Recombination marks the evolutionary dynamics of a recently endogenized retrovirus

Abstract

Background: All vertebrate genomes have been colonized by retroviruses along their evolutionary trajectory. Although it is clear that endogenous retroviruses (ERVs) can contribute important physiological functions to contemporary hosts, such benefits are attributed to long-term co-evolution of ERV and host. Newly colonized ERVs are thought unlikely to contribute to host genome evolution because germline infections are rare and because the host effectively silences them. The genomes of several outbred species including mule deer (Odocoileus hemionus) are currently being colonized by ERVs, which provides an opportunity to study ERV dynamics at a time when few are fixed. Here we investigate the history of cervid endogenous retrovirus (CrERV) acquisition and expansion in the mule deer genome to determine the potential impact of endogenizing retroviruses on host genomic diversity. Methods: A mule deer genome was de novo assembled from short and long insert mate pair reads. Scaffolds were further assembled using reference assisted chromosome assembly (RACA) to provide spatial orientation of CrERV insertion sites and to facilitate assembly of CrERV sequences. We applied phylogenetic and coalescent approaches to non-recombinant genomes to determine CrERV evolutionary history, augmenting ancestral divergence estimates with the prevalence of each CrERV locus in a population of mule deer. Recombination history was investigated on partial genome alignments. Results: The CrERV composition and diversity in the mule deer genome has recently measurably increased by horizontal acquisition of a new retroviruses lineage and because of recombination with existing CrERV. Resulting interlineage recombinants also endogenized and subsequently retrotransposed. CrERV loci are significantly closer to genes than expected if integration were random and gene proximity might explain the recent expansion by retrotransposition of one recombinant CrERV lineage. Conclusions: There has been a burst of CrERV integrations during a recent retrovirus epizootic that increased genomic CrERV burden and has resulted in extensive insertional polymorphism in contemporary mule deer genomes. Recombination is a defining feature of CrERV evolutionary dynamics driven by this colonization, increasing CrERV burden and CrERV genetic diversity. These data support that retroviral colonization during an epizootic provides a burst of genomic diversity to the host population.