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.

Department of Ecology Faculty of Science Charles University Viničná 7 Prague 2 Czech Republic

Laboratory of Fish Genetics Institute of Animal Physiology and Genetics Czech Academy of Sciences Rumburská 89 Liběchov Czech Republic

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Hurley IA, Mueller RL, Dunn KA, Schmidt EJ, Friedman M, Ho RK, et al. A new time-scale for ray-finned fish evolution. Proc R Soc B Biol Sci. 2007;274: 489–498. doi: 10.1098/rspb.2006.3749 PubMed DOI PMC

Braasch I, Postlethwait JH. Polyploidy in fish and the teleost genome duplication In: Soltis PS, Soltis DE, editors. Polyploidy and Genome Evolution. Springer, Berlin; 2012. pp. 341–383.

Sallan LC. Major issues in the origins of ray-finned fish (Actinopterygii) biodiversity. Biol Rev. 2014;89: 950–971. doi: 10.1111/brv.12086 PubMed DOI

Zhan SH, Glick L, Tsigenopoulos CS, Otto SP, Mayrose I. Comparative analysis reveals that polyploidy does not decelerate diversification in fish. J Evol Biol. 2014;27: 391–403. doi: 10.1111/jeb.12308 PubMed DOI

Glasauer SMK, Neuhauss SCF. Whole-genome duplication in teleost fishes and its evolutionary consequences. Mol Genet Genomics. 2014;289: 1045–1060. doi: 10.1007/s00438-014-0889-2 PubMed DOI

Laurent S, Salamin N, Robinson-Rechavi M. No evidence for the radiation time lag model after whole genome duplications in Teleostei. PLoS One. 2017;12: e0176384 doi: 10.1371/journal.pone.0176384 PubMed DOI PMC

Uyeno T, Smith GR. Tetraploid origin of karyotype of catostomid fishes. Science. 1972;175: 644–646. PubMed

Ferris SD, Whitt GS. Genetic variability in species with extensive gene duplication: the tetraploid catostomid fishes. Am Nat. 1980;115: 650–666.

Tsigenopoulos CS, Ráb P, Naran D, Berrebi P. Multiple origins of polyploidy in the phylogeny of southern African barbs (Cyprinidae) as inferred from mtDNA markers. Heredity. 2002;88: 466–473. doi: 10.1038/sj.hdy.6800080 PubMed DOI

Luo J, Gao Y, Ma W, Bi X, Wang S, Wang J, et al. Tempo and mode of recurrent polyploidization in the Carassius auratus species complex (Cypriniformes, Cyprinidae). Heredity. 2014;112: 415–427. doi: 10.1038/hdy.2013.121 PubMed DOI PMC

Schmidt RC, Bart HL Jr. Nomenclatural changes should not be based on equivocally supported phylogenies: reply to Yang et al. 2015. Mol Phylogenet Evol. 2015;90: 193–194. doi: 10.1016/j.ympev.2015.05.025 PubMed DOI

Yang L, Sado T, Hirt MV, Pasco-Viel E, Arunachalam M, Li J, et al. Phylogeny and polyploidy: resolving the classification of cyprinine fishes (Teleostei: Cypriniformes). Mol Phylogenet Evol. 2015;85: 97–116. doi: 10.1016/j.ympev.2015.01.014 PubMed DOI

Wang X, Gan X, Li J, Chen Y, He S. Cyprininae phylogeny revealed independent origins of the Tibetan Plateau endemic polyploid cyprinids and their diversifications related to the Neogene uplift of the plateau. Science China–Life Sciences 2016;59: 1149–1165. doi: 10.1007/s11427-016-0007-7 PubMed DOI

Saitoh K, Chen W-J, Mayden RL. Extensive hybridization and tetrapolyploidy in spined loach fish. Mol Phylogenet Evol. 2010;56: 1001–1010. doi: 10.1016/j.ympev.2010.04.021 PubMed DOI

Marburger S, Alexandrou MA, Taggart JB, Creer S, Carvalho G, Oliveira C, et al. Whole genome duplication and transposable element proliferation drive genome expansion in Corydoradinae catfishes. Proc R Soc B. 2018;285: 20172732 doi: 10.1098/rspb.2017.2732 PubMed DOI PMC

Macqueen DJ, Johnston IA. A well-constrained estimate for the timing of the salmonid whole genome duplication reveals major decoupling from species diversification. Proc Biol Sci. 2014;281: 20132881 doi: 10.1098/rspb.2013.2881 PubMed DOI PMC

Wolfe KH. Yesterday’s polyploids and the mystery of diploidization. Nat Rev Genet. 2001;2: 333–341. doi: 10.1038/35072009 PubMed DOI

Comai L. The advantages and disadvantages of being polyploid. Nat Rev Genet. 2005;6: 836–846. doi: 10.1038/nrg1711 PubMed DOI

Parisod C, Holderegger R, Brochmann C. Evolutionary consequences of autopolyploidy. New Phytol. 2010;186: 5–17. doi: 10.1111/j.1469-8137.2009.03142.x PubMed DOI

Tyalé A, Parisod C. Natural pathways to polyploidy in plants and consequences for genome reorganization. Cytogenet Genome Res. 2013;140: 79–96. doi: 10.1159/000351318 PubMed DOI

Wertheim B, Beukeboom LW, van de Zande L. Polyploidy in animals: effects of gene expression on sex determination, evolution and ecology. Cytogenet Genome Res. 2013;140: 256–269. doi: 10.1159/000351998 PubMed DOI

