Genetic and environmental modulation of transposition shapes the evolutionary potential of Arabidopsis thaliana

International audienceBackground: How species can adapt to abrupt environmental changes, particularly in the absence of standing genetic variation, is poorly understood and a pressing question in the face of ongoing climate change. Here we leveraged multi-omics and bio-climatic data available for >1,000 wild A. thaliana accessions to determine the rate of transposable element (TE) mobilization in natural settings and its potential to create adaptive variation. Results: We show that TEs insert throughout the genome at almost the same rate as SNPs and we confirm this observation experimentally. Mobilization activity of individual TE families varies greatly between accessions, in association with genetic as well as environmental factors and we identified several gene-environment interactions. Although the distribution of TE insertions across the genome is ultimately shaped by purifying selection, reflecting their typically strong deleterious effects when located near or within genes, numerous recent TE-containing alleles show signatures of positive selection. Moreover, high transposition appears to be positively selected at the edge of the species’ ecological niche. Based on these results and mathematical modeling, we predict higher transposition activity in Mediterranean regions within the next decades in response to global warming and thus an acceleration in the creation of large effect alleles. Conclusions: Our study reveals that TE mobilization is a major generator of genetic variation in A. thaliana that is finely modulated by genetic and environmental factors. These findings and modeling indicate that TEs may be essential genomic players in the demise or rescue of native populations in times of climate crises