Effects of culling vampire bats on the spatial spread and spillover of rabies virus.

Controlling pathogen circulation in wildlife reservoirs is notoriously challenging. In Latin America, vampire bats have been culled for decades in hopes of mitigating lethal rabies infections in humans and livestock. Whether culls reduce or exacerbate rabies transmission remains controversial. Using Bayesian state-space models, we show that a 2-year, spatially extensive bat cull in an area of exceptional rabies incidence in Peru failed to reduce spillover to livestock, despite reducing bat population density. Viral whole genome sequencing and phylogeographic analyses further demonstrated that culling before virus arrival slowed viral spatial spread, but reactive culling accelerated spread, suggesting that culling-induced changes in bat dispersal promoted viral invasions. Our findings question the core assumptions of density-dependent transmission and localized viral maintenance that underlie culling bats as a rabies prevention strategy and provide an epidemiological and evolutionary framework to understand the outcomes of interventions in complex wildlife disease systems.

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.

Host-pathogen evolutionary signatures reveal dynamics and future invasions of vampire bat rabies.

Anticipating how epidemics will spread across landscapes requires understanding host dispersal events that are notoriously difficult to measure. Here, we contrast host and virus genetic signatures to resolve the spatiotemporal dynamics underlying geographic expansions of vampire bat rabies virus (VBRV) in Peru. Phylogenetic analysis revealed recent viral spread between populations that, according to extreme geographic structure in maternally inherited host mitochondrial DNA, appeared completely isolated. In contrast, greater population connectivity in biparentally inherited nuclear microsatellites explained the historical limits of invasions, suggesting that dispersing male bats spread VBRV between genetically isolated female populations. Host nuclear DNA further indicated unanticipated gene flow through the Andes mountains connecting the VBRV-free Pacific coast to the VBRV-endemic Amazon rainforest. By combining Bayesian phylogeography with landscape resistance models, we projected invasion routes through northern Peru that were validated by real-time livestock rabies mortality data. The first outbreaks of VBRV on the Pacific coast of South America could occur by June 2020, which would have serious implications for agriculture, wildlife conservation, and human health. Our results show that combining host and pathogen genetic data can identify sex biases in pathogen spatial spread, which may be a widespread but underappreciated phenomenon, and demonstrate that genetic forecasting can aid preparedness for impending viral invasions.