Evolution of germline immunity against transposons

The genomes of all living organisms contain transposable elements (TEs) that replicate selfishly for increasing their copy number, thereby with the potential to affect host fitness. Although TEs can reach more than 50% of the host genome, most of them are silenced by different defense mechanisms including small RNAs from so-called piRNA clusters that function as an unconventional adaptive immune system. Upon host-switching by horizontal transfer, TEs can invade the germline of distantly related naive species, even pandemically. The P transposon is the best-studied horizontal transfer model system for understanding recent TE invasion and world-wide spreading dynamics in Drosophila melanogaster populations, transferred horizontally from neotropical D. willistoni species. Although the multi-level regulatory mechanisms of the P element are well- known in D. melanogaster, we surprisingly lack information on their 1. distribution and evolutionary signatures within the ancestral willistoni host reservoir species, 2. genetic and epigenetic repression modes in the germline and 3. possible interactions between the different P element types we found within the willistoni group species. To answer these pivotal questions, our joint-team consisting of partners in Austria and France have recently collected neotropical flies in Central and Middle America (238 isofemale lines), and discovered that willistoni group species harbor ancestral canonical Ps, we named protocanonical P elements (pcP), which differ from the canonical Ps (cPs) of D. melanogaster and D. simulans in cis-regulatory motives and transposase. In pilot experiment, we identified ovarian small RNAs consistent in size with PIWI interacting RNAs (piRNAs) complementary to P sequences suggesting germline piRNA-based repression in willistoni species. Furthermore, neotropical willistoni host species can be classified into four evolutionary stages, i.e., EXTINCTION (only highly defective pcP copies corresponding to P200-MITEs in D. insularis), EROSION (only degenerative full size and deleted pcP copies in D. paulistorum and D. tropicalis), ACTIVITY (still active pcP copies in D. equinoxialis) and REPLACEMENT (complete loss of pcP copies in D. willistoni, except P200-MITEs, replaced by cP copies of unknown origin). This unique system will allow us to uncover the functional and evolutionary interplay and scenarios between TEs and their ancestral reservoirs and also in de novo hosts like D. melanogaster by combining population genetics, epigenetics, genomics with functional in vitro and in vivo assays. Answering these basic questions by an international team of L. TEYSSET, Paris, A. HUA-VAN, Paris-Saclay both France, Lisa KLASSON, Uppsala, Sweden and W.J. MILLER, Vienna in the model system Drosophila will help to better understand the mechanisms of homeostatic interactions between ancestral hosts and their potentially active mobile DNA.