In most eukaryotes, telomerase counteracts chromosome erosion by adding repetitive sequence to terminal ends. Drosophila melanogaster instead relies on specialized retrotransposons that insert exclusively at telomeres. This exchange of goods between host and mobile element-wherein the mobile element provides an essential genome service and the host provides a hospitable niche for mobile element propagation-has been called a "genomic symbiosis." However, these telomerespecialized, jockey family retrotransposons may actually evolve to "selfishly" overreplicate in the genomes that they ostensibly serve. Under this model, we expect rapid diversification of telomere-specialized retrotransposon lineages and, possibly, the breakdown of this ostensibly symbiotic relationship. Here we report data consistent with both predictions. Searching the raw reads of the 15-Myr-old melanogaster species group, we generated de novo jockey retrotransposon consensus sequences and used phylogenetic tree-building to delineate four distinct telomere-associated lineages. Recurrent gains, losses, and replacements account for this retrotransposon lineage diversity. In Drosophila biarmipes, telomere-specialized elements have disappeared completely. De novo assembly of long reads and cytogenetics confirmed this species-specific collapse of retrotransposon-dependent telomere elongation. Instead, telomere-restricted satellite DNA and DNA transposon fragments occupy its terminal ends. We infer that D. biarmipes relies instead on a recombination-based mechanism conserved from yeast to flies to humans. Telomeric retrotransposon diversification and disappearance suggest that persistently "selfish" machinery shapes telomere elongation across Drosophila rather than completely domesticated, symbiotic mobile elements.

Abstract The germlines of metazoans contain transposable elements (TEs) causing genetic instability and affecting fitness. To protect the germline from TE activity, gonads of metazoans produce TE-derived PIWI-interacting RNAs (piRNAs) that silence TE expression. In Drosophila, our understanding of piRNA biogenesis is mainly based on studies of the Drosophila melanogaster female germline. However, it is not known whether piRNA functions are also important in the male germline or whether and how piRNAs are affected by the global genomic context. To address these questions, we compared genome sequences, transcriptomes, and small RNA libraries extracted from entire testes and ovaries of two sister species: D. melanogaster and Drosophila simulans. We found that most TE-derived piRNAs were produced in ovaries and that piRNA pathway genes were strongly overexpressed in ovaries compared with testes, indicating that the silencing of TEs by the piRNA pathway mainly took place in the female germline. To study the relationship between host piRNAs and TE landscape, we analyzed TE genomic features and how they correlate with piRNA production in the two species. In D. melanogaster, we found that TE-derived piRNAs target recently active TEs. In contrast, although Drosophila simulans TEs do not display any features of recent activity, the host still intensively produced silencing piRNAs targeting old TE relics. Together, our results show that the piRNA silencing response mainly takes place in Drosophila ovaries and indicate that the host piRNA response is implemented following a burst of TE activity and could persist long after the extinction of active TE families.