Chironomus riparius(Diptera) genome sequencing reveals the impact of minisatellite transposable elements on population divergence

Abstract

AbstractActive transposable elements (TEs) may result in divergent genomic insertion and abundance patterns among conspecific populations. Upon secondary contact, such divergent genetic backgrounds can theoretically give rise to classical Dobzhansky-Muller incompatibilities (DMI), a way how TEs can contribute to the evolution of endogenous genetic barriers and eventually population divergence. We investigated whether differential TE activity created endogenous selection pressures among conspecific populations of the non-biting midgeChironomus riparius,focussing on aChironomus-specific TE, the minisatellite-likeCla-element, whose activity is associated with speciation in the genus. Using an improved and annotated draft genome for a genomic study with five naturalC. ripariuspopulations, we found highly population-specific TE insertion patterns with many private insertions. A highly significant correlation of pairwise population FSTfrom genome-wide SNPs with the FSTestimated from TEs suggests drift as the major force driving TE population differentiation. However, the significantly higherCla-elementFSTlevel due to a high proportion of differentially fixedCla-elementinsertions indicates that segregating, i.e. heterozygous insertions are selected against. With reciprocal crossing experiments and fluorescent in-situ hybridisation ofCla-elementsto polytene chromosomes, we documented phenotypic effects on female fertility and chromosomal mispairings that might be linked to DMI in hybrids. We propose that the inferred negative selection on heterozygousCla-elementinsertions causes endogenous genetic barriers and therefore acts as DMI amongC. ripariuspopulations. The intrinsic genomic turnover exerted by TEs, thus, may have a direct impact on population divergence that is operationally different from drift and local adaptation.