Quantifying the impact of heritable epigenetic variation on complex traits is an emerging challenge in population genetics. Here, we analyze a population of isogenic Arabidopsis lines that segregate experimentally induced DNA methylation changes at hundreds of regions across the genome. We demonstrate that several of these differentially methylated regions (DMRs) act as bona fide epigenetic quantitative trait loci (QTL(epi)), accounting for 60 to 90% of the heritability for two complex traits, flowering time and primary root length. These QTL(epi) are reproducible and can be subjected to artificial selection. Many of the experimentally induced DMRs are also variable in natural populations of this species and may thus provide an epigenetic basis for Darwinian evolution independently of DNA sequence changes.

Transposable elements (TEs) contribute to genome size, organization and evolution. In plants, their activity is primarily controlled by transcriptional gene silencing (TGS), usually investigated at steady states, reflecting how long-established silent conditions are maintained, faithfully reiterated or temporarily modified. How active, invasive TEs are detected and silenced de novo in plants remains largely unknown. Using inbred lineages of hybrid Arabidopsis thaliana epigenomes combining wild-type and mutant chromosomes, we have deciphered the sequence of physiological and molecular events underlying the de novo invasion, proliferation and eventual demise of the single-copy endogenous retrotransposon Evadé (EVD). We show how this reconstructed TE burst causes widespread genome diversification and de novo epiallelism that could serve as sources for selectable and potentially adaptive traits.