Abstract Pathogen spillover from wildlife to humans or domestic animals requires a series of conditions to align with space and time. Comparing these conditions between times and locations where spillover does and does not occur presents opportunities to understand the factors that shape spillover risk. Bovine rabies transmitted by vampire bats was first confirmed in 1911 and has since been detected across the distribution of vampire bats. However, Uruguay is an exception. Uruguay was free of bovine rabies until 2007, despite high-cattle densities, the presence of vampire bats and a strong surveillance system. To explore why Uruguay was free of bovine rabies until recently, we review the historic literature and reconstruct the conditions that would allow rabies invasion into Uruguay. We used available historical records on the abundance of livestock and wildlife, the vampire bat distribution and occurrence of rabies outbreaks, as well as environmental modifications, to propose four alternative hypotheses to explain rabies virus emergence and spillover: bat movement, viral invasion, surveillance failure and environmental changes. While future statistical modelling efforts will be required to disentangle these hypotheses, we here show how a detailed historical analysis can be used to generate testable predictions for the conditions leading to pathogen spillover.
more »
« less
Epidemiology and biology of a herpesvirus in rabies endemic vampire bat populations
Rabies is a viral zoonosis transmitted by vampire bats across Latin America. Substantial public health and agricultural burdens remain, despite decades of bats culls and livestock vaccinations. Virally vectored vaccines that spread autonomously through bat populations are a theoretically appealing solution to managing rabies in its reservoir host. We investigate the biological and epidemiological suitability of a vampire bat betaherpesvirus (DrBHV) to act as a vaccine vector. In 25 sites across Peru with serological and/or molecular evidence of rabies circulation, DrBHV infects 80–100% of bats, suggesting potential for high population-level vaccine coverage. Phylogenetic analysis reveals host specificity within neotropical bats, limiting risks to non-target species. Finally, deep sequencing illustrates DrBHV super-infections in individual bats, implying that DrBHV-vectored vaccines might invade despite the highly prevalent wild-type virus. These results indicate DrBHV as a promising candidate vector for a transmissible rabies vaccine, and provide a framework to discover and evaluate candidate viral vectors for vaccines against bat-borne zoonoses.
more » « less- NSF-PAR ID:
- 10360774
- Publisher / Repository:
- Nature Publishing Group
- Date Published:
- Journal Name:
- Nature Communications
- Volume:
- 11
- Issue:
- 1
- ISSN:
- 2041-1723
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
Rabies virus (RABV) transmitted by the common vampire bat ( Desmodus rotundus ) poses a threat to agricultural development and public health throughout the Neotropics. The ecology and evolution of rabies host–pathogen dynamics are influenced by two infection-induced behavioural changes. RABV-infected hosts often exhibit increased aggression which facilitates transmission, and rabies also leads to reduced activity and paralysis prior to death. Although several studies document rabies-induced behavioural changes in rodents and other dead-end hosts, surprisingly few studies have measured these changes in vampire bats, the key natural reservoir throughout Latin America. Taking advantage of an experiment designed to test an oral rabies vaccine in captive male vampire bats, we quantify for the first time, to our knowledge, how rabies affects allogrooming and aggressive behaviours in this species. Compared to non-rabid vampire bats, rabid individuals reduced their allogrooming prior to death, but we did not detect increases in aggression among bats. To put our results in context, we review what is known and what remains unclear about behavioural changes of rabid vampire bats (resumen en español, electronic supplementary material, S1).more » « less
-
more » « less
Abstract Viruses infect all forms of life and play critical roles as agents of disease, drivers of biochemical cycles and sources of genetic diversity for their hosts. Our understanding of viral diversity derives primarily from comparisons among host species, precluding insight into how intraspecific variation in host ecology affects viral communities or how predictable viral communities are across populations. Here we test spatial, demographic and environmental hypotheses explaining viral richness and community composition across populations of common vampire bats, which occur in diverse habitats of North, Central and South America. We demonstrate marked variation in viral communities that was not consistently predicted by a null model of declining community similarity with increasing spatial or genetic distances separating populations. We also find no evidence that larger bat colonies host greater viral diversity. Instead, viral diversity follows an elevational gradient, is enriched by juvenile‐biased age structure, and declines with local anthropogenic food resources as measured by livestock density. Our results establish the value of linking the modern influx of metagenomic sequence data with comparative ecology, reveal that snapshot views of viral diversity are unlikely to be representative at the species level, and affirm existing ecological theories that link host ecology not only to single pathogen dynamics but also to viral communities.
-
more » « less
Abstract Skin is the largest mammalian organ and the first defensive barrier against the external environment. The skin and fur of mammals can host a wide variety of ectoparasites, many of which are phylogenetically diverse, specialized, and specifically adapted to their hosts. Among hematophagous dipteran parasites, volatile organic compounds (VOCs) are known to serve as important attractants, leading parasites to compatible sources of blood meals. VOCs have been hypothesized to be mediated by host‐associated bacteria, which may thereby indirectly influence parasitism. Host‐associated bacteria may also influence parasitism directly, as has been observed in interactions between animal gut microbiota and malarial parasites. Hypotheses relating bacterial symbionts and eukaryotic parasitism have rarely been tested among humans and domestic animals, and to our knowledge have not been tested in wild vertebrates. In this study, we used Afrotropical bats, hematophagous ectoparasitic bat flies, and haemosporidian (malarial) parasites vectored by bat flies as a model to test the hypothesis that the vertebrate host microbiome is linked to parasitism in a wild system. We identified significant correlations between bacterial community composition of the skin and dipteran ectoparasite prevalence across four major bat lineages, as well as striking differences in skin microbial network characteristics between ectoparasitized and nonectoparasitized bats. We also identified links between the oral microbiome and presence of malarial parasites among miniopterid bats. Our results support the hypothesis that microbial symbionts may serve as indirect mediators of parasitism among eukaryotic hosts and parasites.
-
more » « less
Abstract Equitable global access to vaccines requires overcoming challenges associated with complex immunization schedules and their associated economic burdens that hinder delivery in under‐resourced environments. The rabies vaccine, for example, requires multiple immunizations for effective protection and each dose is cost prohibitive, and therefore inaccessibility disproportionately impacts low‐ and middle‐income countries. In this work, an injectable hydrogel depot technology for sustained delivery of commercial inactivated rabies virus vaccines is developed. In a mouse model, it is shown that a single immunization of a hydrogel‐based rabies vaccine elicited comparable antibody titers to a standard prime‐boost bolus regimen of a commercial rabies vaccine, despite these hydrogel vaccines comprising only half of the total dose delivered in the bolus control. Moreover, these hydrogel‐based vaccines elicited similar antigen‐specific T‐cell responses and neutralizing antibody responses compared to the bolus vaccine. Notably, it is demonstrated that while the addition of a potent clinical Toll‐like receptor 4 (TLR4) agonist adjuvant to the gels slightly improved binding antibody responses, inclusion of this adjuvant to the inactivated virion vaccine is detrimental to neutralizing responses. Taken together, these results suggest that these hydrogels can enable an effective regimen compression and dose‐sparing strategy for improving global access to vaccines.
