The Relationship between Host Lifespan and Pathogen Reservoir Potential: An Analysis in the System Arabidopsis thaliana-Cucumber mosaic virus

Identification of the determinants of pathogen reservoir potential is central to understand disease emergence. It has been proposed that host lifespan is one such determinant: short-lived hosts will invest less in costly defenses against pathogens, so that they will be more susceptible to infection, more competent as sources of infection and/or will sustain larger vector populations, thus being effective reservoirs for the infection of long-lived hosts. This hypothesis is sustained by analyses of different hosts of multihost pathogens, but not of different genotypes of the same host species. Here we examined this hypothesis by comparing two genotypes of the plant Arabidopsis thaliana that differ largely both in life-span and in tolerance to its natural pathogen Cucumber mosaic virus (CMV). Experiments with the aphid vector Myzus persicae showed that both genotypes were similarly competent as sources for virus transmission, but the short-lived genotype was more susceptible to infection and was able to sustain larger vector populations. To explore how differences in defense against CMV and its vector relate to reservoir potential, we developed a model that was run for a set of experimentally-determined parameters, and for a realistic range of host plant and vector population densities. Model simulations showed that the less efficient defenses of the short-lived genotype resulted in higher reservoir potential, which in heterogeneous host populations may be balanced by the longer infectious period of the long-lived genotype. This balance was modulated by the demography of both host and vector populations, and by the genetic composition of the host population. Thus, within-species genetic diversity for lifespan and defenses against pathogens will result in polymorphisms for pathogen reservoir potential, which will condition within-population infection dynamics. These results are relevant for a better understanding of host-pathogen co-evolution, and of the dynamics of pathogen emergence.

明确病原体储库潜力（pathogen reservoir potential）的决定因子，是理解疾病出现机制的核心所在。有研究提出宿主寿命便是此类决定因子之一：短寿命宿主对代价高昂的病原体防御行为的投入会更少，因此它们更易受感染、作为感染源的传播效能更强，或是能够维持更大的媒介种群规模，进而成为感染长寿命宿主的有效储库。该假说已通过多宿主病原体的不同宿主类群分析得到验证，但尚未在同一宿主物种的不同基因型间得到证实。本研究针对该假说展开验证，选取了在寿命以及对天然病原体黄瓜花叶病毒（Cucumber mosaic virus, CMV）的耐受性方面均存在显著差异的两种拟南芥（Arabidopsis thaliana）基因型进行比较分析。研究人员借助蚜虫媒介桃蚜（Myzus persicae）开展实验，结果显示两种基因型作为病毒传播源的效能并无显著差异，但短寿命基因型更易受感染，且能够维持更大的蚜虫种群规模。为探究宿主对CMV及其媒介的防御差异如何影响储库潜力，本研究构建了一套模型，并基于实验测定的参数集以及符合真实生态场景的宿主植物与媒介种群密度区间开展模拟运算。模型模拟结果表明，短寿命基因型较弱的防御能力使其具备更高的储库潜力；而在宿主种群异质性的情况下，长寿命宿主更长的感染持续期可抵消这一优势。这种平衡受到宿主与媒介种群的种群动态，以及宿主种群的遗传组成共同调控。因此，同一物种内针对寿命与病原体防御的遗传多样性，会导致病原体储库潜力出现遗传多态性，进而调控种群内的感染动态。上述研究结果有助于更深入地理解宿主-病原体协同进化机制，以及病原体出现的种群动态过程。