Spatial population genetic structure of a bacterial parasite in close coevolution with its host

Knowledge of a species’ population genetic structure can provide insight into fundamental ecological and evolutionary processes including gene flow, genetic drift, and adaptive evolution. Such inference is of particular importance for parasites, as an understanding of their population structure can illuminate epidemiological and coevolutionary dynamics. Here we describe the population genetic structure of the bacterium Pasteuria ramosa, a parasite that infects planktonic crustaceans of the genus Daphnia. This system has become a model for investigations of host-parasite interactions and represents an example of coevolution via negative frequency-dependent selection (a.k.a. ‘Red Queen’ dynamics). To sample P. ramosa, we experimentally infected a panel of Daphnia hosts with natural spore banks from the sediments of 25 ponds throughout much of the species range in Europe and Western Asia. Using 12 polymorphic VNTR loci, we identified substantial genetic diversity both within and among localities that was structured geographically among ponds. Genetic diversity was also structured among host genotypes within ponds, though this pattern varied by locality, with P. ramosa at some localities partitioned into distinct host-specific lineages, and other localities where recombination had shuffled genetic variation among different infection phenotypes. Across the sample range, there was a pattern of isolation-by-distance, and principal components analysis coupled with Procrustes rotation identified congruence between patterns of genetic variation and geography. Our findings support the hypothesis that Pasteuria is an endemic parasite coevolving closely with its host. These results provide important context for previous studies of this model system and inform hypotheses for future research.

解析某一物种的种群遗传结构，可深入揭示其核心生态与演化过程，包括基因流、遗传漂变与适应性演化。这类种群结构解析对于寄生虫而言尤为关键，因为明晰其种群结构能够阐释流行病学与协同演化动态。本研究旨在阐明拉氏芽孢杆菌（Pasteuria ramosa）的种群遗传结构——该菌是一类寄生于溞属（Daphnia）浮游甲壳动物的寄生虫。该研究体系已成为宿主-寄生虫互作研究的经典模型，同时也是通过负频率依赖选择（negative frequency-dependent selection，又称‘红皇后’动态）实现协同演化的典型案例。
为采集拉氏芽孢杆菌样本，研究团队利用覆盖欧洲与西亚大部分分布区的25个池塘沉积物中的自然孢子库，对一组溞属宿主开展了人工感染实验。本研究采用12个多态性可变数目串联重复序列（Variable Number Tandem Repeats，简称VNTR）位点，检测到不同池塘间以及同一池塘内部均存在丰富的遗传多样性，且该多样性呈现出明显的地理空间结构特征。池塘内部的宿主基因型间同样存在遗传多样性结构，但该模式因采样地点而异：部分采样点的拉氏芽孢杆菌可划分为不同的宿主特异性谱系，而另一些采样点则发生了重组，使得不同感染表型间的遗传变异发生了重组洗牌。
在整个采样范围内，研究观察到了距离隔离模式；结合主成分分析（principal components analysis，PCA）与普罗克汝斯特旋转分析，结果表明遗传变异模式与地理分布模式存在显著一致性。本研究结果支持‘拉氏芽孢杆菌是一类与其宿主紧密协同演化的地方性寄生虫’这一假说。上述研究结果为该经典模型体系的既往研究提供了重要背景，同时也为未来的研究假说构建提供了参考依据。