Non-random polymorphisms near transposable elements facilitate evolution across the genome of Arabidopsis thaliana

Evolution is a key characteristic of all life on earth, and is achieved mainly through mutation and recombination. To facilitate evolutionary rates in the absence of recombination, increased mutagenesis could provide essential opportunities for evolution. Here, we harness the genomes of 973 wild accessions of Arabidopsis thaliana, a self-fertilizing species characterized by reduced recombination rates, to study the role of transposable elements (TEs) as mutagenic drivers of non-random genetic variation. We found that multiple TE superfamilies accumulate large numbers of genetic variants in gene-rich regions of the genome. Moreover, TEs were enriched in genes underpinning key molecular processes, including fertilization and mRNA cis-splicing, suggesting that TEs generate genetic variation that is fundamental to organismal functioning and reproduction. An excess of common genetic variants (maf>0.4) flanking TEs, despite the extreme degree of self-fertilization, further corroborates the notion that TEs can generate substantial evolutionary potential in the absence of outcrossing. Nevertheless, while other studies point to TE mobilization as a strategy to facilitate adaptive evolution, we find that only a fraction (4.8%) of TE families was linked to genetic variants involved in climate adaptation to a significantly larger extent than background genomic variation, possibly because the high mutation rates near TEs dilute adaptive signals. Overall, all TE superfamilies but one (Gypsy) were significantly associated with evolutionary processes through their association with genes, functional molecular processes, flanking common variants and/or climate adaptation. We conclude that non-random mutations flanking TEs provide substantial evolutionary potential in a self-fertilizing species.