Arms races between selfish genetic elements and their host defence

Arms races between parasites and hosts are key drivers of evolution. Selfishly replicating transposable elements (TEs) are thought to follow similar dynamics, but strong evidence is missing. We tested this in termites, social insects in which TEs have been linked to ageing. Sequencing genomes and profiling DNA methylation across the termite phylogeny revealed corresponding phylogenetic signals in TEs and TE methylation, indicative of selection. TE methylation reduces TE success, as both TE abundance and spreading efficiency decrease with increasing methylation. TEs also become less harmful with TE age: evolutionarily older TEs spread less, insert less into exons, and erode into short remnants. Correspondingly, defence through methylation is strongest against young TEs. Yet, as in typical host-parasite arms races, some TEs persist, implying resistance or recurrent invasions. Our results reveal arms races between TEs and DNA methylation, positioning TEs as drivers of genome evolution similar to symbionts in organismic evolution.