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