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Abstract BackgroundIn our current understanding of transposable element (TE) invasions, TEs move freely until they accidentally insert into a piRNA cluster, where they are silenced by the production of piRNA cognate to the TE. Under this model, one would expect that selection might favor TEs that avoid piRNA clusters. However, empirical observations show that some TEs, such as theP-element, insert into piRNA clusters preferentially. We were thus wondering if such a bias, by minimizing harm to the host, could facilitate the spread of TEs throughout a population. ResultsWe performed extensive forward simulations of TE invasions with different insertion biases into piRNA clusters to determine if there was ever a situation in which the insertion bias was beneficial to the TE. We found that insertion bias significantly altered the invasion dynamics of TEs, primarily by changing the number of TE copies in individuals before silencing. Insertion into a piRNA cluster reduced the deleterious effects of TEs to the host population, but we found that TEs avoiding piRNA clusters out-compete TEs with a bias toward cluster insertions. Insertion bias was only beneficial to the TE when there was negative selection against TEs and a lack of recombination. ConclusionsDifferent TEs show different insertion biases into piRNA clusters suggesting they are an attribute of the TE not the host, yet scenarios in which this is beneficial for TE propagation are quite limited. This opens up an interesting area for future research into the dynamics of insertion bias during TE invasions. 

Abstract Transposable elements are genetic elements also known as “jumping genes” that increase their copy number within a host through various mechanisms of transposition. TEs can also move between species through unknown intermediaries in a process known as horizontal transfer, infecting novel genomes and increasing in copy number. While many individual invasions have been documented, a large dataset of recent horizontal transfer events that will allow us to understand larger more general HT patterns has not been assembled. In this manuscript we used almost 400 dipteran genomes to uncover 637 recent transposon invasions, mostly inDrosophila. The majority of transfers occurred between closely related species, with the cosmopolitanmelanogastergroup showing the highest recent transfer activity. We even documented a single transposon with 16 recent transfers, many between differentDrosophilagroups. Using species distance on a phylogenetic tree to measure the distance that transposons travel, we found that DNA transposons transfer between distantly related species much more frequently compared to retrotransposons. This potentially represents a different evolutionary strategy for exploiting naive genomes. Our phylogenetic framework advances the understanding of horizontal transfer dynamics at the species level withinDrosophila. 

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. 

Abstract Transposable elements are mobile DNA sequences capable of proliferating within host genomes, occasionally capable of crossing species boundaries via horizontal transfer (HT). Here, we report the discovery and characterization ofKuruka, a newly invading endogenous retrovirus in naturalD. melanogasterpopulations.Kurukaencodes an envelope protein and belongs to thegypsy/gypsysuperfamily. Analysis of over 1000D. melanogastergenomes revealed thatKurukafirst appeared in sub-Saharan Africa in 2010. By 2017-2019Kurukahad spread to Asia, Europe and America in 2017-2019, and is still actively invading Europe and Oceania as of 2021. Phylogenomic analyses suggest thatKurukaentered inD. melanogastervia a recent HT from an AfrotropicalDrosophilaspecies, most likelyD. erecta. This is the first case of a recent HT from an Afrotropical donor species toD. melanogaster. InD. erecta, Kurukahas a single genomic insertion, which is located withinflamenco, a master regulator of TE activity. The presence of an active host defense (piRNAs) suggests thatKurukais silenced inD. erecta. Our findings establishKurukaas a valuable model for studying the early stages of TE invasions and the dynamics of genome defense in real time. 

