The bighead carps of the genus Hypophthalmichthys (H. molitrix and H. nobilis) are important aquaculture species. They were subjected to extensive multidisciplinary research, but with cytogenetics confined to conventional protocols only. Here, we employed Giemsa-/C-/CMA3- stainings and chromosomal mapping of multigene families and telomeric repeats. Both species shared (i) a diploid chromosome number 2n = 48 and the karyotype structure, (ii) low amount of constitutive heterochromatin, (iii) the absence of interstitial telomeric sites (ITSs), (iv) a single pair of 5S rDNA loci adjacent to one major rDNA cluster, and (v) a single pair of co-localized U1/U2 snDNA tandem repeats. Both species, on the other hand, differed in (i) the presence/absence of remarkable interstitial block of constitutive heterochromatin on the largest acrocentric pair 11 and (ii) the number of major (CMA3-positive) rDNA sites. Additionally, we applied here, for the first time, the conventional cytogenetics in H. harmandi, a species considered extinct in the wild and/or extensively cross-hybridized with H. molitrix. Its 2n and karyotype description match those found in the previous two species, while silver staining showed differences in distribution of major rDNA. The bighead carps thus represent another case of taxonomic diversity not associated with gross karyotype differentiation, where 2n and karyotype structure cannot help in distinguishing between genomes of closely related species. On the other hand, we demonstrated that two cytogenetic characters (distribution of constitutive heterochromatin and major rDNA) may be useful for diagnosis of pure species. The universality of these markers must be further verified by analyzing other pure populations of bighead carps.

Departamento de Genética e Evolução Universidade Federal de São Carlos Rod Washington Luiz km 235 cep São Carlos 13565 905 Brazil

Department of Cell Biology Faculty of Science Charles University Viničná 7 2 128 43 Prague Czech Republic

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

Research Institute of Aquaculture No 1 Dinh Bang Tu Son Bac Ninh 16000 Vietnam

Zobrazit více v PubMed

Howes G.J. Anatomy and phylogeny of the Chinese major carps Ctenopharyngodon Steind., 1866 and Hypophthalmichthys Blkr., 1860. Bull. Br. Mus. (Nat. Hist.) Zool. 1981;41:1–52.

Tan M., Armbruster J.W. Phylogenetic classification of extant genera of fishes of the order Cypriniformes (Teleostei. Ostariophysi) Zootaxa. 2018;4476:6–39. doi: 10.11646/zootaxa.4476.1.4. PubMed DOI

Tao W., Zou M., Wang X., Gan X., Mayden R.L., He S. Phylogenomic analysis resolves the formerly intractable adaptive diversification of the endemic clade of East Asian Cyprinidae (Cypriniformes) PLoS ONE. 2010;5:e13508. doi: 10.1371/journal.pone.0013508. PubMed DOI PMC

Kottelat M. A Catalogue and Core Bibliography of the Fishes Known to Occur in Freshwaters, Mangroves and Estuaries. Raffles Bull. Zool; Kent Ridge, Singapore: 2013. The fishes of the inland waters of Southeast Asia; pp. 1–663.

Yen M.D. Species composition and distribution of the freshwater fish fauna of the North of Vietnam. Hydrobiologia. 1985;121:281–286. doi: 10.1007/BF00017548. DOI

FAO Statistics Food and Agriculture. [(accessed on 29 January 2020)]; Available online: http://www.fao.org/fishery/culturedspecies/Hypophthalmichthys_molitrix/en.