Soltis DE, Visger CJ, Blaine Marchant D, Soltis PS. Polyploidy: pitfalls and paths to a paradigm. Am J Bot. 2016;103: 1146–1166. doi: 10.3732/ajb.1500501 PubMed DOI

Ma XF, Gustafson JP. Genome evolution of allopolyploids: a process of cytological and genetic diploidization. Cytogenet Genome Res. 2005;109: 236–249. doi: 10.1159/000082406 PubMed DOI

Leitch IJ, Hanson L, Lim KY, Kovarik A, Chase MW, Clarkson JJ, et al. The ups and downs of genome size evolution in polyploid species of Nicotiana (Solanaceae). Ann Bot. 2008;101: 805–814. doi: 10.1093/aob/mcm326 PubMed DOI PMC

Leitch IJ, Bennett MD. Genome downsizing in polyploid plants. Bot J Linn Soc. 2004;82: 651–663. doi: 10.1111/j.1095-8312.2004.00349.x DOI

Parisod C, Alix K, Just J, Petit M, Sarilar V, Ainouche M, et al. Impact of transposable elements on the organization and function of allopolyploid genomes. New Phytol. 2010;186: 37–45. doi: 10.1111/j.1469-8137.2009.03096.x PubMed DOI

Gromicho M, Coutanceau J-P, Ozouf-Costaz C, Collares-Pereira MJ. Contrast between extensive variation of 28S rDNA and stability of 5S rDNA and telomeric repeats in the diploid-polyploid Squalius alburnoides complex and in its maternal ancestor Squalius pyrenaicus (Teleostei, Cyprinidae). Chromosome Res. 2006;14: 297–306. doi: 10.1007/s10577-006-1047-4 PubMed DOI

Zhu HP, Ma DM, Gui JF. Triploid origin of the gibel carp as revealed by 5S rDNA localization and chromosome painting. Chromosome Res. 2006;14: 767–776. doi: 10.1007/s10577-006-1083-0 PubMed DOI

He W, Qin Q, Liu S, Li T, Wang J, Xiao J, et al. Organization and variation analysis of 5S rDNA in different ploidy-level hybrids of red crucian carp x topmouth culter. PLoS One. 2012;7: 27–37. doi: 10.1371/journal.pone.0038976 PubMed DOI PMC

Spóz A, Boroń A, Porycka K, Karolewska M, Ito D, Abe S, et al. Molecular cytogenetic analysis of the crucian carp, Carassius carassius (Linnaeus, 1758) (Teleostei, Cyprinidae), using chromosome staining and fluorescence in situ hybridisation with rDNA probes. Comp Cytogenet. 2014;8: 233–248. doi: 10.3897/CompCytogen.v8i3.7718 PubMed DOI PMC

Maneechot N, Yano CF, Bertollo LAC, Getlekha N, Molina WF, Ditcharoen S, et al. Genomic organization of repetitive DNAs highlights chromosomal evolution in the genus Clarias (Clariidae, Siluriformes). Mol Cytogenet. 2016;9: 4 doi: 10.1186/s13039-016-0215-2 PubMed DOI PMC

Ye L, Zhang C, Tang X, Chen Y, Liu S. Variations in 5S rDNAs in diploid and tetraploid offspring of red crucian carp × common carp. BMC Genet. 2017;18: 75 doi: 10.1186/s12863-017-0542-2 PubMed DOI PMC

Knytl M, Kalous L, Rylková K, Choleva L, Merilä J, Ráb P. Morphologically indistinguishable hybrid Carassius female with 156 chromosomes: a threat for the threatened crucian carp, C. carassius, L. PLoS One. 2018;13: e0190924 doi: 10.1371/journal.pone.0190924 PubMed DOI PMC

Flajšhans M, Ráb P, Dobosz S. Frequency analyses of active NORs in nuclei of artificially induced triploid fishes. Theor Appl Genet. 85: 68–72. doi: 10.1007/BF00223846 PubMed DOI

Romanenko SA, Biltueva LS, Serdyukova NA, Kulemzina A, Beklemisheva VR, Gladkikh, et al. Segmental paleotetraploidy revealed in sterlet (Acipenser ruthenus) genome by chromosome painting. Mol Cytogenet. 2015;8: 90 doi: 10.1186/s13039-015-0194-8 PubMed DOI PMC

Andreyushkova A, Makunin AI, Beklemisheva VR, Romanenko SA, Druzhkova AS, Biltueva LB, et al. Next generation sequencing of chromosome-specific libraries sheds light on genome evolution in paleotetraploid sterlet (Acipenser ruthenus). Genes. 2017;8: 318 doi: 10.3390/genes8110318 PubMed DOI PMC

Biltueva LS, Prokopov DY, Makunin AI, Komissarov AS, Kudryavtseva AV, Lemskaya NA, et al. Genomic organization and physical mapping of tandemly arranged repetitive DNAs in sterlet (Acipenser ruthenus). Cytogenet Genome Res. 2017;152: 148–157. doi: 10.1159/000479472 PubMed DOI

Symonová R, Havelka M, Amemiya CT, Howell WM, Kořínková T, Flajšhans M, et al. Molecular cytogenetic differentiation of paralogs of Hox paralogs in duplicated and re-diploidized genome of the North American paddlefish (Polyodon spathula). BMC Genet. 2017;18: 19 doi: 10.1186/s12863-017-0484-8 PubMed DOI PMC

Kottelat M. Conspectus Cobitidum: an inventory of loaches of the world (Teleostei: Cypriniformes: Cobitoidei). Raffles Bull Zool. 2012; Suppl 26:1–199.

