Endogenous Viral Elements in Animal Genomes

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Abstract
Integration into the nuclear genome of germ line cells can lead to vertical inheritance of retroviral genes as host alleles. For other viruses, germ line integration has only rarely been documented. Nonetheless, we identified endogenous viral elements (EVEs) derived from ten non-retroviral families by systematic in silico screening of animal genomes, including the first endogenous representatives of double-stranded RNA, reverse-transcribing DNA, and segmented RNA viruses, and the first endogenous DNA viruses in mammalian genomes. Phylogenetic and genomic analysis of EVEs across multiple host species revealed novel information about the origin and evolution of diverse virus groups. Furthermore, several of the elements identified here encode intact open reading frames or are expressed as mRNA. For one element in the primate lineage, we provide statistically robust evidence for exaptation. Our findings establish that genetic material derived from all known viral genome types and replication strategies can enter the animal germ line, greatly broadening the scope of paleovirological studies and indicating a more significant evolutionary role for gene flow from virus to animal genomes than has previously been recognized. The presence of retrovirus sequences in animal genomes has been recognized since the 1970s, but is readily explained by the fact that these viruses integrate into chromosomal DNA as part of their normal replication cycle. Unexpectedly, however, we identified a large and diverse population of sequences in animal genomes that are derived from non-retroviral viruses. Analysis of these sequences—which represent all known virus genome types and replication strategies—reveals new information about the evolutionary history of viruses, in many cases providing the first and only direct evidence for their ancient origins. Additionally, we provide evidence that the functionality of one of these sequences has been maintained in the host genome over many millions of years, raising the possibility that captured viral sequences may have played a larger than expected role in host evolution.