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Abstract Horizontal transfer of genetic material in eukaryotes has rarely been documented over short evolutionary timescales. Here, we show that two retrotransposons,ShellderandSpoink, invaded the genomes of multiple species of themelanogastersubgroup within the last 50 years. Through horizontal transfer,Spoinkspread inD. melanogasterduring the 1980s, while bothShellderandSpoinkinvadedD. simulansin the 1990s. Possibly following hybridization,D. simulansinfected the island endemic speciesD. mauritiana(Mauritius) andD. sechellia(Seychelles) with both TEs after 1995. In the same approximate time-frame,Shellderalso invadedD. teissieri, a species confined to sub-Saharan Africa. We find that the donors ofShellderandSpoinkare likely AmericanDrosophilaspecies from thewillistoni,cardini, andrepletagroups. Thus, the described cascade of TE invasions could only become feasible afterD. melanogasterandD. simulansextended their distributions into the Americas 200 years ago, likely aided by human activity. Our work reveals that cascades of TE invasions, likely initiated by human-mediated range expansions, could have an impact on the genomic and phenotypic evolution of geographically dispersed species. Within a few decades, TEs could invade many species, including island endemics, with distributions very distant from the donor of the TE. 

During the last few centuriesD. melanogasterpopulations were invaded by several transposable elements, the most recent of which was thought to be theP-element between 1950 and 1980. Here we describe a novel TE, which we namedSpoink, that has invadedD. melanogaster. It is a 5216nt LTR retrotransposon of the Ty3/gypsy superfamily. Relying on strains sampled at different times during the last century we show thatSpoinkinvaded worldwideD. melanogasterpopulations after theP-element between 1983 and 1993. This invasion was likely triggered by a horizontal transfer from theD. willistonigroup, much as theP-element.Spoinkis probably silenced by the piRNA pathway in natural populations and about 1/3 of the examined strains have an insertion into a canonical piRNA cluster such as42AB. Given the degree of genetic investigation ofD. melanogasterit is perhaps surprising thatSpoinkwas able to invade unnoticed. 

Suppression of transposable elements (TEs) is paramount to maintain genomic integrity and organismal fitness. InD.melanogaster, theflamencolocus is a master suppressor of TEs, preventing the mobilization of certain endogenous retrovirus-like TEs from somatic ovarian support cells to the germline. It is transcribed by Pol II as a long (100s of kb), single-stranded, primary transcript, and metabolized into ~24–32 nt Piwi-interacting RNAs (piRNAs) that target active TEs via antisense complementarity.flamencois thought to operate as a trap, owing to its high content of recent horizontally transferred TEs that are enriched in antisense orientation. Using newly-generated long read genome data, which is critical for accurate assembly of repetitive sequences, we find thatflamencohas undergone radical transformations in sequence content and even copy number acrosssimulansclade Drosophilid species.Drosophila simulans flamencohas duplicated and diverged, and neither copy exhibits synteny withD.melanogasterbeyond the core promoter. Moreover,flamencoorganization is highly variable acrossD.simulansindividuals. Next, we find thatD.simulansandD.mauritiana flamencodisplay signatures of a dual-stranded cluster, with ping-pong signals in the testis and/or embryo. This is accompanied by increased copy numbers of germline TEs, consistent with these regions operating as functional dual-stranded clusters. Overall, the physical and functional diversity offlamencoorthologs is testament to the extremely dynamic consequences of TE arms races on genome organization, not only amongst highly related species, but even amongst individuals. 

Abstract Small RNAs produced from transposable element (TE)‐rich sections of the genome, termed piRNA clusters, are a crucial component in the genomic defence against selfish DNA. In animals, it is thought the invasion of a TE is stopped when a copy of the TE inserts into a piRNA cluster, triggering the production of cognate small RNAs that silence the TE. Despite this importance for TE control, little is known about the evolutionary dynamics of piRNA clusters, mostly because these repeat‐rich regions are difficult to assemble and compare. Here, we establish a framework for studying the evolution of piRNA clusters quantitatively. Previously introduced quality metrics and a newly developed software for multiple alignments of repeat annotations (Manna) allow us to estimate the level of polymorphism segregating in piRNA clusters and the divergence among homologous piRNA clusters. By studying 20 conserved piRNA clusters in multiple assemblies of fourDrosophilaspecies, we show that piRNA clusters are evolving rapidly. While 70%–80% of the clusters are conserved within species, the clusters share almost no similarity between species as closely related asD. melanogasterandD. simulans. Furthermore, abundant insertions and deletions are segregating within theDrosophilaspecies. We show that the evolution of clusters is mainly driven by large insertions of recently active TEs and smaller deletions mostly in older TEs. The effect of these forces is so rapid that homologous clusters often do not contain insertions from the same TE families.