Stepien C.A., Snyder M.R., Elz A.E. Invasion genetics of the silver carp Hypophthalmichthys molitrix across North America: Differentiation of fronts, introgression, and eDNA metabarcode detection. PLoS ONE. 2019;14:e0203012. doi: 10.1371/journal.pone.0203012. PubMed DOI PMC

Sing A.K., Kumar D., Srivastava S.C., Ansan A., Jena T.K., Sarkar U.K. Invasion and impacts of alien fish species in the Ganga River, India. Aquat. Ecosyst. Health Manag. 2013;16:408–414. doi: 10.1080/14634988.2013.857974. DOI

Luebcker N., Zengeva T.A., Dabrowski J., Robertson J.P. Predicting the potential distribution of invasive silver carp Hypophthalmichthys molitrix in South Africa. Afr. J. Aquat. Sci. 2014;39:157–165. doi: 10.2989/16085914.2014.926856. DOI

Garvey J.E. Bigheads of the genus Hypophthalmichthys. In: Francis R.A., editor. A Handbook of Global Freshwater Invasive Species. Earthscan; New York, NY, USA: 2012. pp. 235–245.

Hayer C.A., Breeggemann J.J., Jason J., Klumb R.A., Graeb B.D.S., Bertrand K.N. Population characteristics of bighead and silver carp on the northwestern front of their North American invasion. Aquat. Invasions. 2014;9:289–303. doi: 10.3391/ai.2014.9.3.05. DOI

Farrington H.L., Edwards C.E., Bartron M., Lance R.F. Phylogeography and population genetics of introduced silver carp (Hypophthalmichthys molitrix) and bighead carp (H. nobilis) in North America. Biol. Invasions. 2017;19:2789–2811. doi: 10.1007/s10530-017-1484-3. DOI

DeBoer J.A., Anderson A.M., Casper A.F. Multi-trophic response to invasive silver carp (Hypophthalmichthys molitrix) in large floodplain river. Freshw. Biol. 2018;63:597–611. doi: 10.1111/fwb.13097. DOI

Tristano E.P., Coulter A.A., Newton T.J., Garvey J.E. Invasive silver carp may compete with unionid mussels for algae: First experimental evidence. Aquat. Conserv. 2019;29:1749–1757. doi: 10.1002/aqc.3185. DOI

Marián T., Krasznai Z. Karyological investigation on Ctenopharyngodon idella and Hypophthalmichthys nobilis and their cross-breeding. Aquac. Hung. (Szarvas) 1978;1:44–50.

Marián T., Krasznai Z. Comparative karyological studies on Chinese carps. Aquaculture. 1979;13:325–336. doi: 10.1016/0044-8486(79)90036-X. DOI

Marián T., Krasznai Z. Zylogische Untersuchungen bei der Familie Cyprinidae (Pisces) Biol. Zent. 1987;97:205–214.

Marián T., Krasznai Z., Oláh J. Characteristic karyological, biochemical and morphological markers of silver carp (Hypophthalmichthys molitrix), bighead carp (Aristicthys nobilis) and their hybrids. Aquac. Hung. 1986;5:15–30.

Vasiliev V.P., Makeeva A.P., Ryabov I.N. The study of chromosome complexes in cyprinid fish and their hybrids. Genetika. 1978;14:1450–1460. (In Russian)

Beck M.L., Biggers C.J., Dupree H.K. Karyological analysis of Ctenopharyngodon idella, Aristichthys nobilis and their F1 hybrid. Trans. Am. Fish. Soc. 1980;109:433–438. doi: 10.1577/1548-8659(1980)109<433:KAOCIA>2.0.CO;2. DOI

Beck M.L., Biggers C.J. Chromosomal investigation of Ctenopharyngodon idella × Aristichthys nobilis hybrids. Experientia. 1982;38:319. doi: 10.1007/BF01949366. DOI

Zan R.G., Song Z. Analysis and comparison between karyotypes of Cyprinus carpio and Carassius auratus and Aristichthys nobilis and Hypophthalmichthys molitrix. Acta Genet. Sin. 1980;7:72–77.

Zan R.G., Song Z., Liu W.G. Studies on karyotypes and nuclear DNA contents of some cyprinoid fishes, with notes on fish polyploids in China. In: Uyeno T., Arai R., Taniuchi T., Matsuura K., editors. Indo-Pacific Fish Biology: Proceedings of the Second International Conference on Indo-Pacific Fish. Ichthyological Society of Japan; Tokyo, Japan: 1986. pp. 877–885.

