Abstract
Quasispecies variants and recombination were studied longitudinally in an emergent outbreak of beak and feather disease virus (BFDV) infection in the orange-bellied parrot (Neophema chrysogaster). Detailed health monitoring and the small population size (<300 individuals) of this critically endangered bird provided an opportunity to longitudinally track viral replication and mutation events occurring in a circular, single-stranded DNA virus over a period of four years within a novel bottleneck population. Optimized PCR was used with different combinations of primers, primer walking, direct amplicon sequencing and sequencing of cloned amplicons to analyze BFDV genome variants. Analysis of complete viral genomes (n = 16) and Rep gene sequences (n = 35) revealed that the outbreak was associated with mutations in functionally important regions of the normally conserved Rep gene and immunogenic capsid (Cap) gene with a high evolutionary rate (3.41×10−3 subs/site/year) approaching that for RNA viruses; simultaneously we observed significant evidence of recombination hotspots between two distinct progenitor genotypes within orange-bellied parrots indicating early cross-transmission of BFDV in the population. Multiple quasispecies variants were also demonstrated with at least 13 genotypic variants identified in four different individual birds, with one containing up to seven genetic variants. Preferential PCR amplification of variants was also detected. Our findings suggest that the high degree of genetic variation within the BFDV species as a whole is reflected in evolutionary dynamics within individually infected birds as quasispecies variation, particularly when BFDV jumps from one host species to another.
Highlights
Psittacine beak and feather disease (PBFD) is recognized as a key threatening process for endangered Australian psittacine birds and is a well characterized threat to a wide variety of psittacine bird species globally [1]
This paper describes a longitudinal study of quasispecies variants and recombination events in an emergent outbreak of beak and feather disease virus (BFDV) infection in a naıve population of the critically endangered orange-bellied parrot
Whilst the origins of the BFDV infections in this population of birds are unknown it is almost certain to have been another psittacine bird species, presumably from the wild in Tasmania, and not from within the orange-bellied parrot population given its small size, as well as the pre-existing health monitoring that was in place immediately before the outbreak of infection that indicated an absence of both viremic birds and circulating antibodies to BFDV
Summary
Psittacine beak and feather disease (PBFD) is recognized as a key threatening process for endangered Australian psittacine birds and is a well characterized threat to a wide variety of psittacine bird species globally [1]. The disease can be expressed peracutely, ranging from sudden death, in neonates [7] or as an acute form in nestling and fledglings, characterized by feather dystrophy, diarrhoea, weakness and depression leading to death within 1–2 weeks [7] or with a chronic prolonged course of feather dystrophy eventually leading to mortality [8]. Compared with other non-enveloped DNA viruses, of which the 5 kb circular genome of avian polyomavirus is probably the best benchmark, BFDV is highly genetically diverse and prone to genetic mutation, yet antigenically conserved [13,14,15]. Within Psittaciformes as a whole BFDV exhibits quasispecies characteristics with emerging geographic or host-specificity demonstrable within various clades while the observed occurrence of closely related clades in highly divergent parrot species is evidence of either host-switching or host-generalism in several BFDV lineages [16]
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