Transposable element competition in shaping the deer mouse genome

Abstract

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 and most LINE content is represented by a single family: L1. 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 other 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 relatively low LINE activity in addition to a massive invasion of lineage-specific endogenous retroviruses (ERVs). Deer mouse ERVs exhibit diverse origins spanning the retroviral phylogeny suggesting that these rodents have been host to a wide range of exogenous retroviruses. Notably, we were able to trace the origin of one ERV lineage, which arose within the last [~]11-18 million years, to a close relative of feline leukemia virus, revealing inter-ordinal horizontal transmission of these zoonotic viruses. Several lineage-specific ERV subfamilies have attained very high copy numbers, with the top five most abundant accounting for [~]2% of the genome. Concomitant to the expansive diversification of ERVs, we also observe a massive expansion of Kruppel-associated box domain-containing zinc finger genes (KZNFs), which likely control ERV activity and whose expansion may have been partially facilitated by ectopic recombination between ERVs. We also find evidence that ERVs directly impacted the evolutionary trajectory of LINEs by outcompeting them for genomic sites and frequently disrupting autonomous LINE copies. Together, our results illuminate the genomic ecology that shaped the deer mouse genomes TE landscape, opening up a range of opportunities to investigate the evolutionary processes that give rise to variation in mammalian genome structure. SummaryTransposable elements (TEs) are a highly diverse collection of genetic elements capable of mobilizing in genomes and function as important drivers of genome evolution. The landscape of TEs in a genome have been compared to a genomic ecosystem, with interactions between TEs and each other as well as TEs and their host, dictating the evolutionary success of TE lineages. While TE diversity and copy numbers can vary dramatically across taxa, the evolutionary reasons for this variation remain poorly understood. In mammals, long interspersed nuclear elements (LINEs) typically dominate, occupying more of the genome than any other TE. Here, we report a unique case in the deer mouse (Peromyscus maniculatus) in which long terminal repeat (LTR) retrotransposons occupy more of the genome than LINEs. We investigate the evolutionary origins and implications of the deer mouses distinct genomic landscape, revealing ecological processes that helped shape its evolution. Together, our results provide much-needed insight into the evolutionary processes that give rise to variation in mammalian genome structure.