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Papillomaviruses (PVs) are ancient viruses infecting vertebrates, from fishes to mammals. Although the genomes of PVs are small and show conserved synteny, PVs display large genotypic diversity and ample variation in the phenotypic presentation of the infection. Most PV genomes contain two small early genes  E6  and  E7 . In a bunch of closely related human papillomaviruses (HPVs), the E6 and E7 proteins provide the viruses with oncogenic potential. The recent discoveries of PVs without  E6  and  E7  in different fish species place a new root on the PV tree, and suggest that ancestral PVs consisted of the minimal PV backbone  E1-E2-L2-L1 . Bayesian phylogenetic analyses date the most recent common ancestor of the PV backbone to 424 million years ago (Ma). Common ancestry tests on extant  E6  and  E7  genes indicate that they share a common ancestor dating back to at least 184 Ma. In  AlphaPVs  infecting Old World monkeys and apes, the appearance of the  E5  oncogene 53–58 Ma concurred with (i) a significant increase in substitution rate, (ii) a basal radiation and (iii) key gain of functions in E6 and E7. This series of events was instrumental to construct the extant phenotype of oncogenic HPVs. Our results assemble the current knowledge on PV diversity and present an ancient evolutionary timeline punctuated by evolutionary innovations in the history of this successful viral family.  This article is part of the theme issue ‘Silent cancer agents: multi-disciplinary modelling of human DNA oncoviruses’.

Origin and evolution of papillomavirus (onco)genes and genomes