Circoviruses evolve more slowly than their hosts

Emerging evidence of endogenous viral elements in host genomes hints towards much older host-virus relationships than predicted by exogenous phylogenies. Resolving the long-term evolutionary history of vertebrate virus-host association and determining the age of a potentially ancient tree based only fresh shoots at the tips is problematic, especially when purifying selection or recombination significantly alters the accuracy of phylogenetic reconstruction methods. Pathogens which occupy entangled multispecies ecological niches add a further layer of complexity but these multi-host scenarios may also provide opportunities to identify allopatric orsympatric paleobiological signals that can unlock longer term phylogenies. Circoviruses are highly mutable single-stranded DNA (ssDNA) viruses with a high rate of genetic admixture through recombination, particularly in beak and feather disease virus (BFDV) which provides an excellent model for studying multi-host scenarios with host-switching events. We generated whole genome circoviral sequences from Australian psittacine birds and analysed those using phylogenetic reconstruction and population genetics approach to infer the macroevolutionary scenario. Endogenous circoviral motifs in kea (Nestor notabilis) with Gondwanan vicariance estimates were used to calibrate the evolutionary timescale. We identified host-based, cryptic, sympatric differentiation in BFDV in the Psittaciforme tribe Loriini with 10 million year divergence coinciding with the Papuan central range orogeny that triggered the radiation of Loriini and segregation of an antecedent viral clade in Australian lorikeets. We also demonstrated a chronology of circovirus speciation in birds highlighting a Gondwanan dominant group in Neoaves with passerine, columbid and larid circoviruses deeply separated from those in waterfowl, consistent with a Triassic divergence of Galloanserae. The circovirus tree had a deep ancestry in invertebrates with a Palaeozoic expansion in fish and mammals. We show how a virus that mutates rapidly might also retain phenotypic stability and wait millennia to change hosts or become a recognisable new virus species, a process that could lag well behind the evolution of the potential hosts.