Host immunity, nutrition and coinfection alter longitudinal infection patterns of schistosomes in a free ranging African buffalo population

Schistosomes are trematode parasites of global importance, causing infections in millions of people, livestock, and wildlife. Most studies on schistosomiasis, involve human subjects; as such, there is a paucity of longitudinal studies investigating parasite dynamics in the absence of intervention. As a consequence, despite decades of research on schistosomiasis, our understanding of its ecology in natural host populations is centered around how environmental exposure and acquired immunity influence acquisition of parasites, while very little is known about the influence of host physiology, coinfection and clearance in the absence of drug treatment. We used a 4-year study in free-ranging African buffalo to investigate natural schistosome dynamics. We asked (i) what are the spatial and temporal patterns of schistosome infections; (ii) how do parasite burdens vary over time within individual hosts; and (iii) what host factors (immunological, physiological, co-infection) and environmental factors (season, location) explain patterns of schistosome acquisition and loss in buffalo? Schistosome infections were common among buffalo. Microgeographic structure explained some variation in parasite burdens among hosts, indicating transmission hotspots. Overall, parasite burdens ratcheted up over time; however, gains in schistosome abundance in the dry season were partially offset by losses in the wet season, with some hosts demonstrating complete clearance of infection. Variation among buffalo in schistosome loss was associated with immunologic and nutritional factors, as well as co-infection by the gastrointestinal helminth Cooperia fuelleborni. Our results demonstrate that schistosome infections are surprisingly dynamic in a free-living mammalian host population, and point to a role for host factors in driving variation in parasite clearance, but not parasite acquisition which is driven by seasonal changes and spatial habitat utilization. Our study illustrates the power of longitudinal studies for discovering mechanisms underlying parasite dynamics in individual animals and populations.

血吸虫（Schistosomes）是一类具有全球重要性的吸虫类寄生虫，可感染数百万人类、家畜与野生动物。目前绝大多数血吸虫病（schistosomiasis）相关研究以人类为研究对象，因此缺乏在无干预条件下探究寄生虫动态的纵向研究。尽管针对血吸虫病的研究已开展数十年，我们对其自然宿主种群中血吸虫病生态学的认知，仍主要聚焦于环境暴露与获得性免疫如何影响寄生虫感染的建立，而对宿主生理、共感染以及未接受药物治疗情况下的寄生虫清除机制的了解却极为匮乏。
本研究依托一项针对野生非洲水牛的为期4年的队列研究，探究自然状态下的血吸虫动态。我们提出三个核心研究问题：（i）血吸虫感染存在怎样的时空分布模式？（ii）单个宿主体内的寄生虫负荷随时间如何变化？（iii）哪些宿主因素（免疫、生理、共感染）与环境因素（季节、采样地点）能够解释水牛体内血吸虫感染的建立与清除模式？
研究结果显示，血吸虫感染在水牛种群中十分普遍。微地理结构可解释部分宿主间的寄生虫负荷差异，提示存在血吸虫传播热点区域。总体而言，寄生虫负荷随时间推移逐步升高；但旱季寄生虫丰度的增加会被雨季的寄生虫丢失部分抵消，部分宿主甚至可实现感染的完全清除。水牛种群中寄生虫清除率的差异与免疫、营养状况以及胃肠道福氏库柏线虫（Cooperia fuelleborni）的共感染密切相关。
本研究结果表明，在自由生活的哺乳动物宿主种群中，血吸虫感染的动态变化远超此前预期，且宿主因素可影响寄生虫的清除过程，但无法解释寄生虫感染的建立——后者主要受季节变化与宿主空间生境利用模式驱动。本研究也彰显了纵向研究在揭示个体动物与种群层面寄生虫动态背后机制方面的重要价值。