The recent invasion of natural Drosophila simulans populations by the P-element

Abstract

The P-element is one of the best understood eukaryotic transposable elements. It invaded Drosophila melanogaster populations within a few decades but was thought to be absent from close relatives, including Drosophila simulans. Five decades after the spread in D. melanogaster, we provide evidence that the P-element has also invaded D. simulans. P-elements in D. simulans appear to have been acquired recently from D. melanogaster probably via a single horizontal transfer event. Expression data indicate that the P-element is processed in the germ line of D. simulans, and genomic data show an enrichment of P-element insertions in putative origins of replication, similar to that seen in D. melanogaster. This ongoing spread of the P-element in natural populations provides a unique opportunity to understand the dynamics of transposable element spread and the associated piwi-interacting RNAs defense mechanisms.T he P-element, one of the best understood eukaryotic transposable elements (TEs), was originally discovered as the causal factor for a syndrome of abnormal phenotypes in Drosophila melanogaster. Crosses in which males derived from newly collected strains were mated with females from long established laboratory stocks produced offspring with spontaneous male recombination, high rates of sterility, and malformed gonadsthat is, "hybrid dysgenesis" (1-4). Eventually it was discovered that hybrid dysgenesis was due to the presence of a TE, the P-element (5, 6), which rapidly became the workhorse of Drosophila transgenesis (5, 7-9). Surveys of strains collected over 70 y show that the P-element spread rapidly in natural D. melanogaster populations, between 1950 and 1990 (10-12), and surveys of other Drosophila species revealed that the P-element had been horizontally transferred (HT) from a distantly related species, Drosophila willistoni (13). As there could be a considerable lag time between the initial transmission of a TE and its invasion of worldwide populations, it is unclear exactly when the P-element first entered D. melanogaster. However, the initial HT event likely occurred somewhere between the spread of D. melanogaster populations into the habitat of D. willistoni, around 1800 (14), and the onset of the worldwide invasion of D. melanogaster populations, around 1950 (10). In any case, the P-element had not been found in close relatives of D. melanogaster, including Drosophila simulans (13-18). The failure of the P-element to invade D. simulans is surprising, as both species are cosmopolitan, are mostly sympatric, and share insertions from many TE families via horizontal transfer (19,20). Furthermore, when artificially injected, the P-element can transpose in D. simulans, albeit at a reduced rate (21, 22). Results and DiscussionThe Recent Invasion of D. simulans Populations. Here, we show that the P-element has recently invaded natural D. simulans populations. We sequenced D. simulans collected from South Africa (in 2012) and from Florida (in 2010) as pools (Pool-seq) (23) and analyzed TE insertions in these ...

Paternal Induction of Hybrid Dysgenesis in Drosophila melanogaster Is Weakly Correlated with Both P-Element and hobo Element Dosage

“…Depending on the estimator, our observations are consistent with—or modestly lower than—previous estimates of P -element abundance in wild-derived genomes based on in situ hybridization [∼30 copies (Ronsseray et al 1989)], and pooled deep sequencing [∼60 copies (Kofler et al 2015)].…”

Suitability of Different Mapping Algorithms for Genome-Wide Polymorphism Scans with Pool-Seq Data

“…For example, Pool-Seq was used to unravel the genetic basis of complex traits (Bastide et al 2013; Cheeseman et al 2015), identify loci contributing to local adaptation (Lamichhaney et al 2012; Turner et al 2010), trace beneficial loci during experimental evolution (Lang et al 2013; Orozco-terWengel et al 2012; Tobler et al 2014), identify positively selected loci in populations (Bergland et al 2014; Kofler et al 2012; Nolte et al 2012), find genes selected during domestication (Axelsson et al 2013; Rubin et al 2010), study the invasion of transposable elements (Kofler et al 2015a), investigate clonal evolution in cancer (Ding et al 2012), and to identify causative mutations in forward genetic screens (Schneeberger et al 2009). With this rapid gain in popularity, it is important to ensure the reliable analysis of Pool-Seq data.…”

Reexamining the P-Element Invasion of Drosophila melanogaster Through the Lens of piRNA Silencing

“…The relative genomic abundance of particular variants can be determined simply by aligning short reads to a consensus sequence for the TE family (Kofler et al 2015a), an approach that could easily be used to compare KP abundance among different wild-derived genotypes. Furthermore, recent technological advancements promise to greatly enhance our ability to examine structural variation at the level of individual TE insertions (Voskoboynik et al 2013;Kim et al 2014;McCoy et al 2014;Berlin et al 2015;Hall et al 2016), which has historically been prevented by the impossibility of assigning most TE-derived sequencing reads to a particular genomic location.…”

“…Additionally, many P cytotypes must be established by insertions into other piRNA clusters, because a worldwide sampling of P strains revealed that only 50% harbor a P-element insertion in cytological position 1A (Ronsseray et al 1989b). Similarly, the KP structural variant is extremely prevalent in wild-derived genomes (Itoh and Boussy 2002;Itoh et al 2007;Ogura et al 2007;Kofler et al 2015a), however, no single euchromatic P-element insertion (KP or otherwise) is observed to segregate at high frequency (Zhuang et al 2014;Kofler et al 2015b). A plethora of repressor alleles have therefore arisen in D. melanogaster populations since the invasion of the P element.…”

“…In particular, the historical timescale of the P-element invasion presents a powerful opportunity to dissect the evolution of repression, with a newly-discovered invasion into D. simulans allowing for parallel comparisons in an independent genetic lineage (Kofler et al 2015a;Hill et al 2016). The recent discovery of the piRNA pathway now paves the way for a deeper understanding of how host genomes respond to invasion by novel TEs by revealing the molecular and genetic framework within which repression evolves.…”