Reexamining the P-Element Invasion of Drosophila melanogaster Through the Lens of piRNA Silencing

Abstract

Transposable elements (TEs) are both important drivers of genome evolution and genetic parasites with potentially dramatic consequences for host fitness. The recent explosion of research on regulatory RNAs reveals that small RNA-mediated silencing is a conserved genetic mechanism through which hosts repress TE activity. The invasion of the Drosophila melanogaster genome by P elements, which happened on a historical timescale, represents an incomparable opportunity to understand how small RNAmediated silencing of TEs evolves. Repression of P-element transposition emerged almost concurrently with its invasion. Recent studies suggest that this repression is implemented in part, and perhaps predominantly, by the Piwi-interacting RNA (piRNA) pathway, a small RNA-mediated silencing pathway that regulates TE activity in many metazoan germlines. In this review, I consider the P-element invasion from both a molecular and evolutionary genetic perspective, reconciling classic studies of P-element regulation with the new mechanistic framework provided by the piRNA pathway. I further explore the utility of the P-element invasion as an exemplar of the evolution of piRNA-mediated silencing. In light of the highly-conserved role for piRNAs in regulating TEs, discoveries from this system have taxonomically broad implications for the evolution of repression.

The sources of adaptive variation

“…An initially very puzzling exception to Mendelian inheritance was provided by the phenomenon of hybrid dysgenesis, discovered in Drosophila melanogaster in the late 1970s, and which is now known to involve high rates of movement of certain types of TEs [42,43]. TEs can cause harmful effects on their hosts when they insert into coding or regulatory sequences.…”

“…Other effects include chromosome breakage when TEs insert or excise, and the production of chromosome rearrangements by recombination between homologous TEs in different genome locations. These harmful fitness effects of TEs often keep their frequencies at potential insertion sites low in natural populations, and generate selection on their hosts to suppress their movement [43,44]. Hybrid dysgenesis occurs when a male that carries members of certain TE families is crossed with a female that lacks them [42,43].…”

“…These harmful fitness effects of TEs often keep their frequencies at potential insertion sites low in natural populations, and generate selection on their hosts to suppress their movement [43,44]. Hybrid dysgenesis occurs when a male that carries members of certain TE families is crossed with a female that lacks them [42,43]. In the eggs of such mothers, the defence system in the cytoplasm fails to inactivate the TEs introduced from the father, which therefore transpose very actively in the offspring, causing sterility.…”

“…Susceptibility to hybrid dysgenesis can be transmitted through the maternal lineage over several generations. The system whose failure causes hybrid dysgenesis involves elaborate molecular mechanisms that have evolved to defend genomes against TEs in both plants and animals [43,45,46], involving small-interfering RNAs that rspb.royalsocietypublishing.org Proc. R. Soc.…”

“…Hybrid dysgenesis is simply a product of the temporary failure of this system; it is a transient, pathological phenomenon, and occurs in nature only when a new TE type is introduced into a population, as is currently happening with the P element in Drosophila simulans [43].…”