Department of Ecology & Evolutionary Biology, Princeton University, Princeton, New Jersey.
Virology Unit, Institut Pasteur de Madagascar, Antananarivo, Madagascar.
J Anim Ecol. 2019 Jul;88(7):1001-1016. doi: 10.1111/1365-2656.12985. Epub 2019 Apr 15.
Bats are reservoirs for emerging human pathogens, including Hendra and Nipah henipaviruses and Ebola and Marburg filoviruses. These viruses demonstrate predictable patterns in seasonality and age structure across multiple systems; previous work suggests that they may circulate in Madagascar's endemic fruit bats, which are widely consumed as human food. We aimed to (a) document the extent of henipa- and filovirus exposure among Malagasy fruit bats, (b) explore seasonality in seroprevalence and serostatus in these bat populations and (c) compare mechanistic hypotheses for possible transmission dynamics underlying these data. To this end, we amassed and analysed a unique dataset documenting longitudinal serological henipa- and filovirus dynamics in three Madagascar fruit bat species. We uncovered serological evidence of exposure to Hendra-/Nipah-related henipaviruses in Eidolon dupreanum, Pteropus rufus and Rousettus madagascariensis, to Cedar-related henipaviruses in E. dupreanum and R. madagascariensis and to Ebola-related filoviruses in P. rufus and R. madagascariensis. We demonstrated significant seasonality in population-level seroprevalence and individual serostatus for multiple viruses across these species, linked to the female reproductive calendar. An age-structured subset of the data highlighted evidence of waning maternal antibodies in neonates, increasing seroprevalence in young and decreasing seroprevalence late in life. Comparison of mechanistic epidemiological models fit to these data offered support for transmission hypotheses permitting waning antibodies but retained immunity in adult-age bats. Our findings suggest that bats may seasonally modulate mechanisms of pathogen control, with consequences for population-level transmission. Additionally, we narrow the field of candidate transmission hypotheses by which bats are presumed to host and transmit potentially zoonotic viruses globally.
蝙蝠是新兴人类病原体的宿主,包括亨德拉和尼帕亨尼帕病毒以及埃博拉和马尔堡丝状病毒。这些病毒在多个系统中的季节性和年龄结构上表现出可预测的模式;以前的工作表明,它们可能在马达加斯加的地方性果蝠中循环,这些果蝠被广泛作为人类食物食用。我们的目的是:(a) 记录马达加斯加果蝠中亨尼帕和丝状病毒暴露的程度,(b) 探索这些蝙蝠种群中血清阳性率和血清状态的季节性,以及 (c) 比较可能导致这些数据的潜在传播动态的机制假说。为此,我们收集和分析了一个独特的数据集,记录了三种马达加斯加果蝠物种中亨尼帕和丝状病毒的纵向血清学动态。我们发现了 Eidolon dupreanum、Pteropus rufus 和 Rousettus madagascariensis 中亨德拉/尼帕相关亨尼帕病毒、E. dupreanum 和 R. madagascariensis 中 Cedar 相关亨尼帕病毒以及 P. rufus 和 R. madagascariensis 中埃博拉相关丝状病毒暴露的血清学证据。我们证明了这些物种中多种病毒的群体血清阳性率和个体血清状态存在显著的季节性,与雌性生殖周期有关。对数据的年龄结构子集的分析表明,在新生儿中存在母体抗体减弱的证据,在幼体中血清阳性率增加,而在老年中血清阳性率降低。对拟合这些数据的机制流行病学模型的比较为允许抗体减弱但在成年蝙蝠中保留免疫力的传播假说提供了支持。我们的研究结果表明,蝙蝠可能会季节性地调节病原体控制机制,从而对种群水平的传播产生影响。此外,我们通过对蝙蝠宿主和传播全球潜在人畜共患病病毒的假定传播假说进行了筛选,缩小了候选传播假说的范围。