Project FlyInnovation: conflict or cooperation between transposons and their Drosophila hosts?

The Diptera’s solution to the end-replication problem – selfish genetic elements as an insect innovation?

Eukaryotes face a challenge: protecting coding DNA from the shortening of chromosomal termini with each round of cell replication. Telomeres are a widespread solution to this challenge. These repetitive DNA motifs cap chromosome ends and buffer coding DNA from attrition. Telomeres themselves are maintained by the enzyme telomerase, which adds repeating DNA motifs onto chromosome ends. Telomeres and telomerase are vital to chromosome integrity and are highly evolutionarily conserved. This makes the Diptera unusual – flies have lost telomeric repeats and telomerase. Among the Diptera, Drosophila are unique: they are the only genus we know of where transposable elements (TEs) are the sole means of maintaining chromosome ends. These TEs act like telomerase, extending telomeric regions by successive transposition. This system has been heralded as a clear-cut example of TE domestication but evidence in support of this idea is lacking and the evolution of telomere-specific TEs is not well understood. FlyInnovation will determine if telomere-specific TEs are an innovative means of preserving telomeres in the absence of telomerase or simply selfish genetic elements avoiding host-silencing in a genomic safe-site. To achieve this, we will apply concepts from ecology to model the evolutionary dynamics of TEs under neutral scenarios, and empirically test for signatures of conflict or cooperation between host and TEs to understand any deviation from neutral modelling predictions. To elucidate the evolutionary origin of this potential genomic innovation, we will characterize the diversity of telomere-specific TEs across the Drosophila genus and, more generally, determine how other Diptera protect telomeric regions in the absence of telomerase. By integrating theoretical and empirical approaches across taxonomic levels, we will gain insight into TE domestication and the evolutionary drivers of innovative mechanisms of telomere maintenance.

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