Range-wide genetic structure of Arabidopsis halleri (Brassicaceae): glacial persistence in multiple refugia and origin of the Northern Hemisphere disjunction
Abstract
Wild relatives of Arabidopsis thaliana are moving into the spotlight of plant evolutionary biologists and molecular geneticists, but patterns of genetic diversity and phenotypic variation in natural populations are often overlooked. This gap in knowledge may in turn hamper generalizations of results from experimental studies using populations of unclear evolutionary background.
Here we present a comprehensive assessment of the genetic structure and morphological variation of Arabidopsis halleri, a model species for studying heavy metal tolerance and phytoremediation. Based on extensive sampling of 768 individuals from 82 populations across the entire distribution of the species, genotyping using multiple molecular markers (AFLP, nuclear microsatellites and sequences of single-copy nuclear regions and plastid DNA) and phenotyping by multivariate morphometrics, we aimed to reconstruct the range-wide phylogeography and morphological trait evolution in A. halleri populations.
In addition, we address general biogeographical questions related to the origin of the striking Northern Hemisphere disjunction (Europe-East Asia) and glacial survival in extra-Mediterranean refugia in Europe. East Asian (Japanese) populations were genetically distinct and slightly depauperate, but their divergence was at levels comparable to major splits within Europe, rejecting both an ancient (old vicariance) and recent (human-mediated spread) origin of the Northern Hemisphere disjunction.
In Europe we detected three major genetic lineages of A. halleri, corresponding well with geography (Western-Central Europe, the Alps and the south-eastern Carpathians + the Balkans). Sequence-based divergence estimates indicated a probable Pleistocene origin of these three lineages.
This, together with elevated diversity and rarity within each group, suggests in situ glacial persistence of A. halleri in multiple northern refugia of eastern Central Europe. The extensive morphological variation of European A. halleri populations only partly correlated with genetic structure.
Rather, it was driven by local environmental characteristics. This suggests a remarkably plastic response of the species to major environmental gradients, manifested by the parallel origin of a distinct alpine phenotype.