ABSTRACT While there is abundant theoretical work on the evolution of phenotype plasticity, empirical support has lagged. One model for the evolution of phenotype plasticity is by genetic accommodation. Under this model of evolution, when a population encounters a new environment there are widely variable responses among different genotypes, which are then pruned by selection into a single adaptive response. Because of the requirement to replicate genotypes, testing this prediction requires inbred lines as well as populations that are both adapted and not adapted to a resource. We previously demonstrated thatD. melanogasteradapted to ethanol through genetic accommodation usingD. simulansas an ancestral proxy lineage. However, we wondered how generalizable these results were. Here, we used a new population ofD. melanogasterfrom France and an ancestral range population from Zambia and measured behavioral tolerance to ethanol exposure in multiple genotypes from each population, as well as genome‐wide gene expression and alternative splicing in response to ethanol using RNA sequencing. We found that the ZambianD. melanogasterhave lower tolerance to ethanol than the FrenchD. melanogaster, with the Zambian flies becoming sedated while the French flies remain active under the same exposure. At the transcriptional level, Zambian genotypes showed extensive genotype‐specific changes in gene expression and splicing in response to ethanol exposure, while the French genotypes showed relatively modest and fewer genotype‐specific changes, consistent with having a more uniform, population response. We also found that gene expression and splicing appear to evolve independently of one another and that the splicing response to ethanol is largely distinct between populations. Thus, we have independently replicated evidence for evolution by genetic accommodation inD. melanogaster, suggesting that the evolution of plasticity may be an important contributor to the ability to exploit novel resources. 

Abstract Transposable elements (TEs) are repetitive sequences capable of mobilizing within genomes, exerting a significant influence on evolution throughout the tree of life. Using a novel approach that does not require prior knowledge of the sequence of repeats, we identified three novel TE invasions in Drosophila melanogaster: McLE spread between 1990–2000, Souslik between 2009–2012, and Transib1 between 2013–2016. We recapitulate previous findings, revealing that a total of 11 TEs invaded D. melanogaster over the past two centuries. These 11 invasions increased the fly genome by ∼1 Mbp. Using data from over 1,400 arthropod genomes, we provide evidence that these TE invasions were triggered by horizontal transfers, with Drosophila simulans and species of the Drosophila willistoni group acting as putative donors. Through the analysis of ∼600 short-read datasets spanning diverse geographic regions, we reveal the rapidity of TE invasions: Transib1 swiftly multiplied from three isolated epicenters in 2014 to all investigated populations in just 2 years. Our findings suggest that anthropogenic activities, which facilitate the range and population expansions of D. melanogaster, could have accelerated the rate of horizontal transposon transfer as well as the spread of the TEs into the worldwide population. Given the significant impact of TEs on evolution and the potential involvement of humans in their dispersal, our research has crucial implications for both evolution and ecology. 

Eukaryotic genomes are ubiquitously occupied by mobile genetic elements termed transposons, which are silenced via a specialized class of small RNA called piRNA. The small RNA is produced from the transposons themselves when they occupy specialized regions of the genome termed piRNA clusters. The formation of these specialized regions, or their evolution over time, is not well understood. Recent work has suggested that they are extremely variable even within a single species such as Drosophila melanogaster. We were interested in taking a comparative approach to piRNA cluster evolution to ask the question - what processes are unique to D.melanogaster and which are shared? Shared phenomena are more likely to be fundamental aspects of piRNA formation and evolution compared to those that are more labile. Using five high-quality long-read genome assemblies and five genotype-specific piRNA libraries, we approach this question from a population genetics standpoint. We annotate piRNA clusters, transposons, and structural variants in each of these five genomes. We found extensive variation in piRNA clusters across strains, with smaller piRNA clusters more likely to be limited to a single genotype. By and large, our results are consistent with a model of piRNA cluster evolution in which piRNA clusters are rapidly formed and lost, with a small subset increasing in frequency and length over time. However, we find that the TEs which nucleate the formation of small piRNA clusters are entirely distinct in D.simulans compared to D.melanogaster, and likely reflect its invasion history rather than any inherent property of the transposon to nucleate clusters. Therefore, while large common clusters can act as 'traps' as has been posited for piRNA clusters, there are also numerous small clusters that are born and lost rapidly within a species. 

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.