Poxvirus gene repertoires are shaped by expansion-biased birth-and-death dynamics and genome architectural constraints

Abstract

Poxviruses (family Poxviridae) are DNA viruses with exceptionally large genomes containing hundreds of genes. Yet the evolutionary processes contributing to their numerous gene repertoires remain insufficiently understood. Here, we inferred ortholog groups of genes across 58 poxvirus genomes and comprehensively analyzed gene gain, gene duplication, gene loss, horizontal gene transfer, and synteny conservation. Across poxviruses, coding capacity scaled linearly with genome length. Gene repertoires evolved through birth-and-death dynamics but generally expanded because gene gain cumulatively exceeded gene loss and gained genes subsequently underwent further duplication. Gene gain and duplication were concentrated in the terminal regions of most poxvirus genomes. In viral lineages whose gene repertoires expanded extensively, terminal-region expansion was accompanied by further accumulation of duplicated genes within the otherwise conserved central genomic regions. The phylogenetic placement of the bird-infecting genus Avipoxvirus, together with evidence that several horizontally acquired genes originated from mammals, raises the possibility of a mammalian origin for Avipoxvirus. Altogether, our findings reveal that poxvirus gene repertoire evolution is shaped by expansion-biased birth-and-death dynamics and genome architectural constraints.