Ecological and genetic trade-offs drive Arabidopsis thaliana range expansion in Europe

Abstract

How trade-offs between traits constrain adaptation to contrasted environments is critical to understand the distribution range of a given species. In Arabidopsis thaliana, genetic analyses recently revealed that a group of genotypes successfully recolonized Europe from its center after the last glaciation, outcompeting older lineages and leaving them only at the distribution margins, where environmental conditions are more stressing. However, whether trade-offs between traits related to dispersal, competition, and stress tolerance explain the success and persistence of different lineages across the species geographic range remains an open question. Here, we compared the genetic and phenotypic differentiation between 72 ecotypes originating from three geographical groups in Europe (North, South and Center). We measured key traits related to fecundity, dispersal ability, competition tolerance, and stress tolerance, and used genomic data to infer the effect of selection on these traits. We showed that a trade-off between plant fecundity and seed mass constrains the diversification of A. thaliana in Europe. In particular, the success of the cosmopolitan genotypes that recolonized Europe can be explained by their higher dispersal ability at the expense of their competitive ability and stress tolerance. Inversely, peripheral ecotypes exhibited the opposite trait syndrome: high competition and stress tolerance but low dispersal ability. Moreover, peripheral genotypes tend to differentiate from central ones at genes involved in dispersal and competitive traits such as seed mass. Combining ecological and genomic approaches, our study demonstrated the role of key ecological trade-offs as evolutionary drivers of the distribution of plant populations along a geographic gradient. SignificanceAcross geographic gradients, differential adaptive phenotypes among populations can reduce the risk of local extinctions and favor niche dynamics. However, a phenotypic advantage often comes at a cost. For instance, the competition-colonization trade-off is proposed as an important driver of plant interspecific diversity, but its role for local adaptation at the intraspecific level is still unclear. Using the broadly-distributed species Arabidopsis thaliana, we evaluate how ecological trade-offs have shaped the demography and evolution of central and peripheral populations in its native geographic gradient. Our study demonstrates that the competition-colonization trade-off is responsible of the spatially-structured phenotypic variation of A. thaliana across its geographical range. Our study highlights seed mass as a key trait for plant adaptation across environmental conditions.