Life History and Demographic Drivers of Reservoir Competence for Three Tick-Borne Zoonotic Pathogens

Animal and plant species differ dramatically in their quality as hosts for multi-host pathogens, but the causes of this variation are poorly understood. A group of small mammals, including small rodents and shrews, are among the most competent natural reservoirs for three tick-borne zoonotic pathogens, Borrelia burgdorferi, Babesia microti, and Anaplasma phagocytophilum, in eastern North America. For a group of nine commonly-infected mammals spanning >2 orders of magnitude in body mass, we asked whether life history features or surrogates for (unknown) encounter rates with ticks, predicted reservoir competence for each pathogen. Life history features associated with a fast pace of life generally were positively correlated with reservoir competence. However, a model comparison approach revealed that host population density, as a proxy for encounter rates between hosts and pathogens, generally received more support than did life history features. The specific life history features and the importance of host population density differed somewhat between the different pathogens. We interpret these results as supporting two alternative but non-exclusive hypotheses for why ecologically widespread, synanthropic species are often the most competent reservoirs for multi-host pathogens. First, multi-host pathogens might adapt to those hosts they are most likely to experience, which are likely to be the most abundant and/or frequently bitten by tick vectors. Second, species with fast life histories might allocate less to certain immune defenses, which could increase their reservoir competence. Results suggest that of the host species that might potentially be exposed, those with comparatively high population densities, small bodies, and fast pace of life will often be keystone reservoirs that should be targeted for surveillance or management.

动植物物种作为多宿主病原（multi-host pathogens）的宿主时，其宿主质量差异悬殊，而造成这种差异的成因仍未得到充分阐释。在北美东部，包括小型啮齿类与鼩鼱在内的一类小型哺乳动物，是三种蜱传人畜共患病原（tick-borne zoonotic pathogens）——伯氏疏螺旋体（Borrelia burgdorferi）、微小巴贝西虫（Babesia microti）及嗜吞噬细胞无形体（Anaplasma phagocytophilum）——最具感染能力的天然储存宿主之一。我们选取了9种常见感染哺乳动物作为研究对象，其体重跨度超过两个数量级，旨在探究生活史特征，或是（未知的）宿主与蜱接触率的替代指标，能否预测各病原的宿主储存能力（reservoir competence）。与快生活史策略相关的生活史特征，通常与宿主储存能力呈正相关。但通过模型比较分析发现，作为宿主与病原接触率替代指标的宿主种群密度，其得到的模型支持度总体高于生活史特征。针对不同病原，关键的生活史特征以及宿主种群密度的重要程度存在一定差异。我们将本研究结果解读为支持两个互为备选但并非互斥的假说，用以解释为何生态分布广泛的伴人物种（synanthropic species）往往是多宿主病原最具感染能力的储存宿主。其一，多宿主病原或许会适配其最常接触的宿主，而这类宿主往往种群数量最多，或最易被蜱媒叮咬。其二，采用快生活史策略的物种，可能会在部分免疫防御方面投入更少资源，这或许会提升其宿主储存能力。研究结果表明，在所有可能接触病原的宿主物种中，种群密度较高、体型较小且采用快生活史策略的物种，往往会成为关键储存宿主，应将其作为监测或防控的重点对象。