P-element invasions in Drosophila erecta shed light on the establishment of host control over a transposable element

To prevent the spread of transposable elements (TEs) hosts have developed sophisticated defence mechanisms. In mammals and invertebrates this defence mechanism operates through piRNAs. It is unclear how piRNA-based defences are established against invading TEs. According to the trap model, a TE insertion into a piRNA cluster, i.e. a distinct genomic locus, activates the host defence. Alternatively, siRNAs, generated by cleavage of dsRNA, may be the trigger for host control. To investigate this we introduced the P-element, one of the most widely studied eukaryotic transposons, into naive lines of Drosophila erecta. We monitored the invasion in 3 replicates for more than 50 generations by sequencing the genomic DNA (using short and long-reads), the small RNAs and the transcriptome at regular intervals. A piRNA based host defence was rapidly established in 2 replicates but not in the third, where P-element copy numbers kept increasing for over 50 generations. We found that siRNAs emerged prior to piRNAs, supporting the view that siRNAs initiate host defence. However, neither insertions in piRNA clusters nor the formation of siRNAs were sufficient to stop the P-element. Instead the activation of the ping-pong cycle was shown to be crucial. We introduce a novel model, the crank-up model, which emphasizes activation of the ping-pong cycle as a critical event in establishing host control over a TE.