Repeated adaptation to whole genome duplication in outcrossing Arabidopsis is mediated by mosaic adaptive haplotypes

Polyploidy, the doubling of an entire genome, is common in many organisms, including plants, yeast, and fish. While it can often be fatal due to the sudden transformation of DNA management and cell physiology, some lineages are able to adapt to this challenge. One proposed mechanism for this adaptation is the increased access to allelic variation in polyploids, reflecting both enhanced gene flow and higher rates of mutation accumulation. Here, we investigated whether this increased allelic diversity is utilized by polyploids to form mosaic adaptive haplotypes made up of diverse allelic sources. To do so, we studied two sister diploid/autotetraploid species (within-species polyploids, Arabidopsis lyrata and Arabidopsis arenosa). We first demonstrated the existence of two novel, independent autotetraploid lineages in these species, bringing the total number known to four. These lineages exhibited consistent changes in probable adaptive traits, as well as strong signatures of selection on the same set of 17 candidate genes involved in cell cycle, meiosis, and transcription. Interestingly, candidate adaptive haplotypes of these genes were completely absent in their natural diploid progenitors. Instead, our analysis of 995 individuals (2970 haploid genomes in 504 diploids and 491 autotetraploids) found that these alleles were made up of fine-scaled mosaics of variants from diverse evolutionary sources, including primarily reassortments of trans-specific polymorphism from diploids, novel mutations, and inter-species hybridization. We speculate that such flexibility in acquisition and re-shuffling of adaptive alleles enabled tetraploids to rapidly adapt to polyploidization, and may further promote their rapid adaptation to environmental challenges. ### Competing Interest Statement The authors have declared no competing interest.