Eschmeyer WN, Fricke R, van der Laan R, editors. Catalog of Fishes: Genera, Species, References. [cited 2017 Nov 28]. Available from: http://researcharchive.calacademy.org/research/ichthyology/catalog/fishcatmain.asp

Tang Q, Xiong B, Yang X, Liu H. Phylogeny of the East Asian botiine loaches (Cypriniformes, Botiidae) inferred from mitochondrial cytochrome b gene sequences. Hydrobiologia. 2005;544: 249–258. doi: 10.1007/s10750-005-0863-4 DOI

Šlechtová V, Bohlen J, Freyhof J, Ráb P. Molecular phylogeny of the Southeast Asian freshwater fish family Botiidae (Teleostei: Cobitoidea) and the origin of polyploidy in their evolution. Mol Phylogenet Evol. 2006;39: 529–541. doi: 10.1016/j.ympev.2005.09.018 PubMed DOI

Bohlen J, Šlechtová V. Phylogenetic position of the fish genus Ellopostoma (Teleostei: Cypriniformes) using molecular genetic data. Ichthyol Explor Freshw. 2009; 20: 157–162.

Arai R. Fish karyotypes: a check list 1st ed. Tokyo: Springer; 2011.

Clift PD, Blusztajn J, Nguyen AD. Large-scale drainage capture and surface uplift in eastern Tibet–SW China before 24 MA inferred from sediments of the Hanoi Basin, Vietnam. Geophys Res Lett. 2006;33: L19403 doi: 10.1029/2006GL027772 DOI

Ali JR, Aitkinson JC. Gondwana to Asia: plate tectonics, paleogeography and the biological connectivity of the Indian sub-continent from the Middle Jurassic through latest Eocene (166–35 Ma). Earth Sci Rev. 2008;88: 145–166. doi: 10.1016/j.earscirev.2008.01.007 DOI

Yue X, Zou Y, Liu J, Wang Y, Wang F, Xie B, et al. Chromosome karyotype of Sinibotia superciliaris. Sichuan Journal of Zoology. 2013;3: 017.

Kaewmad P, Monthatong M, Supiwong W, Saowakoon S, Tanomtong A. Natural autotetraploid and chromosomal characteristics in the subfamily Botiinae (Cypriniformes, Cobitinae) from Northeast Thailand. Cytologia. 2014;79: 299–313. doi: 10.1508/cytologia.79.299 DOI

Bohlen J, Šlechtová V, Šlechta V, Šlechtová V, Sember A, Ráb P. A ploidy difference represents an impassable barrier for hybridisation in animals. Is there an exception among botiid loaches (Teleostei: Botiidae)? PLoS One. 2016;11: e0159311 doi: 10.1371/journal.pone.0159311 PubMed DOI PMC

Boroń A, Ozouf-Costaz C, Coutanceau J-P, Woroniecka K. Gene mapping of 28S and 5S rDNA sites in the spined loach Cobitis taenia (Pisces, Cobitidae) from a diploid population and a diploid-tetraploid population. Genetica. 2006;128: 71–79. doi: 10.1007/s10709-005-5536-8 PubMed DOI

Li YJ, Tian Y, Zhang MZ, Tian PP, Yu Z, Abe S, et al. Chromosome banding and FISH with rDNA in the diploid and tetraploid loach Misgurnus anguillicaudatus. Ichthyol Res. 2010;57: 358–366. doi: 10.1007/s10228-010-0168-0 DOI

Kirtiklis L, Grabowska A, Bazyłyna E, Orzechowska A, Skórczyńska M, Boroń A. Gene mapping of 28S rDNA sites in allotriploid Cobitis females (Pisces: Cobitidae) from a diploid-polyploid population. Biologia (Bratisl). 2014;69: 536–540. doi: 10.2478/s11756-014-0339-y DOI

Sember A, Bohlen J, Šlechtová V, Altmanová M, Symonová R, Ráb P. Karyotype differentiation in 19 species of river loach fishes (Nemacheilidae, Teleostei): extensive variability associated with rDNA and heterochromatin distribution and its phylogenetic and ecological interpretation. BMC Evol Biol. 2015;15: 251 doi: 10.1186/s12862-015-0532-9 PubMed DOI PMC

Majtánová Z, Choleva L, Symonová R, Ráb P, Kotusz J, Pekárik L, et al. Asexual reproduction does not apparently increase the rate of chromosomal evolution: karyotype stability in diploid and triploid clonal hybrid fish (Cobitis, Cypriniformes, Teleostei). PLoS One. 2016;11: 1–18. doi: 10.1371/journal.pone.0146872 PubMed DOI PMC

Spóz A, Boroń A, Ocalewicz K, Kirtiklis L. Polymorphism of the rDNA chromosomal regions in the weatherfish Misgurnus fossilis (Teleostei: Cobitidae). Folia Biol. 2017;65: 63–70. doi: 10.3409/fb65_1.63 DOI

Völker M, Ráb P. Direct chromosome preparation from regenerating fin tissue In: Ozouf-Costaz C, Pisano E, Foresti F, de Almeida Toledo LF, editors. Fish cytogenetic techniques: ray-fin fishes and chondrichthyans. Enfield: CRC Press, Inc.; 2015. pp. 37–41.

