Abstract
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.
Highlights
Pathogens are unevenly distributed across host species, and understanding the underlying coevolutionary processes is important for both ecological and health-motivated research
Even when a species’ total viral diversity has been ground-truthed by thorough metagenomic sampling and rarefaction-based estimation [15], estimates suggest only approximately 3–7% of their viruses are captured by current host-virus association data [10]. With such a small proportion of viruses described, it is plausible that comparative studies of viral diversity are using numbers that are both subject to change and highly sensitive to differences in sampling strategies between different host and virus groups. We explore these questions using a dataset of 6571 mammal host-virus associations and their year of discovery, representing a comprehensive inventory of known associations from 1930 to 2018
Analyses were conducted in R v. 4.0.3 [21]. Both cumulative discovery curves and fitted generalized additive models (GAMs) show that viral discovery in mammals is still in an upward growth phase, with little evidence of discovery rates declining towards zero in any group
Summary
Pathogens are unevenly distributed across host species, and understanding the underlying coevolutionary processes is important for both ecological and health-motivated research. An even greater proportion of the global virome remains completely undescribed [10,11], with current knowledge strongly influenced by discovery strategies [12] This may undermine inference about the distribution of zoonotic risk among host taxa [9], and multiple studies have shown that apparent patterns in zoonotic virus richness become insignificant after adjusting for total viral richness [13,14]. It remains unclear how this impacts more basic scientific questions, including those concerning macroecological patterns in species-level viral diversity
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