Data from: Ecological host fitting of Trypanosoma cruzi TcI in Bolivia: mosaic population structure, hybridization and a role for humans in Andean parasite dispersal

An improved understanding of how a parasite species exploits its genetic repertoire to colonize novel hosts and environmental niches is crucial to establish the epidemiological risk associated with emergent pathogenic genotypes. Trypanosoma cruzi, a genetically heterogeneous, multi-host zoonosis, provides an ideal system to examine the sylvatic diversification of parasitic protozoa. In Bolivia, T. cruzi I, the oldest and most widespread genetic lineage, is pervasive across a range of ecological clines. High-resolution nuclear (26 loci) and mitochondrial (10 loci) genotyping of 199 contemporaneous sylvatic TcI clones was undertaken to provide insights into the biogeographical basis of T. cruzi evolution. Three distinct sylvatic parasite transmission cycles were identified: one highland population among terrestrial rodent and triatomine species, composed of genetically homogenous strains (Ar = 2.95; PA/L = 0.61; DAS = 0.151), and two highly diverse, parasite assemblages circulating among predominantly arboreal mammals and vectors in the lowlands (Ar = 3.40 and 3.93; PA/L = 1.12 and 0.60; DAS = 0.425 and 0.311, respectively). Very limited gene flow between neighbouring terrestrial highland and arboreal lowland areas (distance ~220 km; FST = 0.42 and 0.35) but strong connectivity between ecologically similar but geographically disparate terrestrial highland ecotopes (distance >465 km; FST = 0.016–0.084) strongly supports ecological host fitting as the predominant mechanism of parasite diversification. Dissimilar heterozygosity estimates (excess in highlands, deficit in lowlands) and mitochondrial introgression among lowland strains may indicate fundamental differences in mating strategies between populations. Finally, accelerated parasite dissemination between densely populated, highland areas, compared to uninhabited lowland foci, likely reflects passive, long-range anthroponotic dispersal. The impact of humans on the risk of epizootic Chagas disease transmission in Bolivia is discussed.深入解析寄生虫物种如何利用其遗传储备侵染新型宿主与环境生态位，对于明确新兴致病基因型相关的流行病学风险至关重要。克氏锥虫（Trypanosoma cruzi）是一种遗传异质性强、宿主多样的人兽共患病原体，为研究寄生原虫的丛林多样化过程提供了理想模型。在玻利维亚，作为最古老且分布最广泛的遗传谱系，克氏锥虫I型（TcI）广泛存在于多种生态梯度生境中。本研究对199株同期分离的丛林型TcI克隆进行了高分辨率核基因（26个位点）与线粒体基因（10个位点）分型，以期解析克氏锥虫演化的生物地理学基础。研究共发现3种独立的丛林型寄生虫传播循环：其一为高地种群，传播循环发生在陆生啮齿类与锥蝽（triatomine）媒介之间，其菌株遗传均一性较高（Ar = 2.95; PA/L = 0.61; DAS = 0.151）；另外两种为高度多样化的寄生虫类群，主要在低地的树栖哺乳动物与媒介种群间循环传播（对应参数分别为Ar = 3.40与3.93; PA/L = 1.12与0.60; DAS = 0.425与0.311）。相邻的陆生高地与树栖低地生境（距离约220 km）间基因交流极有限（FST = 0.42和0.35），但生态特征相似却地理相隔较远的陆生高地生态区（距离>465 km）间却存在较强的遗传连通性（FST = 0.016–0.084），这一结果有力支持生态宿主适配是寄生虫多样化的主要驱动机制。高地种群杂合度过剩、低地种群杂合度缺失的异质性杂合度估计结果，以及低地菌株间存在的线粒体基因渐渗现象，或暗示不同种群间的交配策略存在根本性差异。最后，与无人定居的低地疫源地相比，人口稠密的高地区域间寄生虫扩散速度更快，这大概率反映了人类活动介导的被动远距离人源传播。本研究还探讨了人类活动对玻利维亚美洲锥虫病（Chagas disease）流行传播风险的影响。