piRNA clusters predict invasion dynamics

Life is a struggle for survival where, for example, parasites prey on their hosts and hosts combat their parasites. Surprising to many, this battle also rages in our genomes. Parasitic DNA spreads in our genomes, even if this is harming our health. These p arasitic sequences, also called transposable elements (TEs), have been remarkably successful, constituting more than 50% of our human genomes. Interestingly, the abundance of TEs varies dramatically among species. For example the frog genome consists to 77 % of TEs while yeast solely has 3%. Why is the frog ending up with so many more TEs than yeast? In this project we aim to find some answers to this important open question. Our computer simulations previously identified a factor that could be central to this question. The size of piRNA clusters - genomic regions producing small RNAs that silence TEs - might be the most important factor governing the abundance of TEs in species. If we imagine TEs as mice that happily multiply within a house (=the genome), then the piRNA clusters can be imagined as mousetraps. If a house has few mousetraps, then the number of mice in the house will be high, whereas the mice population will be kept small if many mousetraps have been distributed over the house. Similarly genomes with small piRNA clusters may accumulate a lot of TEs, whereas genomes with large clusters may solely end up with few TEs. In this project we will test this hypothesis by studying the size of piRNA clusters and the abundance of TEs in many different Drosophila species. Furthermore we will artificially introduce a TE into different Drosophila species and test if the size of the piRNA cluster accurately predicts the abundance of this novel TE. Finally we aim to develop computer models that are able to describe the spread of TEs. In particular we will test if the size of piRNA clusters and other factors, such as negative selection against TEs, are sufficient to quantitatively predict the curse of TE invasions.

The project was highly successful; we published multiple papers, several in leading journals such as Nature Communications, Genome Research and PNAS. The most important finding about the extent of horizontal transfer may even have a lasting impact on our understanding of evolution. Typically genetic information is strictly vertically transmitted from parent to offspring. Occasionally however genetic material is also horizontally transmitted, for example between two unrelated species. Such a horizontal transfer was thought to be rare, occurring in the order of once every million years.Our work showed that at least 12 such horizontal transfers happened in the last 200 years in the fruit fly, Drosophila melanogaster. This finding raises a lot of questions. First, what are the consequences of so many horizontal transfers for the organism? Second, do other organisms also have such a high rate of horizontal transfer? Finally, is this rate of horizontal transfer constant or has it increased recently? For several reasons we think that it increased recently, most likely due to human activity contributing to climate change and habitat expansions of insects, factors that are likely important for horizontal transfer. This work thus raises the concern that humans might trigger widespread genome invasions in many species. This could have unpredictable consequences to the evolutionary trajectories of the species, ranging from extinctions to accelerated adaption. We plan to test this hypothesis in follow up projects.