Functional Adaptations of Endogenous Retroviruses to the Drosophila Host Underlie their Evolutionary Diversification

Transposable elements profoundly affect the biology and evolution of their hosts, yet their own evolutionary dynamics remain poorly understood. Here, we investigate insect endogenous retroviruses (iERVs), a monophyletic group of LTR retrotransposons that have acquired the trait of infectivity, likely through capture of a Baculovirus envelope gene. In Drosophila ovaries, iERVs with functional envelope have adapted their cis-regulatory sequences to be expressed in any somatic cell type, from where they infect the germline. Strikingly, related retroviruses show distinct expression patterns, indicating niche partitioning. In contrast, all non-infectious iERVs that emerged through secondary envelope-loss are specifically expressed in the germline. Co-evolving with iERVs, the genome-protecting piRNA pathway has assimilated iERV promoter and sequence information into piRNA clusters, underscoring the functional significance of iERV expression in somatic niches. We propose that the evolutionary innovation of cell-to-cell infectivity has triggered the adaptive radiation of iERVs through trait diversification and antagonistic virus-host interactions, processes that likely underpin niche-specific expression of endogenous retroviruses in vertebrates as well.