The evolutionary history of the Arabidopsis lyrata complex: a hybrid in the amphi-Beringian area closes a large distribution gap and builds up a genetic barrier

Abstract

Abstract Background The genomes of higher plants are, on the majority, polyploid, and hybridisation is more frequent in plants than in animals. Both polyploidisation and hybridisation contribute to increased variability within species, and may transfer adaptations between species in a changing environment. Studying these aspects of evolution within a diversified species complex could help to clarify overall spatial and temporal patterns of plant speciation. The Arabidopsis lyrata complex, which is closely related to the model plant Arabidopsis thaliana, is a perennial, outcrossing, herbaceous species complex with a circumpolar distribution in the Northern Hemisphere as well as a disjunct Central European distribution in relictual habitats. This species complex comprises three species and four subspecies, mainly diploids but also several tetraploids, including one natural hybrid. The complex is ecologically, but not fully geographically, separated from members of the closely related species complex of Arabidopsis halleri, and the evolutionary histories of both species compexes have largely been influenced by Pleistocene climate oscillations. Results Using DNA sequence data from the nuclear encoded cytosolic phosphoglucoisomerase and Internal Transcribed Spacers 1 and 2 of the ribosomal DNA, as well as the trnL/F region from the chloroplast genome, we unravelled the phylogeography of the various taxonomic units of the A. lyrata complex. We demonstrate the existence of two major gene pools in Central Europe and Northern America. These two major gene pools are constructed from different taxonomic units. We also confirmed that A. kamchatica is the allotetraploid hybrid between A. lyrata and A. halleri, occupying the amphi-Beringian area in Eastern Asia and Northern America. This species closes the large distribution gap of the various other A. lyrata segregates. Furthermore, we revealed a threefold independent allopolyploid origin of this hybrid species in Japan, China, and Kamchatka. Conclusions Unglaciated parts of the Eastern Austrian Alps and arctic Eurasia, including Beringia, served as major glacial refugia of the Eurasian A. lyrata lineage, whereas A. halleri and its various subspecies probably survived in refuges in Central Europe and Eastern Asia with a large distribution gap in between. The North American A. lyrata lineage probably survived the glaciation in the southeast of North America. The dramatic climatic changes during glaciation and deglaciation cycles promoted not only secondary contact and formation of the allopolyploid hybrid A. kamchatica, but also provided the environment that allowed this species to fill a large geographic gap separating the two genetically different A. lyrata lineages from Eurasia and North America. With our example focusing on the evolutionary history of the A. lyrata species complex, we add substantial information to a broad evolutionary framework for future investigations within this emerging model system in molecular and evolutionary biology.