Symonová R, Majtánová Z, Sember A, Staaks GBO, Bohlen J, Freyhof J, et al. Genome differentiation in a species pair of coregonine fishes: an extremely rapid speciation driven by stress-activated retrotransposons mediating extensive ribosomal DNA multiplications. BMC Evol Biol. 2013;13: 42 doi: 10.1186/1471-2148-13-42 PubMed DOI PMC

Fujiwara A, Nishida-Umehara C, Sakamoto T, Okamoto N, Nakayama I, Abe S. Improved fish lymphocyte culture for chromosome preparation. Genetica. 2001;111: 77–89. doi: 10.1023/A:1013788626712 PubMed DOI

Symonová R, Flajšhans M, Sember A, Havelka M, Gela D, Kořínková T, et al. Molecular cytogenetics in artificial hybrid and highly polyploid sturgeons: an evolutionary story narrated by repetitive sequences. Cytogenet Genome Res. 2013;141: 153–162. doi: 10.1159/000354882 PubMed DOI

Levan A, Fredga K, Sandberg AA. Nomenclature for centromeric position on chromosomes. Hereditas. 1964;52: 201–220. doi: 10.1111/j.1601-5223.1964.tb01953.x DOI

Mayr B, Ráb P, Kalat M. Localisation of NORs and counterstain-enhanced fluorescence studies in Perca fluviatilis (Pisces, Percidae). Genetica. 1985;67: 51–56. doi: 10.1007/BF02424460 PubMed DOI

Sola L, Rossi AR, Iaselli V, Rasch EM, Monaco PJ. Cytogenetics of bisexual/unisexual species of Poecilia. II. Analysis of heterochromatin and nucleolar organizer regions in Poecilia mexicana mexicana by C-banding and DAPI, quinacrine, chromomycin A3, and silver staining. Cytogenet Cell Genet. 1992;60: 229–235. doi: 10.1159/000133346 PubMed DOI

Graham DE. The isolation of high molecular weight DNA from whole organisms or large tissue masses. Anal Biochem. 1978;85: 609–613. doi: 10.1016/0003-2697(78)90262-2 PubMed DOI

Bueno D, Palacios-Gimenez OM, Cabral-de-Mello DC. Chromosomal mapping of repetitive DNAs in the grasshopper Abracris flavolineata reveal possible ancestry of the B chromosome and H3 histone spreading. PLoS One. 2013;8 doi: 10.1371/journal.pone.0066532 PubMed DOI PMC

Scacchetti PC, Utsunomia R, Pansonato-Alves JC, da Costa Silva GJ, Vicari MR, Artoni RF, et al. Repetitive DNA sequences and evolution of ZZ/ZW sex chromosomes in Characidium (Teleostei: Characiformes). PLoS One. 2015;10: e0137231 doi: 10.1371/journal.pone.0137231 PubMed DOI PMC

Hall TA. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/96/NT. Nucleic Acids Res. 1999;41: 95–8. Available from: http://www.mbio.ncsu.edu/BioEdit/bioedit.html.

Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. J Mol Biol. 1990;215: 403–10. Available from: http://blast.ncbi.nlm.nih.gov/blast. doi: 10.1016/S0022-2836(05)80360-2 PubMed DOI

Fuková I, Nguyen P, Marec F. Codling moth cytogenetics: karyotype, chromosomal location of rDNA, and molecular differentiation of sex chromosomes. Genome. 2005;48: 1083–1092. doi: 10.1139/g05-063 PubMed DOI

Šlechtová V, Bohlen J, Tan HH. Families of Cobitoidea (Teleostei; Cypriniformes) as revealed from nuclear genetic data and the position of the mysterious genera Barbucca, Psilorhynchus, Serpenticobitis and Vaillantella. Mol Phylogenet Evol. 2007;44: 1358–1365. doi: 10.1016/j.ympev.2007.02.019 PubMed DOI

Chen W-J, Miya M, Saitoh K, Mayden RL. Phylogenetic utility of two existing and four novel nuclear gene loci in reconstructing Tree of Life of ray-finned fishes: the order Cypriniformes (Ostariophysi) as a case study. Gene. 2008;423: 125–134. doi: 10.1016/j.gene.2008.07.016 PubMed DOI

Ronquist F, Huelsenbeck JP. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics. 2003;19: 1572–1574. doi: 10.1093/bioinformatics/btg180 PubMed DOI

Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol. 2011;28, 2731–2739. doi: 10.1093/molbev/msr121 PubMed DOI PMC

Sawada Y. Chromosomes of Leptobotia curta (Cobitidae, Cypriniformes). Jpn J Icthyol. 1976;23: 175–177. doi: 10.11369/jji1950.23.175 DOI

Suzuki A, Taki Y. Tetraploidization in the cobitid subfamily Botinae (Pisces, Cypriniformes). Cytobios, 1996;85: 229–245.

Yu XJ, Zhou T, Li YC, Li K, Zhou M. Chromosomes of Chinese freshwater fishes Beijing: Science Press; (In Chinese); 1989.

Rishi KK, Haobam MS. Karyotypes of three forms of fishes having high chromosome number. Intl J Acad Ichthyol. 1984;5: 139–144.

Khuda-Bukhsh AR, Chanda T, Barat A. Karyomorphology and evolution in some Indian hillstream fishes with particular reference to polyploidy in some species In: Uyeno T, Arai R, Taniuchi T, Matsuura K, editors. Indo-Pacifific fifish biology. Tokyo: Ichthyological Society of Japan; 1986. pp. 886–898.

