Evolution of circoviruses in lorikeets lags behind its hosts.
The presence of endogenous viral elements in host genomes hints towards much older host-virus relationships than predicted by exogenous phylogenies, with highly mutable single-stranded DNA (ssDNA) viruses and RNA viruses often occupying entangled multispecies ecological niches. The difficulty lies in unravelling the long-term evolutionary history of vertebrate virus-host relationships and determining the age of a potentially ancient tree based only fresh shoots at the tips. Resolving such lineages, and the sometimes great discrepancy amongst evolutionary timescales, is problematic, especially when purifying selection or recombination can significantly alter the accuracy of phylogenetic reconstruction methods. Pathogens which occupy entangled multispecies ecological niches add a further layer of complexity but we show that multi-host scenarios may also provide opportunities to identify allopatric or sympatric paleobiological signals that can unlock longer term phylogenies. We identified host-based, cryptic, sympatric differentiation in beak and feather disease virus in the Psittaciformes tribe Loriini along with endogenous circovirus motifs in Kea (Nestor notabilis) and Gondwanan vicariance estimates to infer the evolutionary timescale of the circoviruses. This demonstrated a chronology of psittacine circovirus speciation aligned to conservative Zealandic divergences for relic circovirus motifs in Kea and a 10million 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. Estimates of circovirus speciation in birds highlighted 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 that longer term evolutionary relationships in viruses which have a high rate of mutation and admixture can be disentangled, highlighting that contemporary virus host-switching can be explained by deep intra-lineage host phylogeny.
School of Animal and Veterinary Sciences, Charles Sturt University, Boorooma St, Wagga Wagga, New South Wales 2678, Australia; Graham Centre for Agricultural Innovation, Pine Gully Road, Wagga Wagga, New South Wales 2650, Australia. Electronic address: sdas@csu.edu.au.
Shubhagata
S
Das
School of Animal and Veterinary Sciences, Charles Sturt University, Boorooma St, Wagga Wagga, New South Wales 2678, Australia; Graham Centre for Agricultural Innovation, Pine Gully Road, Wagga Wagga, New South Wales 2650, Australia. Electronic address: ssarker@csu.edu.au.
Subir
S
Sarker
School of Animal and Veterinary Sciences, Charles Sturt University, Boorooma St, Wagga Wagga, New South Wales 2678, Australia; Graham Centre for Agricultural Innovation, Pine Gully Road, Wagga Wagga, New South Wales 2650, Australia. Electronic address: apeters@csu.edu.au.
Andrew
A
Peters
School of Animal and Veterinary Sciences, Charles Sturt University, Boorooma St, Wagga Wagga, New South Wales 2678, Australia; Graham Centre for Agricultural Innovation, Pine Gully Road, Wagga Wagga, New South Wales 2650, Australia. Electronic address: aghorashi@csu.edu.au.
Seyed A
SA
Ghorashi
Faculty of Veterinary Science, The University of Sydney, 425 Werombi Road, Camden, New South Wales 2570, Australia. Electronic address: david.phalen@sydney.edu.au.
David
D
Phalen
Graham Centre for Agricultural Innovation, Pine Gully Road, Wagga Wagga, New South Wales 2650, Australia; School of Biomedical, Charles Sturt University, Boorooma St, Wagga Wagga, New South Wales 2678, Australia. Electronic address: jforwood@csu.edu.au.
Jade K
JK
Forwood
School of Animal and Veterinary Sciences, Charles Sturt University, Boorooma St, Wagga Wagga, New South Wales 2678, Australia; Graham Centre for Agricultural Innovation, Pine Gully Road, Wagga Wagga, New South Wales 2650, Australia. Electronic address: shraidal@csu.edu.au.
Shane R
SR
Raidal
D000818:Animals; D001715:Bird Diseases / Q000235:genetics / Q000821:virology*; D018173:Circoviridae Infections / Q000662:veterinary* / Q000821:virology; D017925:Circovirus / Q000235:genetics*; D019143:Evolution, Molecular; D005814:Genes, Viral; D014644:Genetic Variation; D016679:Genome, Viral; D008969:Molecular Sequence Data; D010311:Parrots / Q000235:genetics* / Q000821:virology; D010802:Phylogeny; D012641:Selection, Genetic; D056189:Viral Tropism
BFDV; Circoviridae; Circovirus; Host-parasite co-evolution; Host-switch; Paleovirology; Rate of evolution; Virus speciation; ssDNA virus