Genomic basis and phenotypic manifestation of (non-)parallel serpentine adaptation in Arabidopsis arenosa

ABSTRACT Parallel evolution is common in nature and provides one of the most compelling examples of rapid environmental adaptation. In contrast to the recent burst of studies addressing genomic basis of parallel evolution, integrative studies linking genomic and phenotypic parallelism are scarce. Edaphic islands of toxic serpentine soils provide ideal systems for studying rapid parallel adaptation in plants. Serpentines are well-defined by a set of chemical selective factors and recent divergence between serpentine and geographically proximal non-serpentine populations allow mitigating confounding effects of drift. We leveraged threefold independent serpentine adaptation of Arabidopsis arenosa and used reciprocal transplant, ionomics, and available genome-wide polymorphisms to test if parallelism is manifested to a similar extent at both genomic and phenotypic levels. We found the varying magnitude of fitness differences, that was congruent with neutral genetic differentiation between populations, and limited costs of serpentine adaptation. Further, phenotypic parallelism in functional traits was pervasive. The genomic parallelism at the gene level was significant, although relatively minor. Therefore, the similarly modified phenotypes e.g. of ion uptake arose possibly by selection on different loci in similar functional pathways. In summary, we bring evidence for the important role of genetic redundancy in rapid adaptation involving traits with polygenic architecture.