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

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-...

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Main Authors: Samantha Aguillon, Magali Turpin, Gildas Le Minter, Camille Lebarbenchon, Axel O G Hoarau, Céline Toty, Avril Duchet, Léa Joffrin, Riana V Ramanantsalama, Pablo Tortosa, Patrick Mavingui, Muriel Dietrich
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2025-07-01
Series:PLoS Pathogens
Online Access:https://doi.org/10.1371/journal.ppat.1013334
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author Samantha Aguillon
Magali Turpin
Gildas Le Minter
Camille Lebarbenchon
Axel O G Hoarau
Céline Toty
Avril Duchet
Léa Joffrin
Riana V Ramanantsalama
Pablo Tortosa
Patrick Mavingui
Muriel Dietrich
author_facet Samantha Aguillon
Magali Turpin
Gildas Le Minter
Camille Lebarbenchon
Axel O G Hoarau
Céline Toty
Avril Duchet
Léa Joffrin
Riana V Ramanantsalama
Pablo Tortosa
Patrick Mavingui
Muriel Dietrich
author_sort Samantha Aguillon
collection DOAJ
description 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. Reproductively-active individuals (both during the pregnancy and mating) were associated with increased PMV and LEPTO shedding, which could 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.
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spelling doaj-art-ffe78da466404d5b94915da5954a61fe2025-08-20T03:12:32ZengPublic Library of Science (PLoS)PLoS Pathogens1553-73661553-73742025-07-01217e101333410.1371/journal.ppat.1013334Role of individual and population heterogeneity in shaping dynamics of multi-pathogen shedding in an island endemic bat.Samantha AguillonMagali TurpinGildas Le MinterCamille LebarbenchonAxel O G HoarauCéline TotyAvril DuchetLéa JoffrinRiana V RamanantsalamaPablo TortosaPatrick MavinguiMuriel DietrichUnderstanding 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. Reproductively-active individuals (both during the pregnancy and mating) were associated with increased PMV and LEPTO shedding, which could 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.https://doi.org/10.1371/journal.ppat.1013334
spellingShingle Samantha Aguillon
Magali Turpin
Gildas Le Minter
Camille Lebarbenchon
Axel O G Hoarau
Céline Toty
Avril Duchet
Léa Joffrin
Riana V Ramanantsalama
Pablo Tortosa
Patrick Mavingui
Muriel Dietrich
Role of individual and population heterogeneity in shaping dynamics of multi-pathogen shedding in an island endemic bat.
PLoS Pathogens
title Role of individual and population heterogeneity in shaping dynamics of multi-pathogen shedding in an island endemic bat.
title_full Role of individual and population heterogeneity in shaping dynamics of multi-pathogen shedding in an island endemic bat.
title_fullStr Role of individual and population heterogeneity in shaping dynamics of multi-pathogen shedding in an island endemic bat.
title_full_unstemmed Role of individual and population heterogeneity in shaping dynamics of multi-pathogen shedding in an island endemic bat.
title_short Role of individual and population heterogeneity in shaping dynamics of multi-pathogen shedding in an island endemic bat.
title_sort role of individual and population heterogeneity in shaping dynamics of multi pathogen shedding in an island endemic bat
url https://doi.org/10.1371/journal.ppat.1013334
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