Rapid evolutionary adaptation to heavy metal-polluted soils in plant species of the genus Arabidopsis

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The colonization of soils anthropogenically polluted with toxic levels of heavy metals is a promising model for processes of rapid evolutionary adaptation in plants. A large number of parallel incidences of the establishment of populations on soils enriched in the calamine group of metals – zinc (Zn), cadmium (Cd) and lead (Pb) – have occurred only in Arabidopsis halleri among the species in the sister clade of A. thaliana. Interestingly, a small subset of such metalliferous sites host not only A. halleri but also the closely related species A. arenosa. At these sites, the intermediate metal-related physiology in both species as well as the occurrence of a few plants of intermediate morphology suggest the possibility of recurrent inter-species hybridization. Here we aim to address the role of gene flow between A. halleri and A. arenosa in the adaptation of both species to calamine metalliferous soils, as compared to the role of selection within each species individually. The adaptation of A. halleri to metalliferous soils merely required the evolution of enhanced metal hypertolerance. A. halleri already exhibits species-wide hypertolerance to calamine metals as a result of the hyperaccumulation of Zn and Cd to extraordinarily high concentrations of >3,000 and >100 µg g-1 dry leaf biomass, respectively, even on non-contaminated soils. Enhanced metal hypertolerance in A. halleri on metalliferous soils has been shown to involve an attenuation of metal hyperaccumulation. By contrast, A. arenosa is generally a metal excluder species, like almost all other plants. We focus here on geographically clustered site groups of calamine heavy metal-contaminated and non-contaminated sites where both A. halleri and A. arenosa naturally grow together in the field today. These are analysed in a comparative approach in relation to non-metalliferous reference sites hosting only one of the two species. We assess between-species introgression genome-wide and localize genomic regions representing haplotypes introgressed from the other species. In parallel, we apply genome scan approaches to identify genomic regions that have been subject to selection in either of the two species, in continuation of the first phase where we applied this approach to the rare incidences of copper hypertolerance in A. halleri. To test for molecular phenotypic consequences of adaptation, we compare gene expression among a chosen set of populations of both species. In morphologically intermediate plant individuals collected at these sites, we characterize leaf and soil composition in the field to obtain initial phenotypic information. We determine ploidy levels by comparison to the two hypothesized parental species, and we analyse plants at the sequence level with respect to the genomic components originating from A. halleri and A. arenosa.