Transposable elements (TEs) have been shown to shape genome evolution and are suspected to drive speciation processes. However, besides the well-studied cases of classic Drosophila-specific TEs, knowledge on the mechanisms of how TEs may actually confer reproductive isolation (RI) is lacking. In our study on the non-biting midge Chironomus riparius, we propose a novel mechanism how transposons can contribute to species divergence. Focusing on a specific type of TE, the mostly tandem-repetitive, minisatellite-like Cla-element, whose increased activity is possibly associated with speciation events in the genus Chironomus, we investigated whether differential TE activity may be responsible for RI among conspecific populations.
With reciprocal crossing experiments, we found initial stages of RI among geographically and ecologically most distant C. riparius populations and visualized aberrations in giant polytene chromosomes of hybrid individuals. Using a novel C. riparius draft genome assembly, we unveiled diverging TE distribution patterns between populations. A highly significant correlation of the pairwise population FST as inferred by genome wide SNPs with the FST estimated from TEs suggested genomic drift as the major force driving TE population differentiation. However, there is significant indication for negative selection against heterozygous Cla-element insertions that especially occur in inter-population hybrids. Together with a possible imperfect pairing of homologous chromosomes in regions of heterozygous Cla-element bands, we suggest a new hypothesis on how the Cla-element might be involved in conferring RI in C. riparius, and, more generally, how TEs can contribute to species divergence. Our study thus shows that the role of TEs in the organisation of genomic architecture can influence fitness and directly contribute to evolutionary processes.