Transposable element competition in shaping the deer mouse genome

The genomic landscape of transposable elements (TEs) varies dramatically across species, with some TEs demonstrating greater success in colonizing particular lineages than others. In mammals, LINE retrotransposons typically occupy more of the genome than any other TE. Here, we report an unusual genomic landscape of TEs in the deer mouse, Peromyscus maniculatus , a model for studying the genomic basis of adaptation. In contrast to nearly all previously examined mammalian species, LTR elements occupy more of the deer mouse genome than LINEs (11% and 10% respectively). This pattern reflects a combination of reduced lineage-specific LINE gain in addition to a massive invasion of lineage-specific endogenous retroviruses (ERVs). Deer mouse ERVs exhibit diverse origins spanning the retroviral phylogeny and one likely arose de novo from an exogenous Feline Leukemia Virus within the last ~18 million years. Nonetheless, a few lineage-specific subfamilies account for a considerable proportion of ERV content, with the top five most abundant subfamilies occupying a remarkable ~2% of the genome. We also observe a massive expansion of lineage-specific Kruppel-associated box domain-containing zinc finger genes (KZNFs) which likely occurred to suppress ERV activity, and whose expansion may have been partially facilitated by ectopic recombination between ERVs. Significantly, we find evidence that ERVs directly impacted the evolutionary trajectory of LINEs by outcompeting them for genomic space and interrupting formerly intact LINE machinery. This model likely explains the unique genomic landscape of TEs observed in the deer mouse, and may also explain patterns of LINE inactivity in other mammals. Together, our results illuminate the genomic ecology that shaped the deer mouse genome's unique TE landscape, opening up a range of opportunities to investigate the evolutionary processes that give rise to variation in mammalian genome structure. ### Competing Interest Statement The authors have declared no competing interest.