Ráb P, Slavík O. Diploid-triploid-tetraploid complex of the spined loach, genus Cobitis in Pšovka Creek: the first evidence of new species of Cobitis in the ichthyofauna of Czech Republic. Acta Univ Carolinae Biol (O. Oliva memorial issue), 1996; 39: 201–214.

Ayata MK, Unal S, Gaffaroglu M. Chromosomal analysis of Oxynoemacheilus atili Erk´akan, 2012 (Teleostei, Nemacheilidae). Turk J Fish Aquat Sci. 2018;18: 991–994. doi: 10.4194/1303-2712-v18_8_07 DOI

Bohlen J, Völker M, Rábová M, Ráb P. Note on the banded karyotype of the enigmatic South Asian loach Vaillantella maassi (Cypriniformes: Vaillantellidae). Ichthyol Res. 2008;55: 82–84. doi: 10.1007/s10228-007-0007-0 DOI

Betancur-R R, Wiley EO, Arratia G, Acero A, Bailly N, Miya M, et al. Phylogenetic classification of bony fishes. BMC Evol Biol. 2017;17: 162 doi: 10.1186/s12862-017-0958-3 PubMed DOI PMC

Winterfeld G, Schneider J, Röser M. Allopolyploid origin of Mediterranean species in Helictotrichon (Poaceae) and its consequences for karyotype repatterning and homogenisation of rDNA repeat units. Syst Biodivers. 2009;7: 277–295. doi: 10.1017/S1477200009003041 DOI

Rocchi M, Archidiacono N, Schempp W, Capozzi O, Stanyon R. Centromere repositioning in mammals. Heredity. 2012;108: 59–67. doi: 10.1038/hdy.2011.101 PubMed DOI PMC

Hoffmann AA, Rieseberg LH. Revisiting the impact of inversions in evolution: from population genetic markers to drivers of adaptive shifts and speciation? Annu Rev Ecol Evol Syst. 2008;39: 21–42. doi: 10.1146/annurev.ecolsys.39.110707.173532 PubMed DOI PMC

Feulner PGD, De-Kayne R. Genome evolution, structural rearrangements and speciation. J Evol Biol. 2017;30: 1488–1490. doi: 10.1111/jeb.13101 PubMed DOI

Jones FC, Grabherr MG, Chan YF, Russell P, Mauceli E, Johnson J, et al. The genomic basis of adaptive evolution in threespine sticklebacks. Nature. 2012;484: 55–61. doi: 10.1038/nature10944 PubMed DOI PMC

Pucci MB, Barbosa P, Nogaroto V, Almeida MC, Artoni RF, Pansonato-Alves JV, et al. Population differentiation and speciation in the genus Characidium (Characiformes: Crenuchidae): effects of reproductive and chromosomal barriers. Biol J Linn Soc. 2014;111: 541–553. doi: 10.1111/bij.12218 DOI

Takagui FH, Venturelli NB, Dias AL, Swarca AC, Vicari MR, Fenocchio AS, et al. The importance of pericentric inversions in the karyotypic diversification of the species Loricariichthys anus and Loricariichthys platymetopon. Zebrafish. 2014;11: 300–305. doi: 10.1089/zeb.2014.0985 PubMed DOI

Getlekha N, Cioffi MB, Maneechot N, Bertollo LAC, Supiwong W, Tanomtong A, et al. Contrasting evolutionary paths among Indo-Pacific Pomacentrus species promoted by extensive pericentric inversions and genome organization of repetitive sequences. Zebrafish. 2017;15 45–54. doi: 10.1089/zeb.2017.1484 PubMed DOI

Wang X, Paterson AH. Gene conversion in angiosperm genomes with an emphasis on genes duplicated by polyploidization. Genes. 2011;2: 1–20. doi: 10.3390/genes2010001 PubMed DOI PMC

Lien S, Koop BF, Sandve SR, Miller JR, Kent MP, Nome T, et al. The Atlantic salmon genome provides insights into rediploidization. Nature. 2016;533: 200–205. doi: 10.1038/nature17164 PubMed DOI PMC

Schmid M, Guttenbach M. Evolutionary diversity of reverse (R) fluorescent chromosome bands in vertebrates. Chromosoma. 1988;97: 101–114. doi: 10.1007/BF00327367 PubMed DOI

Ráb P, Rábová M, Reed KM, Phillips RB. Chromosomal characteristics of ribosomal DNA in the primitive semionotiform fish, longnose gar Lepisosteus osseus. Chromosome Res. 1999;7: 475–480. doi: 10.1023/A:1009202030456 PubMed DOI

Ráb P, Rábová M, Bohlen J, Lusk S. Genetic differentiation of the two hybrid diploid–polyploid complexes of loaches, genus Cobitis (Cobitidae) involving C. taenia, C. elongatoides and C. sp. in the Czech Republic: karyotypes and cytogenetic diversity. Folia Zool. 2000; 49(Suppl. 1): 55–66.

