Host preferences inhibit transmission from potential superspreader host species

Host species that are particularly abundant, infectious, and/or infected tend to contribute disproportionately to symbiont (parasite or mutualist) maintenance in multi-host systems. Therefore, in a facultative multi-host system where two host species had high densities, high symbiont infestation intensities, and high infestation prevalence, we expected interspecific transmission rates to be high. Instead, we found that interspecific symbiont transmission rates to caged sentinel hosts were an order of magnitude lower than intraspecific transmission rates in the wild. Using laboratory experiments to decompose transmission rates, we found that opportunities for interspecific transmission were frequent, where interspecific and intraspecific contact rate functions were statistically indistinguishable. But most interspecific contacts did not lead to transmission events due to a previously unrecognized transmission barrier: strong host preferences. During laboratory choice experiments, the symbiont preferred staying on or dispersing to its current host species, even though the oligochaete symbiont is a globally distributed host generalist that can survive and reproduce on many snail species. These surprising results suggest that when managing symbiont transmission, identifying key host species is still important, but it may be equally important to identify and manage transmission barriers that keep potential superspreader host species in check.

Methods
Though Chaetogaster limnaei has a broad host distribution, two snail genera, Helisoma and Physa, have been the focus for most prior experiments and are especially abundant in ponds in North America. Therefore, for all field and laboratory studies, we used H. trivolvis snails as the focal host species (i.e., the species in which we quantified infestation rates) and P. gyrina as the alternative host species. We especially focused on interspecific transmission from P. gyrina to H. trivolvis (alternative to focal host transmission; hereafter alternative–focal), which complements prior work that quantified intraspecific transmission among H. trivolvis snails (focal to focal host transmission; hereafter focal–focal). We used a sentinel host approach to quantify the rate that uninfested focal hosts (H. trivolvis) that had been raised in the laboratory became infested when caged in the field due to contacts with wild H. trivolvis and P. gyrina through the mesh on the field cages. We then decomposed the estimated interspecific transmission rate using two laboratory experiments that quantified interspecific contact rates and interspecific transmission success. The three R script files correspond to the analyses of the field data, interspecific contact rate experiment, and interspecific transmission success experiment.

在多宿主系统（multi-host system）中，种群丰度极高、传染性强且/或感染率可观的宿主物种，往往会不成比例地促进共生体（symbiont，包含寄生虫与互利共生者）在多宿主系统中的维持。因此，在两个宿主种群密度高、共生体侵染强度（infestation intensity）大、侵染流行率（infestation prevalence）高的兼性多宿主系统（facultative multi-host system）中，我们曾预测种间传播速率（interspecific transmission rates）会处于较高水平。但实际观测结果却显示，野外环境中，针对笼养哨兵宿主（sentinel host）的种间共生体传播速率，较种内传播速率低一个数量级。我们通过室内实验拆解传播速率的构成要素，发现种间传播的接触机会十分频繁：种间与种内的接触率函数在统计学上并无显著差异。但绝大多数种间接触并未引发传播事件，这源于此前未被发现的传播障碍——强烈的宿主偏好性。室内选择实验表明，即便该寡毛类（oligochaete）共生体是全球分布的宿主泛化种（host generalist），可在多种螺类宿主上存活并繁殖，它仍更倾向于停留在或扩散至当前寄生的宿主物种。这一意外结果表明，在管控共生体传播时，识别关键宿主物种依然至关重要，但识别并管控那些抑制潜在超级传播者（superspreader）宿主种群的传播障碍，或许同样举足轻重。

方法
尽管螺形嗜壳虫（Chaetogaster limnaei）的宿主分布范围较广，但扁卷螺属（Helisoma）与膀胱螺属（Physa）是此前多数实验的研究焦点，且在北美池塘中种群尤为丰富。因此，本研究所有野外与室内实验均以美洲扁卷螺（Helisoma trivolvis, 下称H. trivolvis）作为目标宿主物种（即我们量化侵染率的宿主类群），以细带膀胱螺（Physa gyrina, 下称P. gyrina）作为替代宿主。我们重点关注从P. gyrina到H. trivolvis的种间传播（替代宿主向目标宿主的传播，下称“替代-目标”传播），以此补充此前针对H. trivolvis种内传播（目标宿主向目标宿主的传播，下称“目标-目标”传播）的研究成果。我们采用哨兵宿主法，通过野外笼体的网孔使实验螺与野生H. trivolvis和P. gyrina接触，量化实验室饲养的未侵染目标宿主（H. trivolvis）在野外笼养环境下的侵染速率。随后，我们通过两项室内实验拆解估算得到的种间传播速率，分别量化种间接触率与种间传播成功率。配套的三个R脚本文件分别对应野外数据、种间接触率实验以及种间传播成功率实验的分析流程。