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bioRxiv · 10.1101/2024.06.25.600581

Role of individual and population heterogeneity in shaping dynamics of multi-pathogen excretion in an island endemic bat

Aguillon, S.·Turpin, M.·Le Minter, G.·Lebarbenchon, C.·Hoarau, A. O. G.·Toty, C.·Duchet, A.·Joffrin, L.·Ramanantsalama, R. V.·Tortosa, P.·Mavingui, P.·Dietrich, M.
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Abstract

Understanding processes driving pathogen transmission in bats is critical to prevent spillovers and emergence events. Although substantial research has addressed this topic, few studies have directly examined shedding dynamics (as opposed to serological studies) and co-infection patterns using fine-scale spatio-temporal datasets. Here, based on the monitoring of 5,714 Reunion free-tailed bats (Mormopterus francoismoutoui) in 17 roosts over 24 months, we studied the co-shedding dynamics of paramyxoviruses (PMV) and Leptospira bacteria (LEPTO) in urine, and herpesviruses (HSV) in saliva. We evidenced all year long shedding with high prevalence of all three infectious agents (37% - 87%), as well as an exceptionally high level of co-shedding (59%), with both positive and negative interactions between infectious agents. Shedding patterns displayed temporal synchrony among roosts, with a peak during summer months, but were not influenced by roost size. Repeated shedding in recaptured bats supports within-host persistence, though underlying mechanisms remain to be identified. Our results also showed rapid HSV infection of juveniles (< 6 months), and suggest longer protection of juveniles by maternal antibodies for PMV and LEPTO. Reproductive individuals (both during the pregnancy and mating) were associated to increased PMV and LEPTO shedding, which can result from tradeoffs between reproduction and infection in both sexes, and/or an age-related bias with the progressive infection of older juveniles during reproductive periods. This study highlights the significance of persistent shedding of multiple pathogens, including bacteria, and their intricate interactions within bat populations. Understanding how human-driven ecological changes may disrupt within-host processes and influence pathogen shedding in bats will help assessing the risk of pathogen spillover from bats to other species, including humans. Author summaryUnderstanding risks of bat-borne pathogen spillover is challenging because of the difficulty in studying shedding dynamics in wild bat populations. Here, we used an original island-endemic bat species to build up a fine-scale spatio-temporal shedding analysis of two viruses (paramyxoviruses and herpesviruses) and a bacterium (Leptospira) at both population- (roost) and individual- (through recaptured bats) levels. Shedding patterns are driven by the age of bats and associated to the reproductive periods in both females and males. Results also suggest that persistence, as well as interactions between infectious agents, are important within-host processes that contribute to the transmission of infections in bat populations. More research is essential to understand how human activities may influence these co-shedding patterns and the risk of cross- species transmission.

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Aguillon, S., Turpin, M., Le Minter, G., Lebarbenchon, C., Hoarau, A. O. G., Toty, C., Duchet, A., Joffrin, L., Ramanantsalama, R. V., Tortosa, P., Mavingui, P., Dietrich, M.. 2024-06-29. Role of individual and population heterogeneity in shaping dynamics of multi-pathogen excretion in an island endemic bat. https://doi.org/10.1101/2024.06.25.600581

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