Rábová M, Ráb P, Ozouf-Costaz C. Extensive polymorphism and chromosomal characteristics of ribosomal DNA in a loach fish, Cobitis vardarensis (Ostariophysi, Cobitidae) detected by different banding techniques and fluorescence in situ hybridization (FISH). Genetica. 2001;111: 413–422. doi: 10.1023/A:1013763903513 PubMed DOI

Rábová M, Ráb P, Boroń A, Bohlen J, Janko K, Šlechtová V, et al. Cytogenetics of bisexual species and their asexual hybrid clones in European spined loaches, genus Cobitis. I. Karyotypes and extensive polymorphism of major ribosomal sites in four parental species. Abstracts of 16th European Colloqium on Animal Cytogenetics and Gene Mapping. Cytogenet Genome Res. 2004;106: 16

Ráb P, Crossman EJ, Reed KM, Rábová M. Chromosomal characteristics of ribosomal DNA in two extant species of North American mudminnows Umbra pygmaea and U. limi (Euteleostei: Umbridae). Cytogenet Genome Res. 2002;98: 194–198. doi: 10.1159/000069800 PubMed DOI

Śliwińska-Jewsiewicka A, Kuciński M, Kirtiklis L, Dobosz S, Ocalewicz K, Jankun M. Chromosomal characteristics and distribution of rDNA sequences in the brook trout Salvelinus fontinalis (Mitchill, 1814). Genetica. 2015;143: 425–432. doi: 10.1007/s10709-015-9841-6 PubMed DOI PMC

de Oliveira EA, Bertollo LAC, Yano CF, Liehr T, Cioffi MB. Comparative cytogenetics in the genus Hoplias (Characiformes, Erythrinidae) highlights contrasting karyotype evolution among congeneric species. Mol Cytogenet. 2015;8: 56 doi: 10.1186/s13039-015-0161-4 PubMed DOI PMC

Coluccia E, Deiana AM, Cau A, Cannas R, Tagliavini J, Libertini A, et al. Karyotype analysis of the pumpkinseed Lepomis gibbosus (Actinopterygii, Centrarchidae) by chromosomal banding and in situ hybridization. J Appl Ichthyol. 2010;26: 445–448. doi: 10.1111/j.1439-0426.2009.01384.x DOI

Cabral-de-Mello D, Martins C. Breaking down the genome organization and karyotype differentiation through the epifluorescence microscope lens: insects and fish as models In: Méndez-Vilas A, Díaz J, editors. Microscopy: Science, Technology, Application and Education. Formatex Microscopy No. 4, vol. 1 Badajoz: Formatex Research Center; 2010. pp. 658–669.

Cioffi MB, Bertollo LAC. Chromosomal distribution and evolution of repetitive DNAs in fish In: Garrido-Ramos MA, editor. Repetitive DNA. Genome Dyn, vol. 7 Basel: Karger; 2012. pp. 197–221. PubMed

Symonová R, Howell WM. Vertebrate genome evolution in the light of fish cytogenomics and rDNAomics. Genes. 2018;9: 96 doi: 10.3390/genes9020096 PubMed DOI PMC

Gornung E. Twenty years of physical mapping of major ribosomal RNA genes across the teleosts: a review of research. Cytogenet Genome Res. 2013;141: 90–102. doi: 10.1159/000354832 PubMed DOI

Yano CF, Bertollo LAC, Rebordinos L, Merlo MA, Liehr T, Portela-Bens S. Evolutionary dynamics of rDNAs and U2 small nuclear DNAs in Triportheus (Characiformes, Triportheidae): high variability and particular syntenic organization. Zebrafish. 2017;14: 146–154. doi: 10.1089/zeb.2016.1351 PubMed DOI

Sochorová J, Garcia S, Gálvez F, Symonová R, Kovařík A. Evolutionary trends in animal ribosomal DNA loci: introduction to a new online database. Chromosoma. 2018; 127: 141–150. doi: 10.1007/s00412-017-0651-8 PubMed DOI PMC

Rebordinos L, Cross I, Merlo A. High evolutionary dynamism in 5S rDNA of fish: state of the art. Cytogenet Genome Res. 2013;141: 103–113. doi: 10.1159/000354871 PubMed DOI

Pereira CSA, Ráb P, Collares-Pereira MJ. Chromosomes of Iberian leuciscinae (Cyprinidae) revisited: evidence of genome restructuring in homoploid hybrids using dual-color fish and CGH. Cytogenet Genome Res. 2013;141: 143–152. doi: 10.1159/000354582 PubMed DOI

Fernandes CA, Paiz LM, Baumgärtner L, Margarido VP, Vieira MMR. Comparative cytogenetics of the black ghost knifefish (Gymnotiformes: Apteronotidae): evidence of chromosomal fusion and pericentric inversions in karyotypes of two Apteronotus species. Zebrafish. 2017;14:471–476. doi: 10.1089/zeb.2017.1432 PubMed DOI

Porto-Foresti F, Oliveira C, Gomes EA, Tabata YA, Rigolino MG, Foresti F. A lethal effect associated with polymorphism of the NOR-bearing chromosomes in rainbow trout (Oncorhynchus mykiss). Genet Mol Biol. 2004;27: 51–54. doi: 10.1590/S1415-47572004000100009 DOI

Amorim KDJ, Cioffi MB, Bertollo LAC, Soares RX, de Souza AS, Costa GWWF, et al. Co-located 18S/5S rDNA arrays: an ancient and unusual chromosomal trait in Julidini species (Labridae, Perciformes). Comp Cytogenet. 2016;10: 555.–. doi: 10.3897/CompCytogen.v10i4.10227 PubMed DOI PMC

Ghigliotti L, Near TJ, Ferrando S, Vacchi M, Pisano E. Cytogenetic diversity in the Antarctic plunderfishes (Notothenioidei: Artedidraconidae). Antarct Sci. 2010;22: 805–814. doi: 10.1017/S0954102010000660 DOI

