Ecological determinants of rabies virus dynamics in vampire bats and spillover to livestock.

The pathogen transmission dynamics in bat reservoirs underpin efforts to reduce risks to human health and enhance bat conservation, but are notoriously challenging to resolve. For vampire bat rabies, the geographical scale of enzootic cycles, whether environmental factors modulate baseline risk, and how within-host processes affect population-level dynamics remain unresolved. We studied patterns of rabies exposure using an 11-year, spatially replicated sero-survey of 3709 Peruvian vampire bats and co-occurring outbreaks in livestock. Seroprevalence was correlated among nearby sites but fluctuated asynchronously at larger distances. A generalized additive mixed model confirmed spatially compartmentalized transmission cycles, but no effects of bat demography or environmental context on seroprevalence. Among 427 recaptured bats, we observed long-term survival following rabies exposure and antibody waning, supporting hypotheses that immunological mechanisms influence viral maintenance. Finally, seroprevalence in bats was only weakly correlated with outbreaks in livestock, reinforcing the challenge of spillover prediction even with extensive data. Together our results suggest that rabies maintenance requires transmission among multiple, nearby bat colonies which may be facilitated by waning of protective immunity. However, the likelihood of incursions and dynamics of transmission within bat colonies appear largely independent of bat ecology. The implications of these results for spillover anticipation and controlling transmission at the source are discussed.

Diversification of mammalian deltaviruses by host shifting.

Hepatitis delta virus (HDV) is an unusual RNA agent that replicates using host machinery but exploits hepatitis B virus (HBV) to mobilize its spread within and between hosts. In doing so, HDV enhances the virulence of HBV. How this seemingly improbable hyperparasitic lifestyle emerged is unknown, but it underpins the likelihood that HDV and related deltaviruses may alter other host-virus interactions. Here, we show that deltaviruses diversify by transmitting between mammalian species. Among 96,695 RNA sequence datasets, deltaviruses infected bats, rodents, and an artiodactyl from the Americas but were absent from geographically overrepresented Old World representatives of each mammalian order, suggesting a relatively recent diversification within the Americas. Consistent with diversification by host shifting, both bat and rodent-infecting deltaviruses were paraphyletic, and coevolutionary modeling rejected cospeciation with mammalian hosts. In addition, a 2-y field study showed common vampire bats in Peru were infected by two divergent deltaviruses, indicating multiple introductions to a single host species. One vampire bat-associated deltavirus was detected in the saliva of up to 35% of individuals, formed phylogeographically compartmentalized clades, and infected a sympatric bat, illustrating horizontal transmission within and between species on ecological timescales. Consistent absence of HBV-like viruses in two deltavirus-infected bat species indicated acquisitions of novel viral associations during the divergence of bat and human-infecting deltaviruses. Our analyses support an American zoonotic origin of HDV and reveal prospects for future cross-species emergence of deltaviruses. Given their peculiar life history, deltavirus host shifts will have different constraints and disease outcomes compared to ordinary animal pathogens.

Detection of Trypanosoma cruzi in the saliva of diverse neotropical bats.

Trypanosoma cruzi is widely reported in bats, yet transmission routes remain unclear. We present evidence from metagenomic sequence data that T. cruzi occurs in the saliva of diverse Neotropical bats. Phylogenetic analyses demonstrated that the bat-associated T. cruzi sequences described here formed part of a bat-specific clade, suggesting an independent transmission cycle. Our results highlight the value in repurposing metagenomic data generated for viral discovery to reveal insights into the biology of other parasites. Evaluating whether the presence of T. cruzi in the saliva of two hematophagous bat species represents an ecological route for zoonotic transmission of Chagas disease is an interesting avenue for future research.

Defining New Pathways to Manage the Ongoing Emergence of Bat Rabies in Latin America.

Rabies transmitted by common vampire bats (Desmodus rotundus) has been known since the early 1900s but continues to expand geographically and in the range of species and environments affected. In this review, we present current knowledge of the epidemiology and management of rabies in D. rotundus and argue that it can be reasonably considered an emerging public health threat. We identify knowledge gaps related to the landscape determinants of the bat reservoir, reduction in bites on humans and livestock, and social barriers to prevention. We discuss how new technologies including autonomously-spreading vaccines and reproductive suppressants targeting bats might manage both rabies and undesirable growth of D. rotundus populations. Finally, we highlight widespread under-reporting of human and animal mortality and the scarcity of studies that quantify the efficacy of control measures such as bat culling. Collaborations between researchers and managers will be crucial to implement the next generation of rabies management in Latin America.

