Abstract

BackgroundIberian Leuciscinae are greatly diverse comprising taxa of hybrid origin. With highly conservative karyotypes, Iberian Chondrostoma s.l. have recently demonstrated sub-chromosomal differentiation and rapid genome restructuring in natural hybrids, which was confirmed by ribosomal DNA (rDNA) transposition and/or multiplication. To understand the role of repetitive DNAs in the differentiation of their genomes, a genetic and molecular cytogenetic survey was conducted in Achondrostoma oligolepis, Anaecypris hispanica, Iberochondrostoma lemmingii, I. lusitanicum, Pseudochondrostoma duriense, P. polylepis, Squalius pyrenaicus and hybrids between A. oligolepis x (P. duriense/P. polylepis), representing ‘alburnine’, chondrostomine and Squalius lineages.ResultsPartial Rex3 sequences evidenced high sequence homology among Leuciscinae (≥98 %) and different fish families (80–95 %) proposing a relatively recent activity of these elements in the species inspected. Low nucleotide substitution rates (<20 %) and intact ORFs suggests that Rex3 may in fact be active in these genomes. The chromosomal distribution of Rex3 retroelement was found highly concentrated at pericentromeric and moderately at subtelomeric blocks, co-localizing with 5S rDNA loci, and correlating with blocks of heterochromatin and C0t-1 DNA. This accumulation was evident in at least 10 chromosome pairs, a pattern that seemed to be shared among the different species, likely pre-dating their divergence. Nevertheless, species-specific clusters were detected in I. lusitanicum, P. duriense, P. polylepis and S. pyrenaicus demonstrating rapid and independent differentiation. Natural hybrids followed the same patterns of accumulation and association with repetitive sequences. An increased number of Rex3 clusters now associating also with translocated 45S rDNA clusters vouched for other genomic rearrangements in hybrids. Rex3 sequence phylogeny did not agree with its hosts’ phylogeny but the observed distribution pattern is congruent with an evolutionary tendency to protect its activity, a robust regulatory system and/or events of horizontal transfer.ConclusionsThis is the first report directed at retroelement physical mapping in Cyprinidae. It helped outlining conceivable ancestral homologies and recognizing retrotransposon activation in hybrids, being possibly associated with genome diversification within the subfamily. The extensive diversity of Iberian Leuciscinae makes them excellent candidates to explore the processes and mechanisms behind the great plasticity distinguishing vertebrate genomes.Electronic supplementary materialThe online version of this article (doi:10.1186/s13039-015-0180-1) contains supplementary material, which is available to authorized users.

Highlights

  • Iberian Leuciscinae are greatly diverse comprising taxa of hybrid origin

  • To understand the role of repetitive DNAs in the genome differentiation of Iberian Leuciscinae, a molecular cytogenetic survey was conducted in species of the ‘alburnine’, chondrostomine and Squalius lineages, namely: Anaecypris hispanica (AHI), Achondrostoma oligolepis (AOL), Iberochondrostoma lemmingii (ILE), I. lusitanicum (ILU), Pseudochondrostoma duriense (PDU), P. polylepis (PPO), Squalius pyrenaicus (SPY) and natural hybrids of the type Achondrostoma oligolepis x P. polylepis and A. oligolepis x P. duriense (Table 1). They were chosen as representatives of the main Iberian Leuciscinae genera and natural hybrids occurring in Portugal [3, 4]. This is the first report directed at retroelement physical mapping in Cyprinidae that may contribute to the understanding of whether retrotransposons might be at the basis of genome rearrangements, karyotype differentiation or even speciation

  • BLASTn megablast analyses confirmed high homology to partial sequences of Rex3 retroelement which were described in the fish families Polypteridae (84–86 %), Cyprinidae (84–91 %), Esocidae (95 %), Adrianichthyidae (84 %), Fundulidae (83 %), Percicthyidae (89 %), Cichlidae (80–86 %), and Tetraodontidae (88 %) (Additional file 1, Fig. 2 and Additional file 2)

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Summary

Introduction

Iberian Chondrostoma s.l. have recently demonstrated sub-chromosomal differentiation and rapid genome restructuring in natural hybrids, which was confirmed by ribosomal DNA (rDNA) transposition and/or multiplication. To understand the role of repetitive DNAs in the differentiation of their genomes, a genetic and molecular cytogenetic survey was conducted in Achondrostoma oligolepis, Anaecypris hispanica, Iberochondrostoma lemmingii, I. lusitanicum, Pseudochondrostoma duriense, P. polylepis, Squalius pyrenaicus and hybrids between A. oligolepis x (P. duriense/P. polylepis), representing ‘alburnine’, chondrostomine and Squalius lineages. In the Iberian Peninsula, Leuciscinae comprise at least 24 species and cases of extensive natural hybridization encompassing both homoploid and polyploid systems (e.g., [3,4,5]). Genomes of homoploid hybrids within Iberian Chondrostoma s.l. are apparently characterized by rapid genetic restructuring often associated with inter-specific hybridization [11] where transposable elements may play an important role (e.g., [12,13,14,15]). Rex elements were first described in the live-bearing fish Xiphophorus maculatus (Poeciliidae) [16] and are currently known to associate with rDNA and with increased karyotype variability in fishes (e.g., [19,20,21,22])

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