Collares-Pereira MJ, Ráb P. NOR polymorphism in the Iberian species Chondrostoma lusitanicum (Pisces: Cyprinidae)–re-examination by FISH. Genetica. 1999;105: 301–303. doi: 10.1023/A:1003885922023 PubMed DOI

Nirchio M, Rondón R, Oliveira C, Ferreira IA, Martins C, Pérez J, et al. Cytogenetic studies in three species of Lutjanus (Perciformes: Lutjanidae: Lutjaninae) from the Isla Margarita, Venezuela. Neotrop Ichthyol. 2008;6: 101–108. doi: 10.1590/S1679-62252008000100012 DOI

Symonová R, Ocalewicz K, Kirtiklis L, Delmastro GB, Pelikánová Š, Garcia S, et al. Higher-order organisation of extremely amplified, potentially functional and massively methylated 5S rDNA in European pikes (Esox sp.). BMC Genomics. 2017;18: 391 doi: 10.1186/s12864-017-3774-7 PubMed DOI PMC

Nguyen P, Sahara K, Yoshido A, Marec F. Evolutionary dynamics of rDNA clusters on chromosomes of moths and butterflies (Lepidoptera). Genetica. 2010;138: 343–354. doi: 10.1007/s10709-009-9424-5 PubMed DOI

Cazaux B, Catalan J, Veyrunes F, Douzery EJ, Britton-Davidian J. Are ribosomal DNA clusters rearrangement hotspots? A case study in the genus Mus (Rodentia, Muridae). BMC Evol Biol. 2011;11: 124 doi: 10.1186/1471-2148-11-124 PubMed DOI PMC

Nakajima RT, Cabral-de-Mello DC, Valente GT, Venere PC, Martins C. Evolutionary dynamics of rRNA gene clusters in cichlid fish. BMC Evol Biol. 2012;12: 198 doi: 10.1186/1471-2148-12-198 PubMed DOI PMC

da Silva M, Barbosa P, Artoni RF, Feldberg E. Evolutionary dynamics of 5S rDNA and recurrent association of transposable elements in electric fish of the family Gymnotidae (Gymnotiformes): the case of Gymnotus mamiraua. Cytogenet Genome Res. 2016:149: 297–303. doi: 10.1159/000449431 PubMed DOI

de Moraes RLR, Bertollo LAC, Marinho MMF, Yano CF, Hatanaka T, Barby FF, et al. Evolutionary relationships and cytotaxonomy considerations in the genus Pyrrhulina (Characiformes, Lebiasinidae). Zebrafish. 2017;14: 536–546. doi: 10.1089/zeb.2017.1465 PubMed DOI

Wahl MC, Will CL, Lűhrmann R. The spliceosome: design principles of a dynamic RNP machine. Cell. 2009;136: 701–718. doi: 10.1016/j.cell.2009.02.009 PubMed DOI

Papasaikas P, Valcárcel J. The spliceosome: the ultimate RNA chaperone and sculptor. Trends Biochem Sci. 2016;41: 33–45. doi: 10.1016/j.tibs.2015.11.003 PubMed DOI

Piscor D, Centofante L, Parise-Maltempi PP. Highly similar morphologies between chromosomes bearing U2 snRNA gene clusters in the group Astyanax Baird and Girard, 1854 (Characiformes, Characidae): an evolutionary approach in species with 2n  =  36, 46, 48, and 50. Zebrafish. 2016;13: 565–570. doi: 10.1089/zeb.2016.1292 PubMed DOI

Ráb P, Yano CF, Lavoue S, Jegede OI, Bertollo LAC, Ezaz T, et al. Karyotype and mapping of repetitive DNAs in the african butterfly fish Pantodon buchholzi, the sole species of the family Pantodontidae. Cytogenet Genome Res. 2016;149: 312–320. doi: 10.1159/000450534 PubMed DOI

Araya-Jaime C, Mateussi NTB, Utsunomia R, Costa-Silva GJ, Oliveira C, Foresti F. ZZ/Z0: the new system of sex chromosomes in Eigenmannia aff. trilineata (Teleostei: Gymnotiformes: Sternopygidae) characterized by molecular cytogenetics and DNA barcoding. Zebrafish. 2017;14: 464–470. doi: 10.1089/zeb.2017.1422 PubMed DOI

Eickbush TH, Eickbush DG. Finely orchestrated movements: evolution of the ribosomal RNA genes. Genetics. 2007;175: 477–485. doi: 10.1534/genetics.107.071399 PubMed DOI PMC

Nieto Feliner G, Rossello JA. Concerted evolution of multigene families and homeologous recombination In: Wendel J, Greilhuber J, Doležel J, Leitch IJ, editors. Plant genome diversity, vol. 1 Wien: Springer; 2012. pp. 171–94.

