Host-associated Genetic Differentiation in the Face of Ongoing Gene Flow: Ecological Speciation in a Pathogenic Parasite of Freshwater Fish

Adaptive evolution in response to varying environments, which leads to population divergence, is one of the most intriguing processes of speciation. However, its effectiveness amidst ongoing gene flow remains controversial. Our study challenges the controversy by analysing population genetic structure, degree of gene flow, and the level of genomic divergence between lineages of a tapeworm parasite (Ligula intestinalis), isolated from different species of fish hosts occurring in sympatry. The parasite, which must overcome the host's immunological defences for a successful infection, has a highly pathogenic impact. Utilising genome-wide Single Nucleotide Polymorphisms (SNPs) and transcriptome data, we investigated whether individual host species impose selection pressures on the parasite populations. Genetic clustering analyses revealed divergence between parasites infecting bream (Abramis brama) and those infecting roach (Rutilus rutilus), bleak (Alburnus alburnus), and rudd (Scardinius erythrophthalmus). Historical demography modelling suggested that the most plausible scenario for this divergence is isolation with continuous gene flow. Selection analysis identified 896 SNPs under selection, exhibiting lower to moderate nucleotide diversity and genetic divergence compared to neutral loci. Transcriptome profiling corroborated these results, revealing distinct gene expression profiles for the two parasite populations. An in-depth examination of the selected SNPs and differentially expressed genes revealed specific genes and their physiological functions, as candidates for the molecular mechanisms of immune evasion and, thus, for driving ecological speciation in the parasite. This study showcases the interplay between host specificity, population demography, and disruptive selection in ecological speciation. By dissecting the genomic factors at play, we gain a better understanding of the mechanisms facilitating population divergence in the presence of gene flow.响应多变环境的适应性进化可引发种群分化，是物种形成过程中最引人关注的核心进程之一。然而，在持续存在基因流（gene flow）的背景下，该过程的有效性仍存在争议。本研究通过分析分别采自同域分布不同鱼类宿主的寄生绦虫（肠舌状绦虫*Ligula intestinalis*）各谱系间的种群遗传结构、基因流程度以及基因组分化水平，对这一争议提出了挑战。该寄生绦虫需突破宿主的免疫防御才能成功建立感染，具有极强的致病性。本研究利用全基因组单核苷酸多态性（Single Nucleotide Polymorphisms, SNPs）与转录组数据，探究不同宿主物种是否会对寄生绦虫种群施加选择压力。遗传聚类分析显示，感染欧鳊（*Abramis brama*）的寄生绦虫与感染斜齿鳊（*Rutilus rutilus*）、欧白鱼（*Alburnus alburnus*）以及赤梢鱼（*Scardinius erythrophthalmus*）的绦虫之间存在分化。历史种群动态建模结果表明，该分化最合理的演化情景为持续存在基因流的隔离分化模式。选择分析共筛选出896个受选择的SNPs，相较于中性位点，这些位点的核苷酸多样性与遗传分化水平均处于较低至中等水平。转录组表达谱分析验证了上述结果，发现两类寄生绦虫种群具有显著差异的基因表达谱。对受选择SNPs与差异表达基因的深入解析，揭示了若干与免疫逃逸相关的特定基因及其生理功能，这些可作为寄生绦虫生态物种形成分子机制的候选靶点。本研究揭示了宿主特异性、种群动态与歧化选择在生态物种形成过程中的相互作用。通过解析发挥作用的基因组因子，我们得以更深入地理解在基因流存在的背景下，促进种群分化的分子机制。