Host phylogeny shapes viral transmission networks in an island ecosystem.

Virus transmission between host species underpins disease emergence. Both host phylogenetic relatedness and aspects of their ecology, such as species interactions and predator-prey relationships, may govern rates and patterns of cross-species virus transmission and hence zoonotic risk. To address the impact of host phylogeny and ecology on virus diversity and evolution, we characterized the virome structure of a relatively isolated island ecological community in Fiordland, New Zealand, that are linked through a food web. We show that phylogenetic barriers that inhibited cross-species virus transmission occurred at the level of host phyla (between the Chordata, Arthropoda and Streptophyta) as well as at lower taxonomic levels. By contrast, host ecology, manifest as predator-prey interactions and diet, had a smaller influence on virome composition, especially at higher taxonomic levels. The virus-host community comprised a 'small world' network, in which hosts with a high diversity of viruses were more likely to acquire new viruses, and generalist viruses that infect multiple hosts were more likely to infect additional species compared to host specialist viruses. Such a highly connected ecological community increases the likelihood of cross-species virus transmission, particularly among closely related species, and suggests that host generalist viruses present the greatest risk of disease emergence.

Novel viral and microbial species in a translocated Toutouwai (Petroica longipes) population from Aotearoa/New Zealand.

BACKGROUND: Translocation is a common tool in wildlife management and its implementation has resulted in many conservation successes. During translocations, any associated infectious agents are moved with their wildlife hosts. Accordingly, translocations can present a risk of infectious disease emergence, although they also provide an opportunity to restore natural infectious communities ('infectome') and mitigate the long-term risks of reduced natural resistance. METHODS: We used metatranscriptomic sequencing to characterise the cloacal infectome of 41 toutouwai (North Island robin, Petroica longipes) that were translocated to establish a new population within the North Island of New Zealand. We also screened for pathogenic bacteria, fungi and parasites. RESULTS: Although we did not detect any known avian diseases, which is a positive outcome for the translocated toutouwai population, we identified a number of novel viruses of interest, including a novel avian hepatovirus, as well as a divergent calici-like virus and four hepe-like viruses of which the host species is unknown. We also revealed a novel spirochete bacterium and a coccidian eukaryotic parasite. CONCLUSIONS: The presumably non-pathogenic viruses and microbial species identified here support the idea that most microorganisms likely do not cause disease in their hosts, and that translocations could serve to help restore and maintain native infectious communities. We advise greater surveillance of infectious communities of both native and non-native wildlife before and after translocations to better understand the impact, positive or negative, that such movements may have on both host and infectome ecology.

Metatranscriptomic Comparison of Viromes in Endemic and Introduced Passerines in New Zealand.

New Zealand/Aotearoa has many endemic passerine birds vulnerable to emerging infectious diseases. Yet little is known about viruses in passerines, and in some countries, including New Zealand, the virome of wild passerines has been only scarcely researched. Using metatranscriptomic sequencing we characterised the virome of New Zealand endemic and introduced species of passerine. Accordingly, we identified 34 possible avian viruses from cloacal swabs of 12 endemic and introduced bird species not showing signs of disease. These included a novel siadenovirus, iltovirus, and avastrovirus in the Eurasian blackbird (Turdus merula, an introduced species), song thrush (Turdus philomelos, introduced) and silvereye/tauhou (Zosterops lateralis, introduced), respectively. This is the first time novel viruses from these genera have been identified in New Zealand, likely reflecting prior undersampling. It also represents the first identification of an iltovirus and siadenovirus in blackbirds and thrushes globally. These three viruses were only found in introduced species and may pose a risk to endemic species if they were to jump species boundaries, particularly the iltoviruses and siadenoviruses that have a prior history of disease associations. Further virus study and surveillance are needed in New Zealand avifauna, particularly in Turdus populations and endemic species.

An Ecosystems Perspective on Virus Evolution and Emergence.

Understanding the emergence of pathogenic viruses has dominated studies of virus evolution. However, new metagenomic studies imply that relatively few of an immense number of viruses may lead to overt disease. This suggests a change in emphasis, from viruses as habitual pathogens to integral components of ecosystems. Here we show how viruses alter interactions between host individuals, populations, and ecosystems, impacting ecosystem health, resilience, and function, and how host ecology in turn impacts viral abundance and diversity. Moving to an ecosystems perspective will put virus evolution and disease emergence in its true context, and enhance our understanding of ecological processes.