Abstract
Polyploidization has played an important role in the evolution of vertebrates, particularly at the base of Teleostei–an enormously successful ray-finned fish group with additional genome doublings on lower taxonomic levels. The investigation of post-polyploid genome dynamics might provide important clues about the evolution and ecology of respective species and can help to decipher the role of polyploidy per se on speciation. Few studies have attempted to investigate the dynamics of repetitive DNA sequences in the post-polyploid genome using molecular cytogenetic tools in fishes, though recent efforts demonstrated their usefulness. The demonstrably monophyletic freshwater loach family Botiidae, branching to evolutionary diploid and tetraploid lineages separated >25 Mya, offers a suited model group for comparing the long-term repetitive DNA evolution. For this, we integrated phylogenetic analyses with cytogenetical survey involving Giemsa- and Chromomycin A3 (CMA3)/DAPI stainings and fluorescence in situ hybridization with 5S/45S rDNA, U2 snDNA and telomeric probes in representative sample of 12 botiid species.The karyotypes of all diploids were composed of 2n = 50 chromosomes, while majority of tetraploids had 2n = 4x = 100, with only subtle interspecific karyotype differences. The exceptional karyotype of Botia dario (2n = 4x = 96) suggested centric fusions behind the 2n reduction. Variable patterns of FISH signals revealed cases of intraspecific polymorphisms, rDNA amplification, variable degree of correspondence with CMA3+ sites and almost no phylogenetic signal. In tetraploids, either additivity or loci gain/loss was recorded. Despite absence of classical interstitial telomeric sites, large blocks of interspersed rDNA/telomeric regions were found in diploids only.We uncovered different molecular drives of studied repetitive DNA classes within botiid genomes as well as the advanced stage of the re-diploidization process in tetraploids. Our results may contribute to link genomic approach with molecular cytogenetic analyses in addressing the origin and mechanism of this polyploidization event.
Highlights
Polyploidization events have played an important role since the early evolution of vertebrates, with a spectacular example of teleostean fishes, where this entire lineage experienced the socalled teleost-specific whole genome duplication (TS-whole-genome duplications (WGDs)) approximately between 226–316 million years ago (Mya) [1], following their divergence from the rest of actinopterygian fishes
The findings from the current study allowed us to reach following conclusions: i) selected cytogenetic markers showed different molecular drives, being in agreement with proposed modes of long-term molecular evolution of tandemly arrayed sequences, ii) the evolution of these markers does not seem to follow the phylogenetic relationships of studied botiids, ii) diploids showed unexpectedly higher dynamics of rDNA phenotypes compared to tetraploids, iii) individual tetraploid genomes followed distinct patterns of genome repatterning, but generally exhibit iv) high degree of rediploidization, with mosaic of diploid and tetraploid genomic regions in all studied polyploids, corroborating the view of already old-aged and rather single WGD event that predated Leptobotiinae/Botiinae divergence, especially with regards to uniformly re-diploidized number of U2 snDNA sites
Our findings point to intense post-polyploid genome dynamics and possible impact of repetitive DNAs on genome divergence
Summary
Polyploidization events have played an important role since the early evolution of vertebrates, with a spectacular example of teleostean fishes, where this entire lineage experienced the socalled teleost-specific whole genome duplication (TS-WGD) approximately between 226–316 million years ago (Mya) [1], following their divergence from the rest of actinopterygian fishes. Polyploidization is usually accompanied by large-scale and genome-wide changes that are extensively complex and include–among others–DNA sequence loss, various chromosome rearrangements, changes in gene expression and epigenetic modifications These processes are acting in a species-specific manner, leading to distinct signs and various extent of post-WGD genome restructuring in order to restore the diploid-like inheritance, to buffer the parental genomes’ incompatibilities and/or to prevent meiotic irregularities Distinct repetitive DNA sequences may undergo either biased elimination, leading in vast majority of cases to the so-called genome downsizing; or they can be amplified and/or accumulated in gene-poor regions These changes are thought to be driven by ectopic (nonallelic) recombination, greatly enhanced by deregulated control of (retro-) transposition activity [20,23,24,25,26]
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