Population-level dynamics in experimental mixed infections: evidence for competitive exclusion among bacterial parasites of Paramecium caudatum

Parasites frequently share their host populations with other parasites. However, little is known about how different parasites respond to competition with diverse competitor species in the within-host and between-host environments. We explored the repeatability of competition by simultaneously exposing microcosm populations of the ciliate Paramecium caudatum to pairs of parasites from the Holospora species complex (H. undulata, H. caryophila and H. obtusa) affected the persistence and prevalence of each compared to single infections, across three host genotypes. Three weeks post-inoculation we identified the presence of each parasite using fluorescence in situ hybridisation (FISH). Competitive exclusion (62/72) was more common than co-existence (10/72) in populations inoculated with 2 parasites. There was a clear pattern of competitive superiority, with H. caryophila persisting in all doubly inoculated populations (with either H. undulata or H. obtusa), and H. undulata tending to exclude H. obtusa. This mirrored infection success in single infections, with H. caryophila having a higher infection prevalence in single inoculations, followed by H. undulata then H. obtusa. The probability of persistence in co-inoculations did not change across the different host genotypes, and prevalence was the same as in single infections. Our results are consistent with superinfection models, which assume the competitive exclusion of parasites upon contact within the same host. Furthermore, such non-random competitive epidemiological dynamics, where one parasites always wins, may be of interest for public health management, especially if the winning parasite is avirulent, as is seemingly the case here.

寄生虫通常会与其他寄生虫共享宿主种群。然而，目前学界对不同寄生虫在宿主体内与宿主间环境中，如何响应不同竞争者物种的竞争作用仍知之甚少。本研究通过将纤毛虫尾草履虫（Paramecium caudatum）的微宇宙种群，同时暴露于来自嗜银虫属（Holospora）物种复合体的寄生虫配对组合（包括波动嗜银虫（H. undulata）、卡氏嗜银虫（H. caryophila）与钝嗜银虫（H. obtusa）），并在三种宿主基因型背景下，对比单感染与共感染条件下各寄生虫的存续率与流行率，以此探究竞争作用的可重复性。接种三周后，我们采用荧光原位杂交（fluorescence in situ hybridisation, FISH）技术鉴定各寄生虫的存在情况。在接种了两种寄生虫的种群中，竞争排斥（62/72）的发生频率远高于共存（10/72）。竞争优势存在明确的层级模式：卡氏嗜银虫可在所有双接种种群（与波动嗜银虫或钝嗜银虫共同接种）中存续，而波动嗜银虫往往会排斥钝嗜银虫。这一模式与单感染条件下的感染成功率相符：卡氏嗜银虫的单接种感染流行率最高，其次为波动嗜银虫，最后是钝嗜银虫。双接种条件下的寄生虫存续概率在不同宿主基因型间无显著差异，且其流行率与单感染时一致。我们的研究结果与超级感染模型相符，该模型假设同一宿主体内接触的寄生虫之间会发生竞争排斥。此外，这种存在明确竞争胜者的非随机竞争流行病学动态，或可对公共卫生管理产生参考价值——若该获胜寄生虫无致病性（本研究中似乎正是如此），则参考价值尤为显著。