The impact of insertion bias into piRNA clusters on the invasion of transposable elements

Abstract

In our current understanding of transposable element (TE) invasions TEs move freely until they accidentally insert into a piRNA cluster. They are then silenced by the production of piRNA cognate to the TE. Under this model, one would expect that TEs might evolve to avoid piRNA clusters. Yet empirical observations show that some TEs, such as the P -element, insert into piRNA clusters preferentially. We were thus wondering if such a bias could be beneficial for the TE, for example by minimizing harm to the host while still being able to selfishly spread in populations. We decided to model insertion bias to determine if there was ever a situation in which insertion bias was beneficial to the TE. We performed extensive forward simulations of TE invasions with differing insertion biases into piRNA clusters. We found that insertion bias significantly altered the invasion dynamics of TEs, primarily by changing the copy number of the TE in individuals prior to silencing. Insertion into a piRNA cluster reduced the deleterious effects of TEs to the host population, but we found that TEs avoiding piRNA clusters out-compete TEs with a bias towards cluster insertions. Insertion bias was only beneficial to the TE when there was negative selection against TEs and a lack of recombination. Different TEs show different insertion biases into piRNA clusters suggesting they are an attribute of the TE not the host, yet scenarios in which this is beneficial to the TE are quite limited. This opens up an interesting area of future research into the dynamics of insertion bias during TE invasions. Significance StatementThis study challenges the pre-existing understanding of the TE dynamics by investigating the potential adaptive role of insertion bias into piRNA clusters. Using extensive forward simulations, we demonstrate that while insertion bias significantly alters TE invasion dynamics, it is generally not beneficial for the TEs spread in populations. Our results also show that transposable elements (TEs) that avoid piRNA clusters tend to do better than those that are more likely to preferencially insert into these clusters. This work provides novel insights into the complex dynamics between TEs and host genomes, showing the limited scenarios where the insertion bias could be advantageous to TEs. These results open new area for research into TE invasion dynamics and the evolution of host-TE interactions, further contributing to our understanding of genome evolution and stability.