Relative contributions of pre-existing vs de novo genomic variation to adaptation are poorly understood, especially in polyploid organisms. We assess this in high resolution using autotetraploid Arabidopsis arenosa, which repeatedly adapted to toxic serpentine soils that exhibit skewed elemental profiles. Leveraging a fivefold replicated serpentine invasion, we assess selection on SNPs and structural variants (TEs) in 78 resequenced individuals and discover significant parallelism in candidate genes involved in ion homeostasis. We further model parallel selection and infer repeated sweeps on a shared pool of variants in nearly all these loci, supporting theoretical expectations. A single striking exception is represented by TWO PORE CHANNEL 1, which exhibits convergent evolution from independent de novo mutations at an identical, otherwise conserved site at the calcium channel selectivity gate. Taken together, this suggests that polyploid populations can rapidly adapt to environmental extremes, calling on both pre-existing variation and novel polymorphisms.

Biology Centre Czech Academy of Sciences České Budějovice Czech Republic

Department of Botany Faculty of Science Charles University Prague Czech Republic

Department of Systematic and Evolutionary Botany University of Zurich Zurich Switzerland

Department of Zoology Faculty of Science University of South Bohemia České Budějovice Czech Republic

Future Food Beacon and School of Biosciences University of Nottingham Nottingham UK

Future Food Beacon and School of Life Sciences University of Nottingham Nottingham UK

Institute of Plant Sciences University of Berne Bern Switzerland

John Innes Centre Norwich Research Park Norwich UK

The Czech Academy of Sciences Institute of Botany Průhonice Czech Republic

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Ploidy as a leaky reproductive barrier: mechanisms, rates and evolutionary significance of interploidy gene flow

Novelty and Convergence in Adaptation to Whole Genome Duplication