Genome differentiation in a species pair of coregonine fishes: an extremely rapid speciation driven by stress-activated retrotransposons mediating extensive ribosomal DNA multiplications

Abstract

BackgroundSympatric species pairs are particularly common in freshwater fishes associated with postglacial lakes in northern temperate environments. The nature of divergences between co-occurring sympatric species, factors contributing to reproductive isolation and modes of genome evolution is a much debated topic in evolutionary biology addressed by various experimental tools. To the best of our knowledge, nobody approached this field using molecular cytogenetics. We examined chromosomes and genomes of one postglacial species pair, sympatric European winter-spawning Coregonus albula and the local endemic dwarf-sized spring-spawning C. fontanae, both originating in Lake Stechlin. We have employed molecular cytogenetic tools to identify the genomic differences between the two species of the sympatric pair on the sub-chromosomal level of resolution.ResultsFluorescence in situ hybridization (FISH) experiments consistently revealed a distinct variation in the copy number of loci of the major ribosomal DNA (the 45S unit) between C. albula and C. fontanae genomes. In C. fontanae, up to 40 chromosomes were identified to bear a part of the major ribosomal DNA, while in C. albula only 8–10 chromosomes possessed these genes. To determine mechanisms how such extensive genome alternation might have arisen, a PCR screening for retrotransposons from genomic DNA of both species was performed. The amplified retrotransposon Rex1 was used as a probe for FISH mapping onto chromosomes of both species. These experiments showed a clear co-localization of the ribosomal DNA and the retrotransposon Rex1 in a pericentromeric region of one or two acrocentric chromosomes in both species.ConclusionWe demonstrated genomic consequences of a rapid ecological speciation on the level undetectable by neither sequence nor karyotype analysis. We provide indirect evidence that ribosomal DNA probably utilized the spreading mechanism of retrotransposons subsequently affecting recombination rates in both genomes, thus, leading to a rapid genome divergence. We attribute these extensive genome re-arrangements associated with speciation event to stress-induced retrotransposons (re)activation. Such causal interplay between genome differentiation, retrotransposons (re)activation and environmental conditions may become a topic to be explored in a broader genomic context in future evolutionary studies.

Reproductive isolation in a nascent species pair is associated with aneuploidy in hybrid offspring

“…However, karyotyping suggests that this is not the case, at least at the whole-chromosome scale as both karyotypes are essentially the same ( figure 1a,b). Yet, our results cannot rule out the possibility that more subtle changes at the [44]. Alternatively, nucleotide divergence among ecotypes may prevent the proper functioning of DNA repair pathways, such as the highly conserved MMR DNA repair pathway [45], and result in meiotic breakdown.…”

Linking maternal and somatic 5S rRNA types with different sequence-specific non-LTR retrotransposons

“…Additionally, the absence and presence of Mutsu retrotransposon RNA and piRNA in eggs, respectively, together with the reversed situation in adult tissue, fuel the need to investigate the obvious link between 5S rRNA and these sequence-specific non-LTR retrotransposons. All of this sparks the notion that the retrotransposon elements are involved in the way the copy numbers evolved in both maternal-and somatic-type 5S rDNA loci (Rebordinos et al 2013), similar to that reported in 45S (Symonová et al 2013).…”

Karyotype analysis of three species of Corydoras (Siluriformes: Callichthyidae) from southern Brazil: rearranged karyotypes and cytotaxonomy

“…1) suggests additional chromosomal pairs bearing 45S rDNA (Oliveira et al, 1993), consistent with the occurrence of rearranged karyotypes. Chromosomal rearrangements, such as inversions, translocations, and transposon-mediated transpositions (Symonová et al, 2013), could explain the diversification of the major rDNA clusters in Corydoras.…”

“…paleatus (Upper Iguaçu and Upper Ribeira rivers) and in C. lacrimostigmata, 5S and 18S rDNA sequences were found to be non-syntenic and on different chromosomes, giving rise to heterokaryotypes due to chromosome rearrangements, such as translocations, inversions, and transpositions. According to Symonová et al (2013), there is evidence to suggest that ribosomal DNA spreading is involved in chromosome rearrangements, thereby affecting recombination rates in both genomes and ultimately leading to a rapid genome divergence. Thus, the detection of the rearranged rDNA chromosome sites is an important source of evidence for mechanisms that could prevent genetic introgression.…”