Zhou T. Analysis of karyotype in bighead carp. Freshw. Fish. (Shashi) 1980;4:3–7. (In Chinese)

Zhou T., Lin J., Yang Y. The karyotype of black carp [Mylopharyngodon piceus (Rich.)] J. Wuhan Univ. 1980;4:112–116. (In Chinese with English Abstract)

Liu L.Y. Karyotype analysis of Aristichthys nobilis by the leucocyte culture method. J. Beijing Norm. Univ. (Nat. Sci.) 1981;3:79–83. (In Chinese with English Abstract)

Almeida-Toledo L.F., Bigoni A.P.V., Bernardino G., De Almeida Filho S. Chromosomal location of NORs and C bands in F1 hybrids of bighead carp and silver carp reared in Brazil. Aquaculture. 1995;135:277–284. doi: 10.1016/0044-8486(95)01032-7. DOI

. A preliminary report on the chromosomes number of 52 species of fishes of the Pearl River system in Guandong Province. J. Wuhan Univ. 1983;3:123–125.

Manna G.K., Khuda-Bukhsh A.R. Karyomorphology of cyprinid fishes and cytological evaluation of the family. Nucleus. 1978;43:119–127.

Liu L.Y. Karyotype analysis of Hypophthalmichthys molitrix. Acta Genet. Sin. 1981;8:251–255. (In Chinese with English Abstract)

Su Z., Xu K., Chen S., Bai G. Studies on triploid silver carp and its karyotype. Chin. Zool. Res. (Suppl.) Kunming. 1984;5:15–19. (In Chinese with English Abstract)

Yu X.L., Zhou T., Li Z.C., Li K., Zhou M. On the karyosystematics of cyprinid fishes and a summary of fish chromosome studies in China. Genetica. 1987;72:225–236. doi: 10.1007/BF00116227. DOI

Zhou M., Li Y.C., Zhou T., Yu X.J. A BrdU-BSG method for G-banding in fish chromosomes and an idiogram of G-banded karyotype of silver carp. Acta Genet. Sin. 1989;16:184–187.

Ren X.H., Cui J., Yu Q. Chromosomal heterochromatin differentiation of cyprinid fishes. Genetica. 1992;87:47–51. doi: 10.1007/BF00128772. DOI

Khuda-Bukhsh A.R., Chakrabarti C. Induction of serial bands akin to G-type on metaphase chromosomes of two species of fish, Rita rita (Bagridae) and Hypophthalmichthys molitrix (Cyprinidae) Indian J. Exp. Biol. 1996;34:1271–1273.

Šlechtová V., Šlechta V., Hiep D.D., Valenta M. Biochemical genetic comparison of bighead (Aristichthys nobilis) and silver carp (Hypophthalmichthys molitrix) and their hybrids in Czechoslovakia. J. Fish Biol. 1991;39:349–357. doi: 10.1111/j.1095-8649.1991.tb05097.x. DOI

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., Rodina M., Rábová M., Ráb P. 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

Ráb P., Roth P. Cold-blooded vertebrates. In: Balicek P., Forejt J., Rubeš J., editors. Methods of Chromosome Analysis. Cytogenetická Sekce Československé Biologické Společnosti pri. CSAV; Brno, Czech Republic: 1988. pp. 115–124.

Bertollo L.A.C., Cioffi M.B., Moreira-Filho O. Direct chromosome preparation from freshwater teleost fishes. In: Ozouf-Costaz C., Pisano E., Foresti F., Toledo L.F.A., editors. Fish Cytogenetic Techniques (Ray-Fin Fishes and Chondrichthyans) 2nd ed. Volume 1. CRC Press; Enfield, CT, USA: 2015. pp. 21–26.

