Lawlor, M. A. | bioRxiv Science

bioRxiv2025

Convergence and conflict among telomere specialized transposons across 60 million years of Drosophilid evolution

The Drosophila telomere is one of the best-studied examples of active transposable elements (TEs) benefitting, rather than harming, a host genome. All Drosophila species lack telomerase and instead have telomeres composed of head-to-tail arrays of specialized retrotransposons. These TEs ostensibly act as mutualists by elongating chromosome ends, but evidence from species closely related to Drosophila melanogaster suggests that telomeric transposons may also antagonize their host genome. Importantly, the limited number of Drosophila species characterized thus far has precluded our ability to delineate idiosyncratic from universal evolutionary forces and genetic mechanisms that shape the history of these TEs. Here, we have surveyed long-read genome assemblies of over 100 species of Drosophila, identifying a total of 396 telomeric TE families. Our findings show that these telomere-specialized elements evolve rapidly and also undergo striking convergent evolution: the complete loss of telomeric TEs has occurred repeatedly across the genus while individual telomeric TE lineages have repeatedly lost one of their two protein-coding genes. These elements have also repeatedly undergone horizontal transfer between distantly related Drosophila lineages and have repeatedly captured host gene fragments that promote their selfish suppression of host TE-silencing systems. Furthermore, telomere specialization itself appears to have evolved convergently, as some non-telomeric families have gained the ability to target their insertions to telomeres. These results provide unprecedented resolution into the evolution of these unusual TEs and highlight several novel mechanisms by which they evolve in conflict both with each other and their host genome despite the essential telomere function they provide.

genomics↗

bioRxiv2021

A burst of transposon expression accompanies the activation of Y chromosome fertility genes during Drosophila spermatogenesis

Transposable elements (TEs) must replicate in germline cells to pass novel insertions to offspring. In Drosophila melanogaster ovaries, TEs can exploit specific developmental windows of opportunity to evade host silencing and increase their copy numbers. However, TE activity and host silencing in the distinct cell types of the Drosophila melanogaster testis are not well understood. We reanalyzed publicly available single-cell RNA-seq datasets to quantify TE expression in the distinct cell types of the Drosophila testis. We developed a novel method for identification of TE and host gene expression programs and find that a distinct population of early spermatocytes expresses a large number of TEs at much higher levels than other germline and somatic components of the testes. This burst of TE expression coincides with the activation of Y chromosome fertility factors and spermatocyte-specific transcriptional regulators, as well as downregulation of many components of the piRNA pathway. The TEs expressed by this cell population are enriched on the Y chromosome and depleted on the X chromosome relative to other active TEs. These data suggest that some TEs may achieve high insertional activity in males by exploiting a window of opportunity for mobilization created by the activation of spermatocyte-specific and Y-chromosome-specific transcriptional programs.

genomics↗