Phylogeography of beak and feather disease virus from Australian cockatoos reflects host generalism and an order-wide quasispecies effect within Psittaciformes

We investigated the phylogeny of the highly genetically diverse but antigenically conserved, single-stranded circular, DNA genome of beak and feather disease virus (BFDV) in cockatoo species throughout Australia in order to understand the competing forces of host-switch events, recombination and high mutation rate alongside a predicted slow replication rate within connected ecosystems. Phylogenetic analyses of 38 new BFDV genomes from cockatoos were used to assess host and geographically based divergence as well as probable host-switch events. We found extremely high mutation rate for BFDV of 8.18 ×10-4 subs/site/year along with strong support for recombination indicating active cross-species transmission in various subpopulations. BFDV quasispecies were demonstrated with at least 30 genotypic variants identified within nine individual birds, with one containing up to seven genotypic variants. Single genetic variants were detected in feathers from 2 birds but splenic tissue provided further variants. The rich BFDV genetic diversity points to Australasia as the most likely geographical origin of this virus and supports a mosaic of geographic clustering throughout the landscape and flexible host switching. We propose this as evidence of an Order-wide quasispecies effect for BFDV in the Psittaciformes characterised by high mutability that is buffered by frequent recombination and slow replication strategy. Consistent with quasispecies theory we suggest that maximum attainable rather than average replication interval may be important for contributing to the high degree of genetic diversity seen in BFDV species as a whole.