Opportunistic sampling of wild native and invasive birds reveals a rich diversity of adenoviruses in Australia

Abstract

Little is known about the diversity of adenoviruses in wild birds and how they have evolved and are maintained in complex ecosystems. In this study, 409 samples were collected from woodland birds caught for banding (droppings), birds submitted to a wildlife hospital (droppings and tissues), silver gulls (droppings or tissues), and feral pigeons (Columbia livia; oral, cloacal swabs, or tissues) from the Greater Sydney area in NSW, Australia. Additional samples were from native pigeons and doves (swabs) presented to the Healesville Sanctuary, VIC, Australia. Samples were screened for adenovirus DNA using degenerate primers and polymerase chain reaction. Adenovirus sequences were detected in eighty-three samples representing thirty-five novel amino acid sequences. Fourteen novel sequences were atadenoviruses, seven were aviadenoviruses, twelve were siadenoviruses, and one was a mastadenovirus. Sequences from passerine birds were predominately found to form a single lineage within the atadenoviruses, a second lineage in the siadenoviruses, and a third smaller aviadenovirus lineage. These viruses appeared to have co-evolved with a diverse group of woodland birds that share similar habitat. Evidence for host/virus co-evolution in some viruses and a wide host range in others was observed. A high prevalence of adenovirus infection was found in rainbow lorikeets (Trichoglossus haematodus), galahs (Eolophus roseicapilla), and sulphur-crested cockatoos (Cacatua galerita). Sequences were either identical to or mapped to already established lineages in the Aviadenovirus, Siadenovirus, and Atadenovirus genera, suggesting a possible origin of the psittacine adenoviruses in ancestral Australian psittacine birds. The sequences of passerine and psittacine origin provided insight into diversity and structure of the Atadenovirus genus and demonstrated for the first-time viruses of passerine origin in the Aviadenovirus genus. Four unrelated adenovirus sequences were found in silver gull samples (Chroicocephalus novaehollandiae), including one of pigeon origin, suggesting environmental virus exposure. Three pigeon adenovirus types were detected in feral pigeons and infection prevalence was high. Evidence for host switching between invasive species and native species and native species and invasive species was documented. A variant of a murine adenovirus was detected in kidney tissue from two bird species suggesting mouse to bird transmission.

Keywords: Australia; adenovirus; bird; diversity; evolution.

Figure 1.

Map of Southeast Australia showing sites where wild birds were caught in mist nets and sampled and location of the University of Sydney Avian Reptile and Exotic Pet Hospital.

Figure 2.

Bootstrap Network (1,000 replicates) generated using SplitsTree4.15.1 and partial DNA polymerase gene amino acid sequences from representative adenoviruses and adenovirus sequences obtained from the birds surveyed in this study. Bootstrap values that exceeded 70 per cent are shown. Murine adenovirus 2 variant 1 was found in the four species of birds in parenthesis; however, it is suspected to be of murine origin. Underlined virus sequences are adenoviruses of birds that have been documented in Australia. Virus sequences identified with an asterisk (*) where found in this study. Adenoviruses identified with a hashtag (#) were found in more than one species of bird, either in this study or were found in this study and/or one or more studies by others: Passerine 1: noisy miner, New Holland honeyeater, Indian mynah (all this study); Passerine 2: eastern shrike-tit, eastern yellow robin (all this study); Passerine 3: red-browed finch, silvereye, superb fairy-wren (all this study); Psittacine 1 (psittacine adenovirus 1): Senegal parrot (Italy), rainbow lorikeet (this study); psittacine avia B (psittacine aviadenovirus B): red-bellied parrot, purple-crowned parrot (Australia); psittacine 2 (psittacine adenovirus 2): multiple species (USA and Europe) multiple captive species (Australia); psittacine D (proposed name psittacine siadenovirus D): Budgerigar (Australia), rainbow lorikeet and galah (both this study), variants of this virus sequences found in a budgerigar (Japan), and cockatiel (USA). Pigeon 1 (pigeon adenovirus 1), pigeon B (pigeon adenovirus 2), and pigeon 4 (pigeon adenovirus 4): Feral and domestic pigeons Europe and feral pigeons Australia (this study).