An essential telomere protein evolves adaptively to contain telomeric retrotransposons

Essential, conserved cellular and developmental processes depend not only on essential, conserved proteins but also on essential, unconserved proteins. These unconserved proteins evolve rapidly under positive selection, suggesting that some ostensibly static functions require recurrent innovation. To probe this paradox, we replaced an essential telomere binding protein in Drosophila melanogaster with a highly diverged version from its close relative, D. yakuba. This telomere-binding protein, HOAP, is required to protect chromosome ends from lethal end-to-end telomere fusions in D. melanogaster. We discovered that the D. yakuba version of HOAP localizes to D. melanogaster telomeres and supports robust end-protection. However, HOAP-yakuba fails to rescue a previously uncharacterized HOAP function: telomere length homeostasis. In a D. melanogaster background, HOAP-yakuba upregulates the telomeric retrotransposons that anciently replaced telomerase as the primary telomere elongation mechanism in Drosophila. Experimental evolution, combined with whole genome sequencing and cytogenetics, revealed that telomeric retrotransposons proliferate in the HOAP-yakuba genotype, resulting in aberrantly long telomeres. These data suggest that D. melanogaster requires species-specific HOAP residues to maintain telomere homeostasis. The proliferation of retrotransposons in the presence of a naive version of HOAP, combined with the rapid evolution of both HOAP and the telomeric retrotransposons, implicates an intra-genomic conflict shaping Drosophila telomere evolution.