Parallel adaptation in autopolyploid Arabidopsis arenosa is dominated by repeated recruitment of shared alleles

Abstract

Relative contributions of pre-existing vs de novo genomic variation to adaptation are poorly understood, especially in polyploid organisms, which maintain increased variation. 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 discovered substantial parallelism in candidate genes involved in ion homeostasis. We further modelled parallel selection and inferred 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.