable climates but have low evolvability.