Phylodynamics reveals extinction–recolonization dynamics underpin apparently endemic vampire bat rabies in Costa Rica

Abstract

Variation in disease incidence in wildlife is often assumed to reflect environmental or demographic changes acting on an endemic pathogen. However, apparent endemicity might instead arise from spatial processes that are challenging to identify from traditional data sources including time series and field studies. Here, we analysed longitudinal sequence data collected from rabies virus outbreaks over 14 years in Costa Rica, a Central American country that has recorded continuous vampire bat-transmitted rabies outbreaks in humans and livestock since 1985. We identified five phylogenetically distinct lineages which shared most recent common ancestors with viruses from North and South America. Bayesian phylogeographic reconstructions supported bidirectional viral dispersals involving countries to the north and south of Costa Rica at different time points. Within Costa Rica, viruses showed little contemporaneous spatial overlap and no lineage was detected across all years of surveillance. Statistical models suggested that lineage disappearances were more likely to be explained by viral extinctions than undetected viral circulation. Our results highlight the importance of international viral dispersal for shaping the burden of rabies in Costa Rica, suggest a Central American corridor of rabies virus invasions between continents, and show that apparent disease endemicity may arise through recurrent pathogen extinctions and reinvasions which can be readily detected in relatively small datasets by joining phylodynamic and modelling approaches.

Temporal patterns of vampire bat rabies and host connectivity in Belize

“…More broadly, however, our results suggest that the degree of connectivity found here likely enables virus persistence through inter-site contacts but is not sufficient to synchronize infection dynamics across sites (Blackwood et al, 2013). In further support of this idea, the inverse relationship in seroprevalence between our Belize sites (<10 km) is consistent with prior rates of RABV dispersal in vampire bats of 9-17 km per year (Benavides et al, 2016;Streicker et al, 2019).…”

“…Future phylogenetic analyses of RABV isolates from across Belize as well as nearby countries could help differentiate hypotheses of a persistent transmission cycle in Belize against the potential role of viral invasions and spatial spread (Andrés Velasco-Villa et al, 2006;Biek et al, 2007;Streicker et al, 2019). Although our serological data are consistent with endemic maintenance of RABV in local vampire bat populations, livestock rabies outbreaks are known to show epidemic dynamics, including in Belize, where outbreaks were not reported in livestock in 2014 and 2015 (World Organization for Animal Health, 2016).…”

“…Spatiotemporal studies in Argentina and Peru showed that vampire bat RABV moves in traveling waves, likely driven by male-biased dispersal (Delpietro et al, 1972;Benavides et al, 2016;Streicker et al, 2016). Whether similar dynamics occur among vampire bats across Central America and the Caribbean remains a pressing and open question (Andres Velasco-Villa et al, 2017;Seetahal et al, 2018;Streicker et al, 2019).…”

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

“…Although undersampling of active infections cannot be discarded, one likely explanation for this apparent discrepancy is that the virus undergoes localized epizootics, during which prevalence is substantially elevated, followed by local extinctions. Indeed, such invasion-extinction dynamics are readily observed in the complex spatiotemporal patterns of spillover to livestock, including epizootic waves, where DRRV spreads across the landscape via transmission between neighboring bat colonies at a relatively constant speed [10] and metapopulation persistence, where asynchronous presence of the virus in bat colonies prevents extinction at a larger spatial scale, and localized lineage replacements [33,40,41]. Extended incubation periods can occur but are a less plausible explanation for localized disappearances of DRRV strains over multiple years suggested by passive surveillance of livestock [40].…”

Dynamics of Rabies Epidemics in Vampire Bats

“…Bat population was monitored for rabies by fluorescent antibody testing and simplified fluorescent inhibition microtesting by Almeida et al [14], who indicated an increase in rabies virus circulation among bats and risk of a rabies outbreak. Streicker et al [15] highlighted the importance of international viral dispersal for shaping the burden of rabies in Costa Rica and suggested a Central American corridor of rabies virus invasions between continents. Although researchers have carried out a lot of studies on bat rabies from different aspects, there are relatively few studies on relevant mathematical analysis from the perspective of the dynamic model.…”