Ecological conditions predict the intensity of Hendra virus excretion over space and time from bat reservoir hosts

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.

Host–Pathogen Interactions Influencing Zoonotic Spillover Potential and Transmission in Humans

“…Climate anomalies (in terms of temperature or rainfall patterns for example) and climate change more generally likely drive the emergence and spillover opportunities of bat viruses by altering numerous aspects of bat physiology and ecology (foraging, stress induced by climate variability and related immune changes or migrations, etc.) [ 275 , 279 ]. In particular, food shortage and the altered body condition of bats are associated with decreased immunocompetence and HeV seroprevalence [ 280 , 281 ].…”

“…In particular, food shortage and the altered body condition of bats are associated with decreased immunocompetence and HeV seroprevalence [ 280 , 281 ]. Overall, the ecological conditions experienced by wildlife reservoirs are thus key to predicting and shaping spillover occurrence and intensity [ 279 ].…”

Coupling field and laboratory studies of immunity and infection in zoonotic hosts

“… 3 Thus, characterising how zoonotic pathogens persist in wildlife and identifying the conditions that shape the prevalence of infection and viral shedding over space and time is essential for predicting where and when spillover is likely to occur. 4 Immunology has a key role in deciphering these infection dynamics because the immune response dictates susceptibility, tolerance of infection, and pathogen shedding. Identifying the within-host processes governing infection dynamics in wildlife is crucial for forecasting the spatial and temporal distribution of infectious hosts.…”

“… 7 Analyses of Australian flying foxes also suggest nutritional stress as a driver of bat–virus interactions, with pulses of Hendra virus shedding occurring in winter after food shortages, especially in urban habitats. 4 More broadly, field studies have suggested crucial roles for both intrinsic (eg, reproduction and migration) and extrinsic (eg, food scarcity and land conversion) stressors on shaping bat immunity and within-host dynamics of viral infection. 7 …”

“…By describing patterns in reservoir host infection prevalence, seroprevalence, and immune measures, field studies can first suggest plausible within-host mechanisms of pathogen circulation 5 , 9 and identify probable intrinsic or extrinsic stressors that facilitate susceptibility to infection, pathogen replication, and shedding. 4 , 9 These data-driven hypotheses can then be experimentally interrogated through mechanistic molecular investigations, 10 , 11 given that appropriate in-vitro resources are available (ie, matching bat species and viruses to those in field studies). For example, stressors of a particular intensity could be mimicked at the cellular level by challenging physiologically relevant in-vitro models with surrogate stimulants and cortisols (eg, modifying dose and duration), assessing whether innate immune changes align or depart from differential expression or abundance patterns observed in field studies, and how such changes affect viral susceptibility and replication.…”