Tracking Viral Evolution during a Disease Outbreak: the Rapid and Complete Selective Sweep of a Circovirus in the Endangered Echo Parakeet

Abstract

f Circoviruses are among the smallest and simplest of all viruses, but they are relatively poorly characterized. Here, we intensively sampled two sympatric parrot populations from Mauritius over a period of 11 years and screened for the circovirus Beak and feather disease virus (BFDV). During the sampling period, a severe outbreak of psittacine beak and feather disease, which is caused by BFDV, occurred in Echo parakeets. Consequently, this data set presents an ideal system for studying the evolution of a pathogen in a natural population and to understand the adaptive changes that cause outbreaks. Unexpectedly, we discovered that the outbreak was most likely caused by changes in functionally important regions of the normally conserved replicationassociated protein gene and not the immunogenic capsid. Moreover, these mutations were completely fixed in the Echo parakeet host population very shortly after the outbreak. Several capsid alleles were linked to the replication-associated protein outbreak allele, suggesting that whereas the key changes occurred in the latter, the scope of the outbreak and the selective sweep may have been influenced by positive selection in the capsid. We found evidence for viral transmission between the two host populations though evidence for the invasive species as the source of the outbreak was equivocal. Finally, the high evolutionary rate that we estimated shows how rapidly new variation can arise in BFDV and is consistent with recent results from other small singlestranded DNA viruses.

Evidence of Psittacine Beak and Feather Disease Virus Spillover Into Wild Critically Endangered Orange-Bellied Parrots (Neophema Chrysogaster)

“…The oral or cloacal transmission and environmental persistence of BFDV, as well as the predisposition of young birds to become infected, suggests a potentially significant role of shared nest hollows in facilitating spillover, allowing abundant parrot species to act as reservoirs for circovirus infection in very sparse or small populations of species such as the Orangebellied Parrot. An analogous situation has been documented in Mauritius, where BFDV transmission occurs between invasive and abundant Rose-ringed Parakeets (Psittacula krameri) and the endemic, endangered Echo Parakeet (Psittacula echo) (Kundu et al, 2012).…”

“…The species has been observed reusing nest hollows (Stojanovic et al, 2012) when flowering conditions are favorable. It is not surprising that PBFD infects birds through shared nest hollows, for although a degree of host specificity is seen in psittacine circoviruses, considerable host generalism is also observed in several lineages (Varsani et al, 2011;Kundu et al, 2012;Massaro et al, 2012). Furthermore, the likely prolonged environmental persistence of circovirus virions (Raidal and Cross, 1994;Yilmaz and Kaleta, 2004) provides a mechanism by which transmission can occur in otherwise ecologically disconnected species.…”

“…Like RNA and other ssDNA viruses, BFDV is prone to a high rate of genetic mutation, although the Rep gene is relatively conserved, which conveniently assists with diagnosing infection by PCR detection methods (Ypelaar et al, 1999). Within Psittaciformes, BFDV exhibits quasispecies characteristics with emerging geographic or host specificity demonstrable within various clades (Varsani et al, 2011) and the observed occurrence of closely related clades in highly divergent parrot species is evidence of host switching or host generalism in several BFDV lineages (Varsani et al, 2011;Julian et al, 2012;Kundu et al, 2012;Massaro et al, 2012).…”

Phylogenetic analysis of beak and feather disease virus across a host ring-species complex

“…BFDV occurs in many wild and captive parrot populations worldwide, with the potential to cause high mortality (25,26). Accordingly, it is considered a significant conservation threat and has been implicated in parrot declines in Australia and globally (27)(28)(29)(30). BFDV possesses a single-stranded DNA genome of ∼2,000 nucleotides (31).…”

Recurrent positive selection and heterogeneous codon usage bias events leading to coexistence of divergent pigeon circoviruses

“…Olvera et al (2007) believe the capsid gene is a more suitable marker for phylogenetic and epidemiological analyses and the characteristic of low recombination rates increases the detection accuracy of the signatures of positive selection on circovirus. Several studies have shown that natural selection plays an important role in the diversification of capsid proteins since they can evade the host immune system through amino acid replacement (Kundu et al, 2012;Olvera et al, 2007). Sequence differences between capsid protein genes could alter the antigenicity and cause cross-species transmission by changes in receptor specificity (Baranowski et al, 2001).…”