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

Abstract

Polyploidy, the result of whole genome duplication (WGD), is widespread across the tree of life and is often associated with speciation or adaptability. It is thought that adaptation in autopolyploids (within-species polyploids) may be facilitated by increased access to genetic variation. This variation may be sourced from gene flow with sister diploids and new access to other tetraploid lineages, as well as from increased mutational targets provided by doubled DNA content. Here we deconstruct the origins of haplotype blocks displaying the strongest selection signals in established, successful autopolyploids, Arabidopsis lyrata and Arabidopsis arenosa. We see strong signatures of selection in 17 genes implied in meiosis, cell cycle, and transcription across all four autotetraploid lineages present in our expanded sampling of 983 sequenced genomes. Most prominent in our results is the finding that the tetraploid-characteristic haplotype blocks with the most robust signals of selection were completely absent in diploid sisters. In contrast, the fine-scaled variant mosaics in the tetraploids originated from highly diverse evolutionary sources. These include novel reassortments of trans-specific polymorphism from diploids, new mutations, and tetraploid-specific inter-species hybridization. We speculate that this broad-scale allele acquisition and re-shuffling enabled the autotetraploids to rapidly adapt to the challenges inherent to WGD, and may further promote their adaptation to environmental challenges. Lay summaryPolyploidy, the result of whole genome duplication, is associated with speciation and adaptation. To fuel their often remarkable adaptations, polyploids may access and maintain adaptive alleles more readily than diploids. Here we identify repeated signals of selection on genes that are thought to mediate adaptation to whole genome duplication in two Arabidopsis species. We found that the tetraploid-characteristic haplotype blocks, found in genes exhibiting the most robust signals of selection, were never present in their diploid relatives. Instead, these blocks were made of mosaics forged from multiple allelic sources. We hypothesize that this increased variation helped polyploids to adapt to the process that caused this increase - genome duplication - and may also help them adapt to novel environments.