Haaf T., Schmid M. An early stage of ZZ/ZW sex chromosomes differentiation in Poecilia sphenops var. melanistica (Poeciliidae, Cyprinodontiformes). Chromosoma. 1984;89:37–41. doi: 10.1007/BF00302348. 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 A.R., Iaselli V., Rasch E.M., Monaco P.J. 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

Howell W.M., Black D.A. Controlled silver-staining of nucleolus organizer regions with a protective colloidal developer: A 1-step method. Experientia. 1980;36:1014–1015. doi: 10.1007/BF01953855. PubMed 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

Cioffi M.B., Martins C., Centofante L., Jacobina U., Bertollo L.A.C. 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

Silva D.M.Z.A., Utsunomia R., Pansonato-Alves J.C., Oliveira C., Foresti F. Chromosomal mapping of repetitive DNA sequences in five species of Astyanax (Characiformes, Characidae) reveals independent location of U1 and U2 snRNA sites and association of U1 snRNA and 5S rDNA. Cytogenet. Genome Res. 2015;146:144–152. doi: 10.1159/000438813. PubMed DOI

Yano C.F., Bertollo L.A.C., Cioffi M.B. Fish-FISH: Molecular cytogenetics in fish species. In: Liehr T., editor. Fluorescence In Situ Hybridization (FISH)—Application Guide. 2nd ed. Springer; Berlin, Germany: 2017. pp. 429–443.

Sember A., Bohlen J., Šlechtová V., Altmanová M., Pelikánová Š., Ráb P. Dynamics of tandemly repeated DNA sequences during evolution of diploid and tetraploid botiid loaches (Teleostei: Cobitoidea: Botiidae) PLoS ONE. 2018;13:e0195054. doi: 10.1371/journal.pone.0195054. PubMed DOI PMC

Altschul S.F., Gish W., Miller W., Myers E.W., Lipman D.J. Basic local alignment search tool. [(accessed on 20 March 2018)];J. Mol. Biol. 1990 215:403–410. doi: 10.1016/S0022-2836(05)80360-2. Available online: http://blast.ncbi.nlm.nih.gov/blast. PubMed DOI

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

Matthey R. L’ evolution de la formule chromosomiale chez les vertebrees. Experientia. 1945;1:78–86. doi: 10.1007/BF02156807. DOI

Liu H., Pang M., Yu X., Zhou Y., Tong J., Fu B. Sex-specific markers developed by next-generation sequencing confirmed an XX/XY sex determination system in bighead carp (Hypophthalmichehys nobilis) and silver carp (Hypophthalmichthys molitrix) DNA Res. 2018;25:257–264. doi: 10.1093/dnares/dsx054. PubMed DOI PMC

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

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

Saenjundaeng P., Oliveira E.A., Tanomtong A., Supiwong W., Phimphan S., Collares-Pereira M.J., Sember A., Yano C.F., Hatanaka T., Bertollo L.A.C., et al. Chromosomes of Asian cyprinid fishes: Cytogenetic analysis of two representatives of small paleotetraploid tribe Probarbini. Mol. Cytogenet. 2018;11:51. doi: 10.1186/s13039-018-0399-8. PubMed DOI PMC

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

Schubert I. What is behind “centromere repositioning”? Chromosoma. 2018;127:229–234. doi: 10.1007/s00412-018-0672-y. PubMed DOI

Souza I.L., Moreira-Filho O. Constitutive heterochromatin and Ag-NOR polymorphisms in the small characid fish Astyanax scabripinnis (Jenyns, 1842) Comp. Gen. Pharm. 2007;72:63–69. doi: 10.1508/cytologia.72.63. DOI

Hashimoto D.T., Porto-Foresti F. Chromosome polymorphism of heterochromatin and nucleolar regions in two populations of the fish Astyanax bockmanni (Teleostei: Characiformes) Neotrop. Ichthyol. 2010;8:861–866. doi: 10.1590/S1679-62252010000400016. DOI

Baumgärtner L., Paiz L.M., Zawadzki C.H., Margarido V.P., Castro A.L.B.P. Heterochromatin polymorphism and physical mapping of 5S and 18S ribosomal DNA in four populations of Hypostomus strigaticeps (Regan, 1907) from the Paraná River basin, Brazil: Evolutionary and environmental correlation. Zebrafish. 2014;11:479–487. doi: 10.1089/zeb.2014.1028. PubMed DOI

