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

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 cause population divergence. We investigated differential TE abundance among conspecific populations of the non-biting 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 FST estimated from genome-wide single nucleotide polymorphisms (SNPs) and the FST estimated from TEs, is consistent with drift as the major force driving TE population differentiation. However, the significantly higher Cla-element FST 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 hybridisation 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.

活性转座因子（transposable elements, TEs）可导致同种种群间基因组插入模式与丰度格局产生分化。当群体发生次生接触时，这种分化的遗传背景理论上可引发经典的多布然斯基-穆勒不相容性（Dobzhansky-Muller incompatibilities, DMI），进而推动内源遗传屏障的演化，最终引发种群分化。本研究针对非咬摇蚊（Chironomus riparius）的同种群体间转座因子丰度差异展开调查，并评估其在引发这些群体间内源遗传不相容性中的潜在作用。研究聚焦于摇蚊属特异性转座因子——类小卫星Cla元件，该元件的活性与该属的物种形成过程密切相关。本研究利用新组装并注释的草图基因组，对5个天然C. riparius群体开展基因组研究，结果发现具有高度群体特异性的转座因子插入模式，且存在大量私有插入位点。基于全基因组单核苷酸多态性（single nucleotide polymorphisms, SNPs）估算的成对FST值，与基于转座因子估算的成对FST值呈显著相关，这与"遗传漂变是驱动转座因子种群分化的主要力量"这一结论相符。然而，由于差异固定的Cla元件插入位点占比极高，Cla元件的FST值显著更高，这也表明存在针对分离（即杂合）插入位点的负选择。通过正反交实验以及Cla元件对多线染色体的荧光原位杂交（fluorescent in-situ hybridisation），本研究记录到其对雌性育性与染色体错配的表型效应。我们提出，推断得到的针对杂合Cla元件插入位点的负选择，可能引发内源遗传屏障，进而在C. riparius群体间充当多布然斯基-穆勒不相容性。因此，转座因子介导的固有基因组周转，可能直接影响种群分化，其作用机制与遗传漂变和局部适应存在本质区别。