Volkov RA, Komarova NY, Hemleben V. Ribosomal RNA in plant hybrids: inheritance, rearrangement, expression. Syst Biodivers. 2007;5: 261–276. doi: 10.1017/S1477200007002447 DOI

Chairi H, Rebordinos Gonzalez L. Structure and organization of the Engraulidae family U2 snRNA: an evolutionary model gene? J Mol Evol. 2015;80: 209–218. doi: 10.1007/s00239-015-9674-z PubMed DOI

Barman AS, Singh M, Singh RK, Lal KK. Evidence of birth-and-death evolution of 5S rRNA gene in Channa species (Teleostei, Perciformes). Genetica. 2016;144: 723–732. doi: 10.1007/s10709-016-9938-6 PubMed DOI

Ruiz-Herrera A, Nergadze SG, Santagostino M, Giulotto E. Telomeric repeats far from the ends: mechanisms of origin and role in evolution. Cytogenet Genome Res. 2008;122: 219–228. doi: 10.1159/000167807 PubMed DOI

Ocalewicz K. Telomeres in fishes. Cytogenet Genome Res. 2013;141: 114–125. doi: 10.1159/000354278 PubMed DOI

Machado MA, Cardoso AL, Milhomem-Paixão SSR, Pieczarka JC, Nagamachi CY. Gymnotus coatesi (Gymnotiformes): a case of colocation of multiple sites of 18S rDNA with telomeric sequences. Zebrafish. 2017;14: 459–463. doi: 10.1089/zeb.2017.1435 PubMed DOI

de Sousa JFS, Viana PF, Bertollo LAC, Cioffi MB, Feldberg E. Evolutionary relationships among Boulengerella species (Ctenoluciidae, Characiformes): genomic organization of repetitive DNAs and highly conserved karyotypes. Cytogenet Genome Res. 2017;152: 194–203. doi: 10.1159/000480141 PubMed DOI

Zhdanova NS, Minina JM, Karamisheva TV, Draskovic I, Rubtsov NB, Londoño-Vallejo JA. The very long telomeres in Sorex granarius (Soricidae, Eulipothyphla) contain ribosomal DNA. Chromosome Res. 2007;15: 881–890. doi: 10.1007/s10577-007-1170-x PubMed DOI

Li J, He S, Zhang L, Hu Y, Yang F, Ma L, et al. Telomere and 45S rDNA sequences are structurally linked on the chromosomes in Chrysanthemum segetum L. Protoplasma. 2012;249: 207–215. doi: 10.1007/s00709-011-0279-0 PubMed DOI

Scali V, Coluccia E, Deidda F, Lobina C, Deiana AM, Salvadori S. Co-localization of ribosomal and telomeric sequences in Leptynia (Insecta: Phasmatodea). Ital J Zool. 2016;83: 285–290. doi: 10.1080/11250003.2016.1219403 DOI

Stimpson KM, Sullivan LL, Kuo ME, Sullivan BA. Nucleolar organization, ribosomal DNA array stability, and acrocentric chromosome integrity are linked to telomere function. PLoS One. 2014;9: e92432 doi: 10.1371/journal.pone.0092432 PubMed DOI PMC

Guillén AKZ, Hirai Y, Tanoue T, Hirai H. Transcriptional repression mechanisms of nucleolus organizer regions (NORs) in humans and chimpanzees. Chromosome Res. 2004;12: 225–237. doi: 10.1023/B:CHRO.0000021911.43225.eb PubMed DOI

Barbosa P, de Oliveira LA, Pucci MB, Santos MH, Moreira-Filho O, Vicari MR, et al. Identification and chromosome mapping of repetitive elements in the Astyanax scabripinnis (Teleostei: Characidae) species complex. Genetica. 2015;143: 55–62. doi: 10.1007/s10709-014-9813-2 PubMed DOI

Costa GWWF, Cioffi MB, Bertollo LAC, Molina WF. The evolutionary dynamics of ribosomal genes, histone H3, and transposable Rex elements in the genome of atlantic snappers. J Hered. 2016;107: 173–180. doi: 10.1093/jhered/esv136 PubMed DOI PMC

Vicari MR, Artoni RF, Moreira-Filho O, Bertollo LAC. Colocalization of repetitive DNAs and silencing of major rRNA genes. A case report of the fish Astyanax janeiroensis. Cytogenet Genome Res. 2008;122: 67–72. doi: 10.1159/000151318 PubMed DOI

de Barros AV, Sczepanski TS, Cabrero J, Camacho JPM, Vicari MR, Artoni RF. Fiber FISH reveals different patterns of high-resolution physical mapping for repetitive DNA in fish. Aquaculture. 2011;322/323: 47–50. doi: 10.1016/j.aquaculture.2011.10.002 DOI

Sakofsky CJ, Ayyar S, Deem AK, Chung W-H, Ira G, Malkova A. Translesion polymerases drive microhomology-mediated break-induced replication leading to complex chromosomal rearrangements. Mol Cell. 2015;60: 860–872. doi: 10.1016/j.molcel.2015.10.041 PubMed DOI PMC

Tsekrekou M, Stratigi K, Chatzinikolaou G. The nucleolus: in genome maintenance and repair. Int J Mol Sci. 2017;18 doi: 10.3390/ijms18071411 PubMed DOI PMC

Traldi JB, Vicari MR, Martinez JF, Blanco DR, Lui RL, Moreira-Filho O. Chromosome analyses of Apareiodon argenteus and Apareiodon davisi (Characiformes, Parodontidae): an extensive chromosomal polymorphism of 45S and 5S ribosomal DNAs. Zebrafish. 2016;13: 19–25. doi: 10.1089/zeb.2015.1124 PubMed DOI

A Detailed Karyological Investigation of three Endemic Cobitis Linnaeus, 1758 Species (Teleostei, Cobitidae) in Anatolia, Türkiye

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Large-scale comparative analysis of cytogenetic markers across Lepidoptera

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Cytogenetics, genomics and biodiversity of the South American and African Arapaimidae fish family (Teleostei, Osteoglossiformes)