Host and viral traits predict zoonotic spillover from mammals

Abstract

The majority of human emerging infectious diseases (EIDs) are zoonotic, with viruses originating in wild mammals of particular concern (e.g. HIV, Ebola, SARS)1–3. Understanding patterns of viral diversity in wildlife and determinants of successful cross-species transmission, or spillover, are therefore key goals for pandemic surveillance programs4. However, few analytical tools exist to identify which host species likely harbor the next human virus, or which viruses can cross species boundaries5–7. Here we conduct the most comprehensive analysis yet of mammalian host-virus relationships and show that both the total number of viruses that infect a given species, and the proportion likely to be zoonotic are predictable. After controlling for research effort, the proportion of zoonotic viruses per species is predicted by phylogenetic relatedness to humans, host taxonomy, and human population within a species range – which may reflect human-wildlife contact. We demonstrate for the first time that bats harbor a significantly higher proportion of zoonotic viruses than all other mammalian orders. We identify the taxa and geographic regions with the largest estimated number of ‘missing viruses’ and ‘missing zoonoses’ and therefore of highest value for future surveillance. We then show that phylogenetic host breadth and other viral traits are significant predictors of zoonotic potential, providing a novel framework to assess if a newly discovered mammalian virus could infect people.

When bats go viral: negative framings in virological research imperil bat conservation

“…For instance, authors reported that "many zoonotic viruses that have emerged recently are thought to have their origins in bats" (Wang et al 2015) and that "many emerging and re-emerging infectious diseases are zoonoses derived from wildlife, particularly bats" (Wynne et al 2014). Although it has recently been found that bats host a significantly higher proportion of zoonoses than other mammals (Olival et al 2017), there are still only poor real-world data showing to which extent such diseases might jump from wildlife to humans (Kupferschmidt 2017). Moreover, direct associations of unrelated statements placed in proximity and missing critical information led to misleading conclusions.…”

“…Although we acknowledge that bats may represent an important share of natural virus reservoirs (Anthony et al 2017, Maxmen 2017, Olival et al 2017) that might eventually pose danger to people, we remain firm in asserting that the risk of virus transmission from bats to humans is small (Kingston 2016, Anthony et al 2017, an aspect that is worryingly neglected in most virological bat-related publications. Moreover, the fact that an increasing number of virus outbreaks is largely attributable to human encroachment in natural areas (Buttke et al 2015, Terraube et al 2017) is rarely publicised.…”

“…Bat-associated health risks have all the traits needed for them to be amplified through social media platforms, given the wide array of negative images that bats evoke in the general public. For example, a recent review on zoonotic patterns of viral diversity in wildlife (Olival et al 2017) was covered in the media with headlines such as "Bats are special, but not in a good way" (Anonymous 2017a) and "Bats are the number-one carriers of disease" (Sifferlin 2017). By the same token, the death, diagnosed as being due to rabies, of one man in Brazil who stepped on a bat, triggered widespread media attention with articles such as "Vampire bats terrorise Brazilian city as one man dies of rabies" (Beresford 2017) and "Vampire bats attack, feast on humans in Brazil" (Anonymous 2017b).…”

Bat Biology, Genomes, and the Bat1K Project: To Generate Chromosome-Level Genomes for All Living Bat Species

“…Again, over eons, bats have evolved to cope with these challenges, often leading to survival despite viral exposure (for a comprehensive list of viruses detected in bats, see 54). Epidemiological studies and field surveys suggest viruses circulate in wild bat populations (12,55) without causing the great morbidity or mortality observed as a result of viral spillovers into humans (Table 1) (14,56). Although the processes through which bats manage to clear viral infections remain poorly understood, possible explanations for the resilience of individual bats to these infections include not only heightened immune function but modulation of inflammation and mechanisms of repair (16).…”

“…High-quality bat genomes (e.g., including regulatory regions) from diverse species are needed to determine both how extensive these interactions between bats and viruses have been and what innate genetic mechanisms bats use to clear these viruses. Coupled with viral monitoring in the wild and viral genomics, bat genomic analyses have the potential to predict and manage future spillover events (56).…”