Bats host a number of pathogens that cause severe disease and onward transmission in humans and domestic animals. Some of these pathogens, including henipaviruses and filoviruses, are considered a concern for future pandemics. There has been substantial effort to identify these viruses in bats. However, the reservoir hosts for Ebola virus are still unknown and henipaviruses are largely uncharacterized across their distribution. Identifying reservoir species is critical in understanding the viral ecology within these hosts and the conditions that lead to spillover. We collated surveillance data to identify taxonomic patterns in prevalence and seroprevalence and to assess sampling efforts across species. We systematically collected data on filovirus and henipavirus detections and used a machine-learning algorithm, phylofactorization, in order to search the bat phylogeny for cladistic patterns in filovirus and henipavirus infection, accounting for sampling efforts. Across sampled bat species, evidence for filovirus infection was widely dispersed across the sampled phylogeny. We found major gaps in filovirus sampling in bats, especially in Western Hemisphere species. Evidence for henipavirus infection was clustered within the Pteropodidae; however, no other clades have been as intensely sampled. The major predictor of filovirus and henipavirus exposure or infection was sampling effort. Based on these results, we recommend expanding surveillance for these pathogens across the bat phylogenetic tree.
more »
« less
Temporal and spatial limitations in global surveillance for bat filoviruses and henipaviruses
Sampling reservoir hosts over time and space is critical to detect epizootics, predict spillover and design interventions. However, because sampling is logistically difficult and expensive, researchers rarely perform spatio-temporal sampling of many reservoir hosts. Bats are reservoirs of many virulent zoonotic pathogens such as filoviruses and henipaviruses, yet the highly mobile nature of these animals has limited optimal sampling of bat populations. To quantify the frequency of temporal sampling and to characterize the geographical scope of bat virus research, we here collated data on filovirus and henipavirus prevalence and seroprevalence in wild bats. We used a phylogenetically controlled meta-analysis to next assess temporal and spatial variation in bat virus detection estimates. Our analysis shows that only one in four bat virus studies report data longitudinally, that sampling efforts cluster geographically (e.g. filovirus data are available across much of Africa and Asia but are absent from Latin America and Oceania), and that sampling designs and reporting practices may affect some viral detection estimates (e.g. filovirus seroprevalence). Within the limited number of longitudinal bat virus studies, we observed high heterogeneity in viral detection estimates that in turn reflected both spatial and temporal variation. This suggests that spatio-temporal sampling designs are important to understand how zoonotic viruses are maintained and spread within and across wild bat populations, which in turn could help predict and preempt risks of zoonotic viral spillover.
more »
« less
- Award ID(s):
- 1716698
- PAR ID:
- 10169883
- Date Published:
- Journal Name:
- Biology Letters
- Volume:
- 15
- Issue:
- 12
- ISSN:
- 1744-9561
- Page Range / eLocation ID:
- 20190423
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
Abstract The spatial organization of populations determines their pathogen dynamics. This is particularly important for communally roosting species, whose aggregations are often driven by the spatial structure of their environment.We develop a spatially explicit model for virus transmission within roosts of Australian tree‐dwelling bats (Pteropusspp.), parameterized to reflect Hendra virus. The spatial structure of roosts mirrors three study sites, and viral transmission between groups of bats in trees was modelled as a function of distance between roost trees. Using three levels of tree density to reflect anthropogenic changes in bat habitats, we investigate the potential effects of recent ecological shifts in Australia on the dynamics of zoonotic viruses in reservoir hosts.We show that simulated infection dynamics in spatially structured roosts differ from that of mean‐field models for equivalently sized populations, highlighting the importance of spatial structure in disease models of gregarious taxa. Under contrasting scenarios of flying‐fox roosting structures, sparse stand structures (with fewer trees but more bats per tree) generate higher probabilities of successful outbreaks, larger and faster epidemics, and shorter virus extinction times, compared to intermediate and dense stand structures with more trees but fewer bats per tree. These observations are consistent with the greater force of infection generated by structured populations with less numerous but larger infected groups, and may flag an increased risk of pathogen spillover from these increasingly abundant roost types.Outputs from our models contribute insights into the spread of viruses in structured animal populations, like communally roosting species, as well as specific insights into Hendra virus infection dynamics and spillover risk in a situation of changing host ecology. These insights will be relevant for modelling other zoonotic viruses in wildlife reservoir hosts in response to habitat modification and changing populations, including coronaviruses like SARS‐CoV‐2.more » « less
