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

Radka Symonová,Petr Ráb,Jörg Freyhof,Georg BO Staaks,Alexandr Sember,Marie Rábová,Zuzana Majtánová,Jörg Bohlen

doi:10.1186/1471-2148-13-42

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.

Highlights

Sympatric species pairs are common in freshwater fishes associated with postglacial lakes in northern temperate environments
We examined chromosomes and genomes of the sympatric species Coregonus albula and C. fontanae in the dimictic Lake Stechlin, northern Germany to test whether the above outlined parallelism on karyotype differentiation in intralacustrine species pairs can be observed in incipient speciation processes in young postglacial lakes
A rapid ecological speciation event with an unclear sympatric scenario, i.e. the derived species C. fontanae fully differentiated from C. albula physiologically, ecologically and morphologically within about 12 – 14 kyrs in the newly colonized Stechlin Lake after the last glacier retreated [15]

Summary

Introduction

Sympatric species pairs are common in freshwater fishes associated with postglacial lakes in northern temperate environments. To assess potential modes of speciation in fishes, numerous model systems are available [2], among which one of the best groups with a robust knowledge on adaptive speciation and complex speciation patterns in postglacial lakes are coregonine fishes (Coregoninae, [3]) [4,5,6] Within coregonines, their numerous sympatric species pairs and recent species flocks [7,8,9] are of particular importance [10]. In Coregonus, based on extensive genetic and population genetic [11], phylogenetic, biogeographic, morphological and eco-physiological data, six potential modes of speciation have been proposed [12] None of these approaches utilized cytogenetic data despite salmonid fishes, to which coregonines belong, being one of the best karyologically studied fish groups in terms of the number of species, populations, individuals and material (adults and embryos) examined. Observed evolution of chromosome number in salmonids is likely affected by selection for increased or decreased genetic recombination rate as proposed by Quimseyh [14], explaining high variability in chromosome numbers in mammals based on fundamental numbers (NF, chromosome arms number)

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Conclusion