Fluorescent biomarkers demonstrate prospects for spreadable vaccines to control disease transmission in wild bats.

Vaccines that autonomously transfer among individuals have been proposed as a strategy to control infectious diseases within inaccessible wildlife populations. However, rates of vaccine spread and epidemiological efficacy in real-world systems remain elusive. Here, we investigate whether topical vaccines that transfer among individuals through social contacts can control vampire bat rabies-a medically and economically important zoonosis in Latin America. Field experiments in three Peruvian bat colonies, which used fluorescent biomarkers as a proxy for the bat-to-bat transfer and ingestion of an oral vaccine, revealed that vaccine transfer would increase population-level immunity up to 2.6 times beyond the same effort using conventional, non-spreadable vaccines. Mathematical models showed that observed levels of vaccine transfer would reduce the probability, size and duration of rabies outbreaks, even at low but realistically achievable levels of vaccine application. Models further predicted that existing vaccines provide substantial advantages over culling bats-the policy currently implemented in North, Central and South America. Linking field studies with biomarkers to mathematical models can inform how spreadable vaccines may combat pathogens of health and conservation concern before costly investments in vaccine design and testing.

Leukocyte Profiles Reflect Geographic Range Limits in a Widespread Neotropical Bat.

Quantifying how the environment shapes host immune defense is important for understanding which wild populations may be more susceptible or resistant to pathogens. Spatial variation in parasite risk, food and predator abundance, and abiotic conditions can each affect immunity, and these factors can also manifest at both local and biogeographic scales. Yet identifying predictors and the spatial scale of their effects is limited by the rarity of studies that measure immunity across many populations of broadly distributed species. We analyzed leukocyte profiles from 39 wild populations of the common vampire bat (Desmodus rotundus) across its wide geographic range throughout the Neotropics. White blood cell differentials varied spatially, with proportions of neutrophils and lymphocytes varying up to six-fold across sites. Leukocyte profiles were spatially autocorrelated at small and very large distances, suggesting that local environment and large-scale biogeographic factors influence cellular immunity. Generalized additive models showed that bat populations closer to the northern and southern limits of the species range had more neutrophils, monocytes, and basophils, but fewer lymphocytes and eosinophils, than bats sampled at the core of their distribution. Habitats with access to more livestock also showed similar patterns in leukocyte profiles, but large-scale patterns were partly confounded by time between capture and sampling across sites. Our findings suggest that populations at the edge of their range experience physiologically limiting conditions that predict higher chronic stress and greater investment in cellular innate immunity. High food abundance in livestock-dense habitats may exacerbate such conditions by increasing bat density or diet homogenization, although future spatially and temporally coordinated field studies with common protocols are needed to limit sampling artifacts. Systematically assessing immune function and response over space will elucidate how environmental conditions influence traits relevant to epidemiology and help predict disease risks with anthropogenic disturbance, land conversion, and climate change.

Livestock abundance predicts vampire bat demography, immune profiles and bacterial infection risk.

Human activities create novel food resources that can alter wildlife-pathogen interactions. If resources amplify or dampen, pathogen transmission probably depends on both host ecology and pathogen biology, but studies that measure responses to provisioning across both scales are rare. We tested these relationships with a 4-year study of 369 common vampire bats across 10 sites in Peru and Belize that differ in the abundance of livestock, an important anthropogenic food source. We quantified innate and adaptive immunity from bats and assessed infection with two common bacteria. We predicted that abundant livestock could reduce starvation and foraging effort, allowing for greater investments in immunity. Bats from high-livestock sites had higher microbicidal activity and proportions of neutrophils but lower immunoglobulin G and proportions of lymphocytes, suggesting more investment in innate relative to adaptive immunity and either greater chronic stress or pathogen exposure. This relationship was most pronounced in reproductive bats, which were also more common in high-livestock sites, suggesting feedbacks between demographic correlates of provisioning and immunity. Infection with both Bartonella and haemoplasmas were correlated with similar immune profiles, and both pathogens tended to be less prevalent in high-livestock sites, although effects were weaker for haemoplasmas. These differing responses to provisioning might therefore reflect distinct transmission processes. Predicting how provisioning alters host-pathogen interactions requires considering how both within-host processes and transmission modes respond to resource shifts.This article is part of the theme issue 'Anthropogenic resource subsidies and host-parasite dynamics in wildlife'.