How does parasite environmental transmission stage concentration change before, during, and after disease outbreaks?

Outbreaks of environmentally transmitted parasites require that susceptible hosts encounter transmission stages in the environment and become infected, but we also know that transmission stages can be in the environment without triggering disease outbreaks. One challenge for understanding the relationship between environmental transmission stages and disease outbreaks is that the distribution and abundance of transmission stages outside of their hosts have been difficult to quantify. Thus, we have limited data about how changes in transmission stage abundance influence disease dynamics; moreover, we do not know whether the relationship between transmission stages and outbreaks differs among parasite species. We used digital PCR to quantify environmental transmission stages of five parasites in six lakes in southeastern Michigan every two weeks from June to November 2021. At the same time, we quantified infection prevalence in hosts and host density. Our study focused on eight zooplankton host species (Daphnia spp. and Ceriodaphnia dubia) and five of their parasites from diverse taxonomic groups (bacteria, yeast, microsporidia, and oomycete) with different infection mechanisms. We found that parasite transmission stage concentration increased prior to disease outbreaks for all parasites. However, parasites differed significantly in the relative timing of peaks in transmission stage concentration and infection outbreaks. The 'continuous shedder' parasites had transmission stage peaks at the same time as or slightly after the outbreak peaks. In contrast, parasites relying on host death for transmission ('obligate killers') had transmission stage peaks before outbreak peaks. For most parasites, lakes with outbreaks had higher spore concentrations than those without outbreaks, especially once an outbreak began; the exception was for a parasite, Pasteuria ramosa, with very strong genotypic specificity of infection. Overall, our results show that disease outbreaks are tightly linked to transmission stage concentration; outbreaks were preceded by increases in transmission stage concentration in the environment and then were fueled by the production of more transmission stages during the outbreak itself, with concentrations decreasing to pre-outbreak levels as outbreaks waned. Thus, tracking transmission stages in the environment improves our understanding of the drivers of disease outbreaks and reveals how parasite traits may affect these dynamics.

环境传播性寄生虫的暴发，需要易感宿主在环境中接触传播阶段并发生感染，但我们同时也已知晓，环境中存在传播阶段并不一定会触发疾病暴发。理解环境传播阶段与疾病暴发之间关联的一大挑战在于，宿主体外的传播阶段的分布与丰度始终难以量化。因此，我们关于传播阶段丰度变化如何影响疾病动态的数据十分有限；此外，我们也尚不明确不同寄生虫物种间，传播阶段与暴发之间的关联是否存在差异。
为此，我们于2021年6月至11月期间，每两周对密歇根州东南部6个湖泊中的5种寄生虫的环境传播阶段开展数字PCR（digital PCR）定量检测。与此同时，我们还对宿主的感染率与宿主密度进行了量化分析。本研究聚焦于8种浮游动物（zooplankton）宿主物种：水蚤属（Daphnia）物种与莫氏网纹溞（Ceriodaphnia dubia），以及它们所属不同分类类群、具备不同感染机制的5种寄生虫（涵盖细菌、酵母菌、微孢子虫（microsporidia）与卵菌（oomycete））。
我们发现，所有寄生虫的传播阶段浓度均在疾病暴发前出现上升。不过，不同寄生虫的传播阶段浓度峰值与感染暴发的相对时序存在显著差异。‘持续释放型’寄生虫的传播阶段峰值与暴发峰值同步，或略晚于暴发峰值。与之形成鲜明对比的是，依赖宿主死亡完成传播的‘专性致死型’寄生虫，其传播阶段峰值早于暴发峰值。
对于多数寄生虫而言，暴发湖泊的孢子浓度显著高于未暴发湖泊，尤其是在暴发开始后；唯一的例外是Pasteuria ramosa，该寄生虫具备极强的感染基因型特异性。
总体而言，我们的研究结果表明，疾病暴发与传播阶段浓度紧密相关：暴发前期，环境中的传播阶段浓度会逐步升高；暴发期间，宿主产生的更多传播阶段会进一步推动暴发进程；随着暴发消退，浓度会回落至暴发前水平。因此，对环境中的传播阶段进行监测，能够增进我们对疾病暴发驱动因素的理解，并揭示寄生虫性状如何影响这些动态过程。