Population genetics of piRNAs in Drosophila

Transposable elements (TEs) selfish genetic elements that survive by replicating within host genomesare one of the most important kinds of parasitic elements. Most genomes are riddled with substantial numbers of TEs, e.g, the human genome is comprised of 44% TE-derived DNA, compared to only 1-2% protein coding DNA. Such a substantial evolutionary burden is likely to provoke a strong evolutionary response; in fact, parasites in general have been consistently shown to be among the primary driving forces underlying rapid adaptation. However, the evolutionary response to TEs is comparatively poorly understood. The reason is that the TE defense system has a important small RNA component, the piRNAs, and the evolution of such small RNA systems is relatively poorly studied. Here, we aim to study the evolution of piRNA loci, asking if these loci show the same sort of rapid evolutionary response as other immunity loci. Specifically, we will investigate the population genetics of piRNA loci, looking for rapid population differentiation in response to active TEs. To this end, we plan to survey Drosophila populations for the presence of protective piRNA loci. At the same time, we plan to survey these same populations for the transposable element content, to obtain a picture of both sides of the co-evolutionary equation.

Some genes are essential for organisms to function, but others act as parasites-using their hosts to promote their own proliferation. These 'selfish genes' take many forms, including chromosomes that are parasitic, chromosomes that kill competing chromosomes, and bacteria that manipulate their host's reproduction. Each of these is a fascinating instance of the universality of genetic conflict, but they typically evolve sporadically, appearing in relatively few species or taxonomic groups. In contrast, the simplest form of selfish gene is also the most successful. Nearly every eukaryote examined to date contains 'jumping genes'-- parasitic pieces of DNA that spread through genomes by 'jumping', or copying themselves, within the genome. This parasitic DNA can spread quite successfully through genomes-roughly half the DNA in the human genome, for example, is derived from these selfish genes. One key feature of these jumping genes is that, in addition to jumping within a genome, they can also jump across species boundaries. These invasions of new species appear to be common-sequence data shows that many species share their parasitic genes. However, they are rarely observed. In this work, we happened to catch the spread of a transposable element in fruit flies, nearly as it happened. The 'P-element', a selfish gene that infects Drosophila (fruit fly) species, invaded D. simulans population around the world. The spread of the P-element was remarkably fast-undetectable in 2000, it was found nearly everywhere by 2014. Through this study, we show that selfish genes can have a strong and unexpectedly rapid impact on genomes, setting the stage for further genetic studies of these important selfish genes.