Historical adaptation to transposable element invasions in Drosophila is primarily due to insertions in existing piRNA clusters

Abstract

Transposable elements (TEs) are genomic parasites that shift between host species, which may allow them to escape sequence-specific host silencing mechanisms. One such silencing mechanism, the piRNA pathway, is the main line of defense in the germline of animals, and acts through small RNAs targeting specific TE sequences. Though many mechanistic details of this pathway are known, how it evolves to respond to a new transposable element invasion is not. Here, we examine the piRNA-based response to three recently invading TEs in Drosophila simulans, the P-element, Shellder and Spoink. To this end, we assembled genomes of 22 strains, annotated piRNA-producing loci (piRNA clusters) in each strain, and located insertions of the new TEs within these loci. We find that piRNA clusters are highly polymorphic among strains and piRNAs targeting the new TEs come mostly from clusters that likely pre-date the invasions, though there is also some evidence of piRNAs generated de novo, particularly for the long-terminal repeat (LTR) elements. Moreover, resistance to each TE appears to have evolved mostly independently in the different strains through distinct insertions, often in different clusters, although some loci, such as flamenco for Shellder, are recurrent targets.