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 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 FSTestimated from genomewide single-nucleotide polymorphisms (SNPs) and the FSTestimated from TEs is consistent with drift as the major force driving TE population differentiation. However, the significantly higher Cla-element FSTlevel 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.
Molecular Ecology Group, Institute for Ecology, Evolution & Diversity, Goethe-University Frankfurt am Main, Max-von-Laue-Str. 9, 60438 Frankfurt am Main, Hessen, Germany.|Senckenberg Biodiversity and Climate Research Centre, Georg-Voigt-Str. 14-16, 60325, Frankfurt am Main, Hessen, Germany.
Ann-Marie
http://orcid.org/0000-0003-2637-0766
AM
Oppold
Senckenberg Biodiversity and Climate Research Centre, Georg-Voigt-Str. 14-16, 60325, Frankfurt am Main, Hessen, Germany.
Hanno
H
Schmidt
Molecular Ecology Group, Institute for Ecology, Evolution & Diversity, Goethe-University Frankfurt am Main, Max-von-Laue-Str. 9, 60438 Frankfurt am Main, Hessen, Germany.
Marcel
M
Rose
Institute of Molecular Genetics, Johannes Gutenberg-University, Johann-Joachim-Becherweg 30a, 55128, Mainz, Rheinland-Pfalz, Germany.
Sören Lukas
SL
Hellmann
Institute of Molecular Genetics, Johannes Gutenberg-University, Johann-Joachim-Becherweg 30a, 55128, Mainz, Rheinland-Pfalz, Germany.
Florian
F
Dolze
Institute of Molecular Genetics, Johannes Gutenberg-University, Johann-Joachim-Becherweg 30a, 55128, Mainz, Rheinland-Pfalz, Germany.
Fabian
F
Ripp
Institute of Molecular Genetics, Johannes Gutenberg-University, Johann-Joachim-Becherweg 30a, 55128, Mainz, Rheinland-Pfalz, Germany.
Bettina
B
Weich
Department of Organismal Biology and Anatomy, University of Chicago, 920 E. 58th Street, 1061C, Chicago, IL, 60637, USA.
Urs
U
Schmidt-Ott
Institute of Molecular Genetics, Johannes Gutenberg-University, Johann-Joachim-Becherweg 30a, 55128, Mainz, Rheinland-Pfalz, Germany.
Erwin
E
Schmidt
Institut für Populationsgenetik, Vetmeduni Vienna, 1210, Vienna, Austria.
Robert
R
Kofler
Institute of Molecular Genetics, Johannes Gutenberg-University, Johann-Joachim-Becherweg 30a, 55128, Mainz, Rheinland-Pfalz, Germany.
Thomas
T
Hankeln
Molecular Ecology Group, Institute for Ecology, Evolution & Diversity, Goethe-University Frankfurt am Main, Max-von-Laue-Str. 9, 60438 Frankfurt am Main, Hessen, Germany.|Senckenberg Biodiversity and Climate Research Centre, Georg-Voigt-Str. 14-16, 60325, Frankfurt am Main, Hessen, Germany.
Markus
M
Pfenninger
D000818:Animals; D002683:Chironomidae / Q000235:genetics*; D004251:DNA Transposable Elements; D019143:Evolution, Molecular; D005260:Female; D005828:Genetics, Population; D049750:Genome, Insect; D017404:In Situ Hybridization, Fluorescence; D018598:Minisatellite Repeats; D020641:Polymorphism, Single Nucleotide
D004251:DNA Transposable Elements
Pool-Seq; endogenous selection; genome draft; insect genome; speciation; transposon