Purifying selection shapes the dynamics of P-element invasion in Drosophila simulans populations

Transposable elements (TEs) are DNA sequences that can move within a host genome. Many new TE insertions have deleterious effects on their host and are therefore removed by purifying selection. The genomic distribution of TEs thus reflects a balance between new insertions and purifying selection. However, the inference of purifying selection against deleterious TE insertions from the patterns observed in natural populations is challenged by the confounding effects of demographic events, such as population bottlenecks and migration.

We use experimental evolution to study the role of purifying selection during the invasion of the P-element, a highly invasive TE, in replicated Drosophila simulans populations under controlled laboratory conditions. Because the change in P-element copy number over time provides information about the transposition rate and the effect of purifying selection, we repeatedly sequence the experimental populations to study the P-element invasion dynamics. Based on the empirical data, we use Gaussian process surrogate models to efficiently explore the parameter space and identify parameter combinations that best reproduce the experimental P-element invasion trajectories. Assuming that beneficial P-element insertions are negligible, and that transposition regulation is well-approximated by our simulation framework, we estimate that, in our experimental populations, 73% (60.9-76.1%) of new P-element insertions are under purifying selection with a mean selection coefficient of - 0.056 (- 0.060 to - 0.042), highlighting the central role of selection in shaping P-element invasion dynamics.

This study underscores the power of experimental evolution as a tool for studying transposable element invasions and highlights the pivotal role of purifying selection in regulating P-element dynamics.