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.适应不同环境的适应性演化可导致种群分化，是物种形成过程中最引人入胜的机制之一。然而，在持续存在基因流的背景下，该过程的有效性仍存在广泛争议。本研究以寄生于同域分布不同鱼类宿主的舌状绦虫（Ligula intestinalis）为研究对象，通过分析其不同谱系间的种群遗传结构、基因流程度与基因组分化水平，对这一争议提出了新的挑战。该寄生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（SNPs）与转录组数据，探究不同宿主物种是否会对寄生虫种群施加差异化选择压力。遗传聚类分析结果显示，寄生于欧鳊（Abramis brama）的寄生虫种群，与寄生于拟鲤（Rutilus rutilus）、欧白鱼（Alburnus alburnus）以及红鳍鳑鲏（Scardinius erythrophthalmus）的寄生虫种群之间存在显著分化。种群历史动态建模表明，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。选择分析共鉴定出896个受选择的SNPs位点，与中性位点相比，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。转录组分析验证了上述结果，发现两类寄生虫种群具有显著差异的基因表达谱。对受选择SNPs位点与差异表达基因的深入解析，揭示了若干候选基因及其生理功能，这些基因可能参与免疫逃避的分子机制，进而推动该寄生虫的生态物种形成。本研究阐明了宿主特异性、种群人口统计学与歧化选择在生态物种形成过程中的相互作用。通过解析其中发挥关键作用的基因组因子，我们得以更深入地理解在基因流持续存在的条件下，推动种群分化的分子与演化机制。