Abstract
The diversification of flowers, largely driven by mutualistic interactions with animal pollinators, has generated remarkable variation in floral form and size and is thought to have driven the evolutionary radiation of angiosperms. Here, we investigate the geographic variation in reproductive organ growth in the self-fertilizing species Arabidopsis thaliana, where the loss of pollinator dependence is predicted to favour reduced floral investment through resource reallocation. We find extensive variation in flower size underpinned by a polygenic architecture, in which derived alleles both increase and decrease petal size and show signatures of positive selection. The direction of flower-size evolution varies geographically, reflecting environmentally mediated shifts in the relationship between flower size and seed production. Strong purifying selection at the species' climatic margins favors smaller flowers, whereas relaxed environmental constraints in more suitable habitats allow the persistence and potential adaptive value of large-flower variants. This biogeographic pattern extends to other life-history traits, illustrating how environmental heterogeneity, acting through resource allocation constraints, shapes evolutionary trajectories and maintains phenotypic diversity in selfing lineages.