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Host-virus association data underpin research into the distribution and eco-evolutionary correlates of viral diversity and zoonotic risk across host species. However, current knowledge of the wildlife virome is inherently constrained by historical discovery effort, and there are concerns that the reliability of ecological inference from host-virus data may be undermined by taxonomic and geographical sampling biases. Here, we evaluate whether current estimates of host-level viral diversity in wild mammals are stable enough to be considered biologically meaningful, by analysing a comprehensive dataset of discovery dates of 6571 unique mammal host-virus associations between 1930 and 2018. We show that virus discovery rates in mammal hosts are either constant or accelerating, with little evidence of declines towards viral richness asymptotes, even in highly sampled hosts. Consequently, inference of relative viral richness across host species has been unstable over time, particularly in bats, where intensified surveillance since the early 2000s caused a rapid rearrangement of species' ranked viral richness. Our results illustrate that comparative inference of host-level virus diversity across mammals is highly sensitive to even short-term changes in sampling effort. We advise caution to avoid overinterpreting patterns in current data, since it is feasible that an analysis conducted today could draw quite different conclusions than one conducted only a decade ago. 

ABSTRACT Data that catalogue viral diversity on Earth have been fragmented across sources, disciplines, formats, and various degrees of open sharing, posing challenges for research on macroecology, evolution, and public health. Here, we solve this problem by establishing a dynamically maintained database of vertebrate-virus associations, called The Global Virome in One Network (VIRION). The VIRION database has been assembled through both reconciliation of static data sets and integration of dynamically updated databases. These data sources are all harmonized against one taxonomic backbone, including metadata on host and virus taxonomic validity and higher classification; additional metadata on sampling methodology and evidence strength are also available in a harmonized format. In total, the VIRION database is the largest open-source, open-access database of its kind, with roughly half a million unique records that include 9,521 resolved virus “species” (of which 1,661 are ICTV ratified), 3,692 resolved vertebrate host species, and 23,147 unique interactions between taxonomically valid organisms. Together, these data cover roughly a quarter of mammal diversity, a 10th of bird diversity, and ∼6% of the estimated total diversity of vertebrates, and a much larger proportion of their virome than any previous database. We show how these data can be used to test hypotheses about microbiology, ecology, and evolution and make suggestions for best practices that address the unique mix of evidence that coexists in these data. IMPORTANCE Animals and their viruses are connected by a sprawling, tangled network of species interactions. Data on the host-virus network are available from several sources, which use different naming conventions and often report metadata in different levels of detail. VIRION is a new database that combines several of these existing data sources, reconciles taxonomy to a single consistent backbone, and reports metadata in a format designed by and for virologists. Researchers can use VIRION to easily answer questions like “Can any fish viruses infect humans?” or “Which bats host coronaviruses?” or to build more advanced predictive models, making it an unprecedented step toward a full inventory of the global virome. 

Abstract The fields of viral ecology and evolution are rapidly expanding, motivated in part by concerns around emerging zoonoses. One consequence is the proliferation of host–virus association data, which underpin viral macroecology and zoonotic risk prediction but remain fragmented across numerous data portals. In the present article, we propose that synthesis of host–virus data is a central challenge to characterize the global virome and develop foundational theory in viral ecology. To illustrate this, we build an open database of mammal host–virus associations that reconciles four published data sets. We show that this offers a substantially richer view of the known virome than any individual source data set but also that databases such as these risk becoming out of date as viral discovery accelerates. We argue for a shift in practice toward the development, incremental updating, and use of synthetic data sets in viral ecology, to improve replicability and facilitate work to predict the structure and dynamics of the global virome. 

In the light of the urgency raised by the COVID-19 pandemic, global investment in wildlife virology is likely to increase, and new surveillance programmes will identify hundreds of novel viruses that might someday pose a threat to humans. To support the extensive task of laboratory characterization, scientists may increasingly rely on data-driven rubrics or machine learning models that learn from known zoonoses to identify which animal pathogens could someday pose a threat to global health. We synthesize the findings of an interdisciplinary workshop on zoonotic risk technologies to answer the following questions. What are the prerequisites, in terms of open data, equity and interdisciplinary collaboration, to the development and application of those tools? What effect could the technology have on global health? Who would control that technology, who would have access to it and who would benefit from it? Would it improve pandemic prevention? Could it create new challenges? This article is part of the theme issue ‘Infectious disease macroecology: parasite diversity and dynamics across the globe’.