Utsunomia R., Pansonato-Alves J.C., Costa-Silva G.J., Mendonça F.F., Scacchetti P.C., Oliveira C., Foresti F. Molecular and cytogenetic analyses of cryptic species within the Synbranchus marmoratus Bloch, 1795 (Synbranchiformes: Synbranchidae) grouping: Species delimitations, karyotypic evolution and intraspecific diversification. Neotrop. Ichthyol. 2014;12:903–911. doi: 10.1590/1982-0224-20140039. DOI

Cioffi M.B., Bertollo L.A.C. Chromosomal distribution and evolution of repetitive DNAs in fish. Genome Dyn. 2012;7:197–221. doi: 10.1159/000337950. PubMed DOI

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

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

Castro J., Rodriguez S., Pardo B.G., Sanchez L., Martinez P. Population analysis of an unusual NOR-site polymorphism in brown trout (Salmo trutta L.) Heredity. 2001;86:291–302. doi: 10.1046/j.1365-2540.2001.00834.x. PubMed DOI

Piscor D., Alves A.L., Parise-Maltempi P.P. Chromosomal microstructure diversity in three Astyanax (Characiformes, Characidae) species: Comparative analysis of the chromosomal locations of the 18S and 5S rDNAs. Zebrafish. 2015;12:81–90. doi: 10.1089/zeb.2014.1036. PubMed DOI

Traldi J.B., Vicari M.R., Martinez J.D.F., Blanco D.R., Lui R.L., 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

Da Silva A.F., Feldberg E., Moura Carvalho N.D., Hernández Rangel S.M., Schneider C.H., Carvalho-Zilse G.A., Fonsêca da Silva V., Gross M.C. Effects of environmental pollution on the rDNAomics of Amazonian fish. Environ. Pollut. 2019;252:180–187. doi: 10.1016/j.envpol.2019.05.112. PubMed DOI

Pereira C.S.A., Aboim M.A., Ráb P., Collares-Pereira M.J. 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

Cioffi M.B., Molina W.F., Artoni R.F., Bertollo L.A.C. Chromosomes as tools for discovering biodiversity—The case of Erythrinidae fish family. Recent Trends Cytogenet. Stud. Methodol. Appl. 2012:125–146. doi: 10.5772/35890. DOI

Prizon A.C., Bruschi D.P., Borin-Carvalho L.A., Cius A., Barbosa L.M., Ruiz H.B., Zawadzki C.H., Fenocchio A.S., Portela-Castro A.L.B. Hidden diversity in the populations of the armored catfish Ancistrus Kner, 1854 (Loricariidae, Hypostominae) from the Paraná River Basin revealed by molecular and cytogenetic data. Front. Genet. 2017;8:185. doi: 10.3389/fgene.2017.00185. PubMed DOI PMC

Nirchio M., Paim F.G., Milana V., Rossi A.R., Oliveira C. Identification of a new mullet species complex based on an integrative molecular and cytogenetic investigation of Mugil hospes (Mugilidae: Mugiliformes) Front. Genet. 2018;9:17. doi: 10.3389/fgene.2018.00017. PubMed DOI PMC

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

Zhang C., Ye L., Chen Y., Xiao J., Wu Y., Tao M., Xiao Y., Liu S. 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

Zhu H.P., Ma D.M., Gui J.F. 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

Li Y.J., Tian Y., Zhang M.Z., Tian P.P., Yu Z., Abe S., Arai K. 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

Da Silva M., Matoso D.A., Ludwig L.A.M., Gomes E., Almeida M.C., Vicari M.R., Artoni R.F. Natural triploidy in Rhamdia quelen identified by cytogenetic monitoring in Iguaçu basin, southern Brazil. Environ. Biol. Fishes. 2011;91:361–366. doi: 10.1007/s10641-011-9794-2. DOI

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

Symonová R., Majtánová Z., Sember A., Staaks G.B., Bohlen J., Freyhof J., Rábová M., Ráb P. 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

