Long-term prevalence data reveals spillover dynamics in a multi-host (Artemia), multi-parasite (Microsporidia) community

In the study of multi-host parasites, it is often found that host species contribute asymmetrically to parasite transmission. Yet in natural populations, identifying which hosts contribute to parasite transmission and maintenance is a recurring challenge. Here, we approach this issue by taking advantage of natural variation in the composition of a host community. We studied the brine shrimps Artemia franciscana and Artemia parthenogenetica and their microsporidian parasites Anostracospora rigaudi and Enterocytospora artemiae. Previous laboratory experiments had shown that each host can transmit both parasites, but could not predict their actual contributions to the parasites’ maintenance in the field. To resolve this, we gathered long-term prevalence data from a metacommunity of these species. Metacommunity patches could contain either or both of the Artemia host species, so that the presence of the hosts could be linked directly to the persistence of the parasites. First, we show that the microsporidian A. rigaudi is a spillover parasite: it was unable to persist in the absence of its maintenance host A. parthenogenetica. This result was particularly striking, as A. rigaudi displayed both high prevalence (in the field) and high infectivity (when tested in the laboratory) in both hosts. Moreover, the seasonal presence of A. parthenogenetica imposed seasonality on the rate of spillover, causing cyclical pseudo-endemics in the spillover host A. franciscana. Second, while our prevalence data was sufficient to identify E. artemiae as either a spillover or a facultative multi-host parasite, we could not distinguish between the two possibilities. This study supports the importance of studying the community context of multi-host parasites, and demonstrates that in appropriate multi-host systems, sampling across a range of conditions and host communities can lead to clear conclusions about the drivers of parasite persistence.

在多宿主寄生虫（multi-host parasites）研究中，人们常发现宿主物种对寄生虫传播的贡献存在不对称性。然而在自然种群中，明确哪些宿主参与寄生虫的传播与维持始终是一项反复出现的难题。本研究借助宿主群落组成的自然变异来解决这一问题。我们以卤虫属（Artemia）的两个物种——旧金山卤虫（Artemia franciscana）与孤雌生殖卤虫（Artemia parthenogenetica），以及它们的两种微孢子虫寄生虫（microsporidian parasites）：里加额虫藻孢虫（Anostracospora rigaudi）和肠孢虫（Enterocytospora artemiae）为研究对象。既往实验室研究已证实，每种宿主均可传播这两种寄生虫，但无法预测它们在野外实际对寄生虫维持的贡献度。为解决这一问题，我们从这些物种的集合群落（metacommunity）中收集了长期感染率（prevalence）数据。集合群落斑块可仅包含其中一种卤虫宿主，或同时包含两种，因此宿主的存在与否可直接与寄生虫的持续存活建立关联。首先，我们证实微孢子虫A. rigaudi属于溢出型寄生虫（spillover parasite）：在缺乏其维持宿主（maintenance host）A. parthenogenetica的情况下，该寄生虫无法持续存活。这一结果尤为引人注目，因为A. rigaudi在两种宿主的野外种群中均表现出高感染率，且在实验室测试中对两种宿主均具有高感染性。此外，孤雌生殖卤虫的季节性出现为溢出速率带来了季节性特征，导致溢出宿主旧金山卤虫中出现周期性伪地方性流行（cyclical pseudo-endemics）。其次，尽管我们的感染率数据足以将肠孢虫E. artemiae归类为溢出型寄生虫或兼性多宿主寄生虫（facultative multi-host parasite），但无法区分这两种可能性。本研究凸显了在群落背景下开展多宿主寄生虫研究的重要性，并证实：在合适的多宿主系统中，通过对多种环境条件与宿主群落进行采样，可明确阐明寄生虫持续存在的驱动因素。