BACKGROUND: Polyploidy, although still poorly explored, represents an important evolutionary event in several cyprinid clades. Herein, Catlocarpio siamensis and Probarbus jullieni - representatives of the paleotetraploid tribe Probarbini, were characterized both by conventional and molecular cytogenetic methods. RESULTS: Alike most other paleotetraploid cyprinids (with 2n = 100), both species studied here shared 2n = 98 but differed in karyotypes: C. siamensis displayed 18m + 34sm + 46st/a; NF = 150, while P. jullieni exhibited 26m + 14sm + 58st/a; NF = 138. Fluorescence in situ hybridization (FISH) with rDNA probes revealed two (5S) and eight (18S) signals in C. siamensis, respectively, and six signals for both probes in P. jullieni. FISH with microsatellite motifs evidenced substantial genomic divergence between both species. The almost doubled size of the chromosome pairs #1 in C. siamensis and #14 in P. jullieni compared to the rest of corresponding karyotypes indicated chromosomal fusions. CONCLUSION: Based on our findings, together with likely the same reduced 2n = 98 karyotypes in the remainder Probarbini species, we hypothesize that the karyotype 2n = 98 might represent a derived character, shared by all members of the Probarbini clade. Besides, we also witnessed considerable changes in the amount and distribution of certain repetitive DNA classes, suggesting complex post-polyploidization processes in this small paleotetraploid tribe.

Departamento de Genética e Evolução Universidade Federal de São Carlos São Carlos SP Brazil

Faculdade de Ciencias Centre for Ecology Evolution and Environmental Changes Universidade de Lisboa Campo Grande PT 1749 016 Lisbon Portugal

Faculty of Applied Science and Engineering Khon Kaen University Nong Kai Campus Muang Nong Kai Thailand

Institute of Human Genetics Jena University Hospital Am Klinikum 1 D 07747 Jena Germany

Laboratory of Fish Genetics Institute of Animal Physiology and Genetics Czech Academy of Sciences Rumburská 89 277 21 Liběchov Czech Republic

Secretaria de Estado de Educação de Mato Grosso SEDUC MT Cuiabá MT Brazil

Toxic Substances in Livestock and Aquatic Animals Research Group Department of Biology Faculty of Science Khon Kaen University Muang District Khon Kaen Thailand

See more in PubMed

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 London 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. Berlin: Springer; 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

Uyeno T, Smith GR. Tetraploid origin of the karyotype of catostomid fishes. Science. 1972;175:644–646. doi: 10.1126/science.175.4022.644. 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

Alexandrou MA, Oliveira C, Maillard M, McGill RAR, Newton J, Creer S, et al. Competition and phylogeny determine community structure in Müllerian co-mimics. Nature. 2011;469:84. doi: 10.1038/nature09660. 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 R Soc B Biol Sci. 2014;281:20132881. doi: 10.1098/rspb.2013.2881. PubMed DOI PMC

Yang L, Sado T, Vincent Hirt M, 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

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

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. Sci China Life Sci. 2016;59:1149–1165. doi: 10.1007/s11427-016-0007-7. PubMed DOI

Smith HM. The freshwater fishes of Siam, or Thailand. Bull - United States Natl Museum. 1945;188:1–633.

Rainboth WJ. Fishes of the cambodian mekong. Rome: Food & Agriculture Org.; 1996.

Robert TR. Revision of the southeast Asian cyprinid fish genus Probarbus, with two new species threatened by proposed construction of dams on the Mekong River. Ichthyol Explor Freshwaters. 1992;3:37–48.

Hogan Z, Baird I. Probarbus jullieni. The IUCN Red List of Threatened Species. 2011. 10.2305/IUCN.UK.2011-1.RLTS.T18182A7742599.en. Accessed 6 Sep 2017.

Baird I. Probarbus labeamajor. The IUCN Red List of Threatened Species. 2011. 10.2305/IUCN.UK.2011-1.RLTS.T18183A7744836.en. Accessed 6 Sep 2017.

Baird I. Probarbus labeaminor. The IUCN Red List of Threatened Species 2012. 10.2305/IUCN.UK.2012-1.RLTS.T18184A1728617.en. Accessed 6 Sep 2017.

Hogan Z. Catlocarpio siamensis. The IUCN Red List of Threatened Species. 2011. 10.2305/IUCN.UK.2011-1.RLTS.T180662A7649359.en. Accessed 6 Sep 2017.

Arai R. Fish karyotypes: a check list. Tokio: Springer Science & Business Media; 2011.

Singh M, Kumar R, Nagpure NS, Kushwaha B, Gond I, Lakra WS. Chromosomal localization of 18s and 5s rDNA using FISH in the genus Tor (Pisces, Cyprinidae) Genetica. 2009;137:245–252. doi: 10.1007/s10709-009-9367-x. PubMed DOI

Mani I, Kumar R, Singh M, Nagpure NS, Kushwaha B, Srivastava PK, et al. Nucleotide variation and physical mapping of ribosomal genes using FISH in genus Tor (Pisces, Cyprinidae) Mol Biol Rep. 2011;38:2637–2647. doi: 10.1007/s11033-010-0405-7. PubMed DOI

Suzuki A, Taki Y. Chromosomes and DNA values of two cyprinid fishes of the subfamily Barbinae. Japanese J Ichthyol. 1986;32:459–462.

Suzuki A, Taki Y. Karyotype and DNA content in the cyprinid Catlocarpio siamensis. Japanese J Ichthyol. 1988;35:389–391.

Otto SP, Whitton J. Polyploid incidence and evolution. Annu Rev Genet. 2000;34:401–437. doi: 10.1146/annurev.genet.34.1.401. PubMed DOI

Le Comber SC, Smith C. Polyploidy in fishes: patterns and processes. Biol J Linn Soc. 2004;82:431–442. doi: 10.1111/j.1095-8312.2004.00330.x. DOI

Mable BK, Alexandrou MA, Taylor MI. Genome duplication in amphibians and fish: an extended synthesis. J Zool. 2011;284:151–182. doi: 10.1111/j.1469-7998.2011.00829.x. DOI

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

Ráb P, Collares-Pereira MJ. Chromosomes of European cyprinid fishes (Cyprinidae, Cypriniformes). A review. Folia Zool. 1995;44:193–214.

Spoz A, Boron 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

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

Rishi KK, Singh J, Kaul MM. Chromosome analysis of Schizothoracichthys progastus (McCll) (Cypriniformes) Chromosom Inform Serv. 1983;34:12–13.

Rishi KK, Rishi S. Karyotype study on six Indian hill-stream fishes. Chromosom Sci. 1998;2:9–13.

Zan RG, Liu WG, Song Z. Tetraploid-hexaploid relationship in Schizothoracinae. Acta Genet Sin. 1985;12:137–142.

Mazik EJ, Toktosunovic A, Ráb P. Karyotype study of four species of the genus Diptychus (Pisces, Cyprinidae), with remarks on polyploidy of schizothoracine fishes. Folia Zool. 1989;38:325–332.

Ahmad F, Yousuf AR, Tripathi NK, Zargar UR. On the chromosomes of two cyprinid fishes of the subfamily Schizothoracinae from Kashmir. Nat Sci. 2011;9:53–61.

Yu X, Zhou T, Li K, Li Y, Zhou M. On the karyosystematics of cyprinid fishes and a summary of fish chromosome studies in China. Genetica. 1987;72:225–235. doi: 10.1007/BF00116227. DOI

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

Yu XY, Li YC, Zhou T. Karyotype studies of cyprinid fishes in China-comparative study of the karyotypes of 8 species of schizothoracine fishes. Wuhan Univ J Nat Sci. 1990;2:97–104.

He D, Chen Y, Chen Y, Chen Z. Molecular phylogeny of the specialized schizothoracine fishes (Teleostei: Cyprinidae), with their implications for the uplift of the Qinghai-Tibetan Plateau. Chin Sci Bull. 2004;49:39–48. doi: 10.1007/BF02901741. DOI

Yu XY, Yu XJ. A schizothoracine fish species, Diptychus dipogon, with a very high number of chromosomes. Chromosom Inf Serv. 1990;48:17–18.

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

Ma X-F, 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

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

Madlung A. Polyploidy and its effect on evolutionary success: old questions revisited with new tools. Heredity. 2013;110:99–104. doi: 10.1038/hdy.2012.79. PubMed DOI PMC

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

Schwarzacher T, Leitch AR, Bennett MD, Heslop-Harrison JS. In situ localization of parental genomes in a wide hybrid. Ann Bot. 1989;64:315–324. doi: 10.1093/oxfordjournals.aob.a087847. DOI

Leitch IJ, Bennett MD. Genome downsizing in polyploid plants. Biol 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, Mhiri C, 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

Chester M, Leitch AR, Soltis PS, Soltis DE. Review of the application of modern cytogenetic methods (FISH/GISH) to the study of reticulation (polyploidy/hybridisation) Genes (Basel) 2010;1:166–192. doi: 10.3390/genes1020166. PubMed DOI PMC

Xiong Z, Pires JC. Karyotype and identification of all homoeologous chromosomes of allopolyploid Brassica napus and its diploid progenitors. Genetics. 2011;187:37–49. doi: 10.1534/genetics.110.122473. PubMed DOI PMC

Cuadrado Á, de Bustos A, Jouve N. On the allopolyploid origin and genome structure of the closely related species Hordeum secalinum and Hordeum capense inferred by molecular karyotyping. Ann Bot. 2017;120:245–255. PubMed PMC

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

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

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

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

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

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) Chromosom Res. 2006;14:297–306. doi: 10.1007/s10577-006-1047-4. PubMed DOI

Zhu H-P, Gui J-F. Identification of genome organization in the unusual allotetraploid form of Carassius auratus gibelio. Aquaculture. 2007;265:109–117. doi: 10.1016/j.aquaculture.2006.10.026. DOI

Da Silva M, Matoso DA, Ludwig LAM, Gomes E, Almeida MC, Vicari MR, et al. Natural triploidy in Rhamdia quelen identified by cytogenetic monitoring in Iguaçu basin, southern Brazil. Environ Biol Fish. 2011;91:361–366. doi: 10.1007/s10641-011-9794-2. DOI

Zhang C, Ye L, Chen Y, Xiao J, Wu Y, Tao M, et al. The chromosomal constitution of fish hybrid lineage revealed by 5S rDNA FISH. BMC Genet. 2015;16:140. doi: 10.1186/s12863-015-0295-8. PubMed DOI PMC

Ribeiro LB, Moraes Neto A, Artoni RF, Matoso DA, Feldberg E. Chromosomal mapping of repetitive sequences (Rex3, Rex6, and rDNA Genes) in hybrids between Colossoma macropomum (Cuvier, 1818) and Piaractus mesopotamicus (Holmberg, 1887) Zebrafish. 2017;14:155–160. doi: 10.1089/zeb.2016.1378. PubMed DOI

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

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

Qin Q, Wang J, Hu M, Huang S, Liu S. Autotriploid origin of Carassius auratus as revealed by chromosomal locus analysis. Sci China Life Sci. 2016;59:622–626. doi: 10.1007/s11427-016-5040-7. 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

Feliner GN, Rosselló JA. Concerted evolution of multigene families and homoeologous recombination. In: Wendel JF, editor. Plant genome diversity volume 1. Vienna: Springer-Verlag; 2012. pp. 171–193.

Qin Q, He W, Liu S, Wang J, Xiao J, Liu Y. Analysis of 5S rDNA organization and variation in polyploid hybrids from crosses of different fish subfamilies. J Exp Zool Part B Mol Dev Evol. 2010;314:403–411. doi: 10.1002/jez.b.21346. 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 × topmouth culter. PLoS One. 2012;7:e38976. doi: 10.1371/journal.pone.0038976. PubMed DOI PMC

Huang P, Xiao A, Tong X, Lin S, Zhang B. Targeted mutagenesis in zebrafish by TALENs. In: Clifton NJ, editor. Methods in molecular biology. New Jersey: Human Press; 2016. pp. 191–206. PubMed

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

Fontdevila A. Hybrid genome evolution by transposition. Cytogenet Genome Res. 2005;110:49–55. doi: 10.1159/000084937. PubMed DOI

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

Kovarik A, Dadejova M, Lim YK, Chase MW, Clarkson JJ, Knapp S, et al. Evolution of rDNA in Nicotiana allopolyploids: a potential link between rDNA homogenization and epigenetics. Ann Bot. 2008;101:815–823. doi: 10.1093/aob/mcn019. 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

Zhang X, Eickbush MT, Eickbush TH. Role of recombination in the long-term retention of transposable elements in rRNA gene loci. Genetics. 2008;180:1617–1626. doi: 10.1534/genetics.108.093716. PubMed DOI PMC

Cioffi MB, Martins C, Bertollo LAC. Chromosome spreading of associated transposable elements and ribossomal DNA in the fish Erythrinus erythrinus. Implications for genome change and karyoevolution in fish. BMC Evol Biol. 2010;10:271. doi: 10.1186/1471-2148-10-271. PubMed DOI PMC

Symonová R, Majtánová Z, Sember A, Staaks GBO, Bohlen J, Freyhof J. 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

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

Singh M, Kumar R, Nagpure NS, Kushwaha B, Mani I, Chauhan UK, et al. Population distribution of 45S and 5S rDNA in golden mahseer, Tor putitora: population-specific FISH marker. J Genet. 2009;88:315–320. doi: 10.1007/s12041-009-0045-7. PubMed DOI

Singh M, Kumar R, Nagpure NS, Kushwaha B, Mani I, Lakra WS. Extensive NOR site polymorphism in geographically isolated populations of golden mahseer, Tor putitora. Genome. 2009;52:783–789. doi: 10.1139/G09-052. PubMed DOI

Pereira CSA, Aboim MA, Ráb P, Collares-Pereira MJ. Introgressive hybridization as a promoter of genome reshuffling in natural homoploid fish hybrids (Cyprinidae, Leuciscinae) Heredity. 2014;112:343–350. doi: 10.1038/hdy.2013.110. PubMed DOI PMC

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

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

Libertini A, Sola L, Rampin M, Rossi AR, Iijima K, Ueda T. Classical and molecular cytogenetic characterization of allochthonous European bitterling Rhodeus amarus (Cyprinidae, Acheilognathinae) from northern Italy. Genes Genet Syst. 2008;83:417–422. doi: 10.1266/ggs.83.417. PubMed DOI

Pereira CSA, Ráb P, Collares-Pereira MJ. Chromosomes of European cyprinid fishes: comparative cytogenetics and chromosomal characteristics of ribosomal DNAs in nine Iberian chondrostomine species (Leuciscinae) Genetica. 2012;140:485–495. doi: 10.1007/s10709-013-9697-6. PubMed DOI

Rossi AR, Milana V, Hett AK, Tancioni L. Molecular cytogenetic analysis of the Appenine endemic cyprinid fish Squalius lucumonis and three other Italian leuciscines using chromosome banding and FISH with rDNA probes. Genetica. 2012;140:469–476. doi: 10.1007/s10709-012-9695-0. PubMed DOI

Li Y-J, Gao Y-C, Zhou H, Liu B, Gao M, Wang Y-S, et al. Molecular cytogenetic study of genome ploidy in the German mirror carp Cyprinus carpio. Fish Sci. 2014;80:963–968. doi: 10.1007/s12562-014-0774-2. DOI

Kumar R, Baisvar VS, Kushwaha B, Waikhom G, Nagpure NS. Cytogenetic investigation of Cyprinus carpio (Linnaeus, 1758) using giemsa, silver nitrate, CMA 3 staining and fluorescence in situ hybridization. Nucl. 2017;60:1–8. doi: 10.1007/s13237-016-0189-9. DOI

Inafuku J, Nabeyama M, Kikuma Y, Saitoh J, Kubota S, Kohno S. Chromosomal location and nucleotide sequences of 5S ribosomal DNA of two cyprinid species (Osteichthyes, Pisces) Chromosom Res. 2000;8:193–199. doi: 10.1023/A:1009292610618. PubMed DOI

Murakami M, Fujitani H. Characterization of repetitive DNA sequences carrying 5S rDNA of the triploid ginbuna (Japanese silver crucian carp, Carassius auratus langsdorfi) Genes Genet Syst. 1998;73:9–20. doi: 10.1266/ggs.73.9. PubMed DOI

Phillips RB, Reed KM. Localization of repetitive DNAs to zebrafish (Danio rerio) chromosomes by fluorescence in situ hybridization (FISH) Chromosom Res. 2000;8:27–35. doi: 10.1023/A:1009271017998. PubMed DOI

Tautz D, Renz M. Simple sequences are ubiquitous repetitive components of eukaryotic genomes. Nucleic acids Res Acids Res. 1984;12:4127–4138. doi: 10.1093/nar/12.10.4127. PubMed DOI PMC

Ellegren H. Microsatellites: simple sequences with complex evolution. Nat Rev Genet. 2004;5:435–445. doi: 10.1038/nrg1348. PubMed DOI

Chistiakov DA, Hellemans B, Volckaert FAM. Microsatellites and their genomic distribution, evolution, function and applications: a review with special reference to fish genetics. Aquaculture. 2006;255:1–29. doi: 10.1016/j.aquaculture.2005.11.031. DOI

Yano CF, Bertollo LAC, Liehr T, Troy WP, Cioffi MDB. W chromosome dynamics in Triportheus species (Characiformes, Triportheidae): an ongoing process narrated by repetitive sequences. J Hered. 2016;107:342–348. doi: 10.1093/jhered/esw021. PubMed DOI PMC

