Host phylogeny shapes viral transmission networks in an island ecosystem.

Rebecca K French, Sandra H Anderson, Kristal E Cain, Terry C Greene, Maria Minor, Colin M Miskelly, Jose M Montoya, Michelle Wille, Chris G Muller, Michael W Taylor, Andrew Digby, Edward C Holmes

Journal: Nature ecology & evolution 2023;7(11):1834-1843

PMID: 37679456

Abstract

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.

© 2023. The Author(s).

Address: Sydney Institute for Infectious Diseases, School of Medical Sciences, The University of Sydney, Sydney, New South Wales, Australia. [email protected].; School of Biological Sciences, University of Auckland, Auckland, New Zealand.; Biodiversity Group, Department of Conservation, Christchurch, New Zealand.; School of Natural Sciences, Massey University, Palmerston North, New Zealand.; Te Papa Tongarewa Museum of New Zealand, Wellington, New Zealand.; Theoretical and Experimental Ecology Station, National Centre for Scientific Research (CNRS), Moulis, France.; Sydney Institute for Infectious Diseases, School of Medical Sciences, The University of Sydney, Sydney, New South Wales, Australia.; Wildbase, School of Veterinary Science, Massey University, Palmerston North, New Zealand.; Kākāpō Recovery Team, Department of Conservation, Invercargill, New Zealand.; Sydney Institute for Infectious Diseases, School of Medical Sciences, The University of Sydney, Sydney, New South Wales, Australia. [email protected].

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