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

Abstract

Active 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 midge Chironomus riparius, focussing on a Chironomus-specific TE, the minisatellite-like Cla-element, whose activity is associated with speciation in the genus.Using an improved 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 highly significant correlation of pairwise population F ST from genome-wide SNPs with the F ST estimated from TEs suggests 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 indicates that segregating, i.e. heterozygous insertions are selected against. With reciprocal crossing experiments and fluorescent in-situ hybridisation of Cla-elements to 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 heterozygous Claelement insertions causes endogenous genetic barriers and therefore acts as DMI among C. riparius populations. 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.

Direct estimation of the spontaneous mutation rate by short-term mutation accumulation lines inChironomus riparius

“…Monomer nucleotide runs in the C. riparius draft genome have a strong A/T bias (98%, Supplemental Text 2) and are product of and contribute over proportionally to the overall high A/T content (69%) of the genome (Oppold et al. ). The comparison of the abundance and length of monomer nucleotide runs in the genomes of C. riparius and D. melanogaster revealed a larger number of longer monomer nucleotide runs in C. riparius (Supplemental Text 2: Fig.…”

“…Even though not significantly different, the observed bias toward G/C > A/T mutations is in line with the high A/T content of the C. riparius genome (G/C content 31%, Oppold et al . ). This A/T bias of the C. riparius genome is probably also responsible for the observed shift from SNMs to indel mutations compared to other organisms (Supplemental Text 2).…”

“…We used a strain of C. riparius that was established from a field population in Western Germany and kept since several decades in various laboratories for genetic and ecotoxicological research (“Laufer population”), from which also the C. riparius reference draft genome was sequenced (Oppold et al. ). Larvae from a single egg‐clutch were raised at 20°C under most permissive conditions concerning space and food (OECD ) to avoid selection.…”

“…Using coalescence estimates of the population mutation parameter (θ) from 30 unlinked nongenic regions in European natural C. riparius populations (Oppold et al. , Supplemental Text S1: Table ) between 0.018 and 0.034, we estimate N e for these populations following Charlesworth (): N e = θ/4μ .…”

“…Table 1 : Estimated population mutation parameter θ and effective population size for each of five natural C. riparius populations (refer to Oppold et al . for detailed sample information). Figure 1 .…”