-
Habitat degradation can increase zoonotic disease risks by altering infection dynamics in wildlife and increasing wildlife–human interactions. Bats are an important taxonomic group to consider these effects, because they harbour many relevant zoonotic viruses and have species‐ and context‐dependent responses to degradation that could affect zoonotic virus dynamics. Yet our understanding of the associations between habitat degradation and bat virus prevalence and seroprevalence are limited to a small number of studies, which often differ in the bats or viruses sampled, the study region, and methodology. To develop a broad understanding of the associations between bat viruses and habitat degradation, we conducted an initial phylogenetic meta‐analysis that combines published prevalence and seroprevalence (‘(sero)prevalence') with remote‐sensing habitat degradation data. Our dataset includes 588 unique records of (sero)prevalence across 16 studies, 64 bat species, and five virus families. We quantified the overall strength and direction of the relationship between habitat degradation and bat virus outcomes and tested how this relationship is moderated by the time between habitat degradation and bat sampling and by ecological traits of bat hosts while controlling for phylogenetic non‐independence among bat species. We found no effect of degradation on prevalence overall, although a weak effect may exist when forest loss occurs the year prior to bat sampling. In contrast, we detected a negative but weak association between degradation and seroprevalence overall that was strengthened when forest loss occurred the year prior to bat sampling. No bat traits that we investigated interacted with habitat degradation to impact virus outcomes, suggesting observed trends are independent of these traits. Biases in our initial dataset highlight opportunities for future work; prevalence was highly zero‐inflated, and seroprevalence was dominated byDesmodus rotundusand rabies virus. These findings and subsequent analyses will improve our understanding of how global change affects host–pathogen dynamics.more » « less
-
Significance The clear need to mitigate zoonotic risk has fueled increased viral discovery in specific reservoir host taxa. We show that a combination of viral and reservoir traits can predict zoonotic virus virulence and transmissibility in humans, supporting the hypothesis that bats harbor exceptionally virulent zoonoses. However, pandemic prevention requires thinking beyond zoonotic capacity, virulence, and transmissibility to consider collective “burden” on human health. For this, viral discovery targeting specific reservoirs may be inefficient as death burden correlates with viral, not reservoir, traits, and depends on context-specific epidemiological dynamics across and beyond the human–animal interface. These findings suggest that longitudinal studies of viral dynamics in reservoir and spillover host populations may offer the most effective strategy for mitigating zoonotic risk.more » « less
-
Abstract The ecological conditions experienced by wildlife reservoirs affect infection dynamics and thus the distribution of pathogen excreted into the environment. This spatial and temporal distribution of shed pathogen has been hypothesised to shape risks of zoonotic spillover. However, few systems have data on both long‐term ecological conditions and pathogen excretion to advance mechanistic understanding and test environmental drivers of spillover risk. We here analyse three years of Hendra virus data from nine Australian flying fox roosts with covariates derived from long‐term studies of bat ecology. We show that the magnitude of winter pulses of viral excretion, previously considered idiosyncratic, are most pronounced after recent food shortages and in bat populations displaced to novel habitats. We further show that cumulative pathogen excretion over time is shaped by bat ecology and positively predicts spillover frequency. Our work emphasises the role of reservoir host ecology in shaping pathogen excretion and provides a new approach to estimate spillover risk.more » « less
An official website of the United States government

