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

Abstract

Abstract Active transposable elements ( TE s) 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 ), thus contributing to the evolution of endogenous genetic barriers and eventually causing population divergence. We investigated differential TE abundance among conspecific populations of the nonbiting midge Chironomus riparius and evaluated their potential role in causing endogenous genetic incompatibilities between these populations. We focussed on a Chironomus ‐specific TE , the minisatellite‐like Cla‐element , whose activity is associated with speciation in the genus. Using a newly generated and annotated draft genome for a genomic study with five natural C. riparius populations, we found highly population‐specific TE insertion patterns with many private insertions. A significant correlation of the pairwise F ST estimated from genomewide single‐nucleotide polymorphisms ( SNP s) and the F ST estimated from TE s is consistent with drift as the major force driving TE population differentiation. However, the significantly higher Cla‐element F ST level due to a high proportion of differentially fixed Cla‐element insertions also indicates selection against segregating (i.e. heterozygous) insertions. With reciprocal crossing experiments and fluorescent in situ hybridization of Cla‐elements to polytene chromosomes, we documented phenotypic effects on female fertility and chromosomal mispairings. We propose that the inferred negative selection on heterozygous Cla‐element insertions may cause endogenous genetic barriers and therefore acts as DMI among C. riparius populations. The intrinsic genomic turnover exerted by TE s may thus have a direct impact on population divergence that is operationally different from drift and local adaptation.