Genotypic variation in parasite avoidance behavior and other mechanistic, non-linear components of transmission

Traditional epidemiological models assume that transmission increases proportionally to the density of parasites. However, empirical data frequently contradict this assumption. General yet mechanistic models can explain why transmission depends non-linearly on parasite density and thereby identify potential defensive strategies of hosts. For example, hosts could decrease their exposure rates at higher parasite densities (via behavioral avoidance) or decrease their per-parasite susceptibility when encountering more parasites (e.g., via stronger immune responses). To illustrate, we fit mechanistic transmission models to 19 genotypes of Daphnia dentifera hosts over gradients of the trophically-acquired parasite, Metschnikowia bicuspidata. Exposure rate (foraging, F) frequently decreased with parasite density (Z), and per-parasite susceptibility (U) frequently decreased with parasite encounters (FxZ). Consequently, infection rates (FxUxZ) often peaked at intermediate parasite densities. Moreover, host genotypes varied substantially in these responses. Exposure rates remained constant for some genotypes, but decreased sensitively with parasite density for others (up to 78%). Furthermore, genotypes with more sensitive foraging/exposure also foraged faster in the absence of parasites (suggesting ‘fast and sensitive’ versus ‘slow and steady’ strategies). These relationships suggest that high densities of parasites can inhibit transmission by decreasing exposure rates and/or per-parasite susceptibility, and identify several intriguing axes for the evolution of host defense.

传统流行病学模型假设，寄生虫传播速率与寄生虫密度呈正比增长。然而，实证数据时常与该假设相悖。兼具通用性与机制阐释性的模型，可阐明传播随寄生虫密度呈非线性变化的内在原因，并借此识别宿主的潜在防御策略。例如，宿主可在寄生虫密度升高时通过行为规避降低暴露率，或是在接触更多寄生虫时（如通过强化免疫应答）降低单寄生虫易感性。为验证上述理论，我们针对19种齿突水蚤（Daphnia dentifera）基因型，在经营养途径传播的寄生虫——两孢梅奇酵母（Metschnikowia bicuspidata）的浓度梯度环境下，拟合了机制性传播模型。研究发现，暴露率（即觅食行为F）常随寄生虫密度Z升高而降低，且单寄生虫易感性U随寄生虫接触量（F×Z）的增加而下降。由此，感染率（F×Z×U）通常在寄生虫密度处于中等水平时达到峰值。此外，不同宿主基因型的这类响应存在显著差异：部分基因型的暴露率保持恒定，而另一些则随寄生虫密度变化呈现敏感下降，降幅最高可达78%。进一步分析显示，觅食/暴露响应更敏感的基因型，在无寄生虫的环境下觅食速度更快，这提示宿主防御存在“快速敏感型”与“缓慢稳健型”两类策略。上述关联表明，高寄生虫密度可通过降低宿主暴露率或（和）单寄生虫易感性来抑制传播，同时为宿主防御的演化研究指明了若干颇具潜力的方向。