Sympatric versus allopatric evolutionary contexts shape differential immune response in Biomphalaria / Schistosoma interaction

Selective pressures between hosts and their parasites can result in reciprocal evolution or adaptation of specific life history traits. Local adaptation of resident hosts and parasites should lead to increase parasite infectivity/virulence (higher compatibility) when infecting hosts from the same location (in sympatry) than from a foreign location (in allopatry). Analysis of geographic variations in compatibility phenotypes is the most common proxy used to infer local adaptation. However, in some cases, allopatric host-parasite systems demonstrate similar or greater compatibility than in sympatry. In such cases, the potential for local adaptation remains unclear. Here, we study the interaction between Schistosoma and its vector snail Biomphalaria in which such discrepancy in local versus foreign compatibility phenotype has been reported. Herein, we aim at bridging this gap of knowledge by comparing life history traits (immune cellular response, host mortality, and parasite growth) and molecular responses in highly compatible sympatric and allopatric Schistosoma/Biomphalaria interactions originating from different geographic localities (Brazil, Venezuela and Burundi). We found that despite displaying similar prevalence phenotypes, sympatric schistosomes triggered a rapid immune suppression (dual-RNAseq analyses) in the snails within 24h post infection, whereas infection by allopatric schistosomes (regardless of the species) was associated with immune cell proliferation and triggered a non-specific generalized immune response after 96h. We observed that, sympatric schistosomes grow more rapidly. Finally, we identify miRNAs differentially expressed by Schistosoma mansoni that target host immune genes and could be responsible for hijacking the host immune response during the sympatric interaction. We show that despite having similar prevalence phenotypes, sympatric and allopatric snail-Schistosoma interactions displayed strong differences in their immunobiological molecular dialogue. Understanding the mechanisms allowing parasites to adapt rapidly and efficiently to new hosts is critical to control disease emergence and risks of Schistosomiasis outbreaks.宿主与寄生虫之间的选择压力可引发特定生活史性状的协同进化与适应性演化。常驻宿主与寄生虫的局部适应（local adaptation）应会使寄生虫在感染同域（sympatric）宿主时，其感染性与毒力（兼容性更高）高于感染异域（allopatric）宿主的情形。对兼容性表型的地理变异进行分析，是推断局部适应最常用的替代指标。然而部分异域宿主-寄生虫系统展现出的兼容性与同域系统相似甚至更高，此类情形下局部适应的潜力仍不明确。 本研究针对已报道存在同域-异域兼容性表型差异的血吸虫（Schistosoma）与其媒介螺类光滑双脐螺（Biomphalaria）的互作展开探究。我们旨在通过比较源自巴西、委内瑞拉与布隆迪等不同地理区域的高兼容性同域与异域血吸虫-光滑双脐螺互作的生活史性状（免疫细胞应答、宿主死亡率与寄生虫增殖情况）及分子应答，填补这一认知空白。 研究结果显示：尽管二者的表型感染率相似，经双转录组测序（dual-RNAseq）分析证实，同域血吸虫在感染后24小时内即可在螺体内引发快速的免疫抑制；而异域血吸虫（无论所属物种）感染则会引发免疫细胞增殖，并在感染96小时后触发非特异性的全身性免疫应答。我们还观察到，同域血吸虫的增殖速度更快。此外，我们鉴定出曼氏血吸虫（Schistosoma mansoni）的差异表达microRNAs（miRNAs），这些miRNAs可靶向宿主免疫基因，或可在同域互作过程中操控宿主免疫应答。 本研究表明，尽管同域与异域的螺类-血吸虫互作具有相似的表型感染率，但其免疫生物学层面的分子互作对话存在显著差异。阐明寄生虫能够快速高效适应新宿主的机制，对于控制血吸虫病（Schistosomiasis）的暴发风险与疾病传播至关重要。