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个体和种群异质性在塑造岛屿特有蝙蝠多种病原体脱落动态中的作用。

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

作者信息

Aguillon Samantha, Turpin Magali, Le Minter Gildas, Lebarbenchon Camille, Hoarau Axel O G, Toty Céline, Duchet Avril, Joffrin Léa, Ramanantsalama Riana V, Tortosa Pablo, Mavingui Patrick, Dietrich Muriel

机构信息

UMR PIMIT (Processus Infectieux en Milieu Insulaire Tropical), Université de la Réunion/ INSERM1187/ CNRS9192/ IRD249, Sainte-Clotilde, Reunion Island.

出版信息

PLoS Pathog. 2025 Jul 11;21(7):e1013334. doi: 10.1371/journal.ppat.1013334. eCollection 2025 Jul.

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. 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.

摘要

了解驱动蝙蝠病原体传播的过程对于预防溢出和新发事件至关重要。尽管已有大量研究涉及该主题,但很少有研究使用精细尺度的时空数据集直接检查脱落动态(与血清学研究相对)和共感染模式。在此,基于对17个栖息地的5714只留尼汪游离尾蝠(Mormopterus francoismoutoui)进行的24个月监测,我们研究了副粘病毒(PMV)和钩端螺旋体细菌(LEPTO)在尿液中的共脱落动态,以及疱疹病毒(HSV)在唾液中的共脱落动态。我们证明了全年所有三种传染原的高流行率(37% - 87%)下的脱落情况,以及异常高的共脱落水平(59%),传染原之间存在正、负相互作用。脱落模式在栖息地之间表现出时间同步性,在夏季月份达到峰值,但不受栖息地大小的影响。重新捕获的蝙蝠中的反复脱落支持了宿主体内的持续性,尽管潜在机制仍有待确定。我们的结果还显示幼年蝙蝠(<6个月)快速感染HSV,并表明母体抗体对PMV和LEPTO对幼年蝙蝠的保护时间更长。繁殖活跃个体(怀孕和交配期间)与PMV和LEPTO脱落增加有关,这可能是由于两性在繁殖和感染之间的权衡,和/或与年龄相关的偏差,即繁殖期年长幼蝠逐渐感染。这项研究强调了多种病原体(包括细菌)持续脱落及其在蝙蝠种群中复杂相互作用的重要性。了解人类驱动的生态变化如何破坏宿主体内过程并影响蝙蝠病原体脱落,将有助于评估病原体从蝙蝠溢出到其他物种(包括人类)的风险。

https://cdn.ncbi.nlm.nih.gov/pmc/blobs/5066/12273948/7009238d222f/ppat.1013334.g001.jpg

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