Chironomus riparius (Diptera) genome sequencing reveals the impact of minisatellite transposable elements on population divergence |
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| Authors: | Ann‐Marie Oppold Hanno Schmidt Marcel Rose Sören Lukas Hellmann Florian Dolze Fabian Ripp Bettina Weich Urs Schmidt‐Ott Erwin Schmidt Robert Kofler Thomas Hankeln Markus Pfenninger |
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| Institution: | 1. Molecular Ecology Group, Institute for Ecology, Evolution & Diversity, Goethe‐University Frankfurt am Main, Hessen, Germany;2. Senckenberg Biodiversity and Climate Research Centre, Frankfurt am Main, Hessen, Germany;3. Institute of Molecular Genetics, Johannes Gutenberg‐University, Mainz, Rheinland‐Pfalz, Germany;4. Department of Organismal Biology and Anatomy, University of Chicago, Chicago, IL, USA;5. Institut für Populationsgenetik, Vienna, Austria |
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| 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 FST estimated from genomewide 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 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. |
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| Keywords: | endogenous selection genome draft insect genome Pool‐Seq speciation transposon |
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