Evolution of P-element Repression in Drosophila Melanogaster through the Piwi-Interacting RNA Pathway

Transposable elements (TEs) are ubiquitous and selfish genetic entities whose mobilization poses a significant threat to their host. In the germline of metazoan, the Piwi-interacting RNAs (piRNAs) derived from TE-enriched loci (called piRNA clusters) regulate TE activity in a sequence specific manner. However, the emergence and dynamics of piRNA-mediated repressor alleles to an invading TE remain elusive. P-element, a DNA transposon that recently invaded the D. melanogaster genome around 1950, provides a unique opportunity to study the evolution of host repression. In this dissertation, I first adapted a targeted sequencing strategy and developed a computational pipeline to annotate P-element insertions in a sequenced Drosophila melanogaster genome. My approach precisely determined P-element insertion breakpoints and found new P-element insertions, which were undetected by previously methods. Next, I modified the pipeline to annotate P-element insertions in the Drosophila melanogaster genetic reference panel (DGRP), a panel composed of 205 fully sequenced inbred lines. I found over 90% of DGRP genomes have P-elements in ancestral piRNA clusters that are active prior to the P-element invasion. This indicates de novo mutation, in which P-elements transpose into pre-existing piRNA clusters, is the predominant mechanism for the origin of repressor alleles. Moreover, I detected no fewer than 84 independent P-element insertions in ancestral piRNA clusters. Finally, I observed that P-element insertions in piRNA clusters segregate at significant higher frequency than P-elements outside of piRNA clusters, suggesting that cluster P-elements confer a selective advantage. Taken together, my results revealed a striking example of polygenic adaptation, in which a plethora of de novo beneficial P-element insertions into multiple piRNA clusters, fueled the evolution of a ubiquitous repressive phenotype in <60 years.