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), 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 estimated from genomewide single-nucleotide polymorphisms (SNPs) and the F estimated from TEs is consistent with drift as the major force driving TE population differentiation. However, the significantly higher Cla-element F 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 TEs may thus have a direct impact on population divergence that is operationally different from drift and local adaptation.

The genomic footprint of climate adaptation in Chironomus riparius

“…We used 100‐bp paired‐end, Illumina sequencing as Pool‐Seq data, derived from 105 to 168 individuals for each population to analyse allele frequency differences and gene flow among populations (see Oppold et al., ; for more details about library preparation, sequencing process and quality processing of raw data, ENA project number PRJEB19848). Pool‐Seq data were mapped to the C. riparius draft genome (European Nucleotide Archive Accession no.…”

“…Pool‐Seq data were mapped to the C. riparius draft genome (European Nucleotide Archive Accession no. PRJEB15223, Oppold et al., ) and processed for downstream analysis with PoPoolation2 (version 1201, Kofler, Pandey, & Schlötterer, ; Supporting information 1.4).…”

“…We conducted common‐garden experiments to determine phenotypic differences in several life history traits among populations and confirmed their adaptation to different temperatures. Making use of the recently published C. riparius draft genome (Oppold et al., ), we performed genome scans in a comparative outlier approach to identify signatures of adaptation. Outlier thresholds were obtained from a statistical and a modelling approach based on the demographic population histories inferred by Multiple Sequentially Markovian Coalescence (MSMC, Schiffels & Durbin, ), and separately estimated migration rates.…”

Establishing laboratory cultures and performing ecological and evolutionary experiments with the emerging model species Chironomus riparius

“…If the genetic variability is supposed to approach conditions in the field, not less than 20–30 egg clutches should be used. Please note that mixing egg clutches or reinforcing an existing laboratory population from different populations may result in diminished fitness due to outbreeding depression among geographically distant populations (Oppold et al, ).…”

“…Moreover, the integration of experimental investigations with genetics and genomics is possible since the publication of a high‐quality draft genome as reference sequence (Oppold et al, ). Furthermore, important population genetic parameters have been studied, such as the species‐specific spontaneous mutation rate (Oppold & Pfenninger, ), its genomic and transcriptomic basis of niche differentiation (Schmidt, Greshake, Feldmeyer, Hankeln, & Pfenninger, ), demography in European populations (Waldvogel et al, ), and its genomic architecture (Kraemer & Schmidt, ; Oppold et al, ; Zampicinini, Blinov, Cervella, Guryev, & Sella, ). The possibility to easily obtain natural populations from a large distribution range, its capacity to cope with laboratory culture conditions and the availability of genetic and genomic resources makes C. riparius a suitable study organism for many disciplines and research areas.…”