The composition of piRNA clusters in Drosophila melanogaster deviates from expectations under the trap model

Abstract

It is widely assumed that the invasion of a transposable element (TE) in mammals and invertebrates is stopped when a copy of the TE jumps into a piRNA cluster (i.e. the trap model). However, recent works, which for example showed that deletion of three major piRNA clusters has no effect on TE activity, cast doubt on the trap model. Therefore, we aim to test the trap model. We show with population genetic simulations that the composition of regions that act as transposon traps (i.e. possible piRNA clusters) ought to deviate from regions that have no effect on TE activity. Next, we investigated TEs in five D. melanogaster strains using three complementary approaches to test whether the composition of piRNA clusters matches these expectations. We found that the abundance of TE families inside and outside of piRNA clusters is highly correlated, although this is not expected under the trap model. Furthermore, we found that the distribution of the number of TE insertions in piRNA clusters is also much broader than expected, where some families have zero cluster insertions and others more than 14. One feasible explanation is that insertions in piRNA clusters have little effect on TE activity and that the trap model is therefore incorrect. Alternatively, dispersed piRNA producing TE insertions and temporal as well as spatial heterogeneity of piRNA clusters may explain some of our observations.