Oliveira EA, Sember A, Bertollo LAC, Yano CF, Ezaz T, Moreira-Filho O, et al. Tracking the evolutionary pathway of sex chromosomes among fishes: characterizing the unique XX/XY1Y2 system in Hoplias malabaricus (Teleostei, Characiformes) Chromosoma. 2018;127:115–128. doi: 10.1007/s00412-017-0648-3. PubMed DOI

Cioffi MB, Kejnovsky E, Bertollo LAC. The chromosomal distribution of microsatellite repeats in the genome of the wolf fish Hoplias malabaricus, focusing on the sex chromosomes. Cytogenet Genome Res. 2011;132:289–296. doi: 10.1159/000322058. PubMed DOI

Xu D, Lou B, Bertollo LAC, Cioffi MDB. Chromosomal mapping of microsatellite repeats in the rock bream fish Oplegnathus fasciatus, with emphasis of their distribution in the neo-Y chromosome. Mol Cytogenet. 2013;6:12. doi: 10.1186/1755-8166-6-12. PubMed DOI PMC

Terencio ML, Schneider CH, Gross MC, Vicari MR, Farias IP, Passos KB, et al. Evolutionary dynamics of repetitive DNA in Semaprochilodus (Characiformes, Prochilodontidae): a fish model for sex chromosome differentiation. Sex Dev. 2013;7:325–333. doi: 10.1159/000356691. PubMed DOI

Yano CF, Poltronieri J, Bertollo LAC, Artoni RF, Liehr T, Cioffi MDB. Chromosomal mapping of repetitive DNAs in Triportheus trifurcatus (Characidae, Characiformes): insights into the differentiation of the Z and W chromosomes. PLoS One. 2014;9:e90946. doi: 10.1371/journal.pone.0090946. PubMed DOI PMC

Oliveira EA, Bertollo LAC, Yano CF, Liehr T, Cioffi MDB. 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

Pucci MB, Barbosa P, Nogaroto V, Almeida MC, Artoni RF, Scacchetti PC, et al. Chromosomal spreading of microsatellites and (TTAGGG)n sequences in the Characidium zebra and C. gomesi genomes (Characiformes: Crenuchidae) Cytogenet Genome Res. 2016;149:182–190. doi: 10.1159/000447959. PubMed DOI

Piscor D, Parise-Maltempi PP. Microsatellite organization in the B chromosome and a chromosome complement in Astyanax (Characiformes, Characidae) species. Cytogenet Genome Res. 2016;148:44–51. doi: 10.1159/000444728. PubMed DOI

Bertollo LAC, Cioffi MB, Moreira-Filho O. Direct chromosome preparation from freshwater teleost fishes. In: Ozouf-Costaz C, Pisano E, Foresti F, Almeida Toledo LF, editors. Fish cytogenetic techniques. Enfield USA: CRC Press; 2015. pp. 21–26.

Sumner AT. A simple technique for demonstrating centromeric heterochromatin. Exp Cell Res. 1972;75:304–306. doi: 10.1016/0014-4827(72)90558-7. PubMed DOI

Pendás AM, Móran P, Freije JP, Garcia-Vásquez E. Chromosomal location and nucleotide sequence of two tandem repeats of the Atlantic salmon 5S rDNA. Cytogenet Cell Genet. 1994;67:31–36. doi: 10.1159/000133792. PubMed DOI

Cioffi MB, Martins C, Centofante L, Jacobina U, Bertollo LAC. Chromosomal variability among allopatric populations of erythrinidae fish Hoplias malabaricus: mapping of three classes of repetitive DNAs. Cytogenet Genome Res. 2009;125:132–141. doi: 10.1159/000227838. PubMed DOI

Yano CF, Bertollo LAC, Cioffi MB. FISH-FISH: molecular cytogenetics in fish species. In: Liehr T, editor. Fluorescence in situ hybridization (FISH) - application guide. 2. Berlin: Springer; 2017. pp. 429–443.

Kubat Z, Hobza R, Vyskot B, Kejnovsky E. Microsatellite accumulation on the Y chromosome in Silene latifolia. Genome. 2008;51:350–356. doi: 10.1139/G08-024. 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

Chromosomes of Asian Cyprinid Fishes: Genomic Differences in Conserved Karyotypes of 'Poropuntiinae' (Teleostei, Cyprinidae)

Taxonomic Diversity Not Associated with Gross Karyotype Differentiation: The Case of Bighead Carps, Genus Hypophthalmichthys (Teleostei, Cypriniformes, Xenocyprididae)