Lima-Filho P.A., Bertollo L.A.C., Cioffi M.B., Costa G.W.W.F., Molina W.F. Karyotype divergence and spreading of 5S rDNA sequences between genomes of two species: Darter and emerald gobies (Ctenogobius, Gobiidae) Cytogenet. Genome Res. 2014;142:197–203. doi: 10.1159/000360492. PubMed DOI

Mazzei F., Ghigliotti L., Bonillo C., Coutanceau J.-P., Ozouf-Costaz C., Pisano E. Chromosomal patterns of major and 5S ribosomal DNA in six icefish species (Perciformes, Notothenioidei, Channichthyidae) Polar Biol. 2004;28:47–55. doi: 10.1007/s00300-004-0642-0. DOI

Ziemniczak K., Barros A.V., Rosa K.O., Nogaroto V., Almeida M.C., Cestari M.M., Moreira-Filho O., Artoni R.F., Vicari M.R. Comparative cytogenetics of Loricariidae (Actinopterygii: Siluriformes): Emphasis in Neoplecostominae and Hypoptopomatinae. Ital. J. Zool. 2012;79:492–501. doi: 10.1080/11250003.2012.676677. DOI

Piscor D., Fernandes C.A., Parise-Maltempi P.P. Conserved number of U2 snDNA sites in Piabina argentea, Piabarchus stramineus and two Bryconamericus species (Characidae, Stevardiinae) Neotrop. Ichthyol. 2018;16:e170066. doi: 10.1590/1982-0224-20170066. DOI

Yano C.F., Merlo M.A., Portela-Bens S., Cioffi M.B., Bertollo L.A.C., Santos-Júnior C.D., Rebordinos L., Esteban M.A., Albert J.S. Evolutionary dynamics of multigene families in Triportheus (Characiformes, Triportheidae): A transposon mediated mechanism? Front. Mar. Sci. 2020;7:6. doi: 10.3389/fmars.2020.00006. DOI

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

He W., Qin Q., Liu S., Li T., Wang J., Xiao J., Xie L., Zhang C., Liu Y. 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

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

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

Gromicho M., Coutanceau J.-P., Ozouf-Costaz C., Collares-Pereira M.J. 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

Pereira C.S.A., Ráb P., Collares-Pereira M.J. 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 A.R., Milana V., Hett A.K., 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

Singh M., Kumar R., Nagpure N.S., Kushwaha B., Mani I., Lakra W.S. 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

Libertini A., Sola L., Rampin M., Rossi A.R., 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

Han C.C., Yen T.B., Chen N.C., Tseng M.C. Comparative studies of 5S rDNA profiles and Cyt b sequences in two Onychostoma species (Cyprinidae) Int. J. Mol. Sci. 2015;16:29663–29672. doi: 10.3390/ijms161226193. PubMed DOI PMC

Kirtiklis L., Porycka K., Boroń A., Coutanceau J.-P., Dettai A. Use of the chromosomal co-location of the minor 5S and the major 28S rDNA as a cytogenetic marker within the genus Leuciscus (Pisces, Cyprinidae) Folia Biol. 2010;58:245–249. doi: 10.3409/fb58_3-4.245-249. PubMed DOI

Merlo M.A., Cross I., Rodríguez-Rúa A., Manchado M., Rebordinos L. First approach to studying the genetics of the meagre (Argyrosomus regius; Asso, 1801) using three multigene families. Aquac. Res. 2013;44:974–984. doi: 10.1111/j.1365-2109.2012.03103.x. DOI

Scacchetti P.C., Utsunomia R., Pansonato-Alves J.C. 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

Yano C.F., Bertollo L.A.C., Rebordinos L., Merlo M.A., Liehr T., Portela-Bens S., Cioffi M.B. 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

Araya-Jaime C., Mateussi N.T.B., Utsunomia R., Costa-Silva G.J., 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

Ponzio J.C., Piscor D., Parise-Maltempi P.P. Chromosomal locations of U2 snDNA clusters in Megaleporinus, Leporinus and Schizodon (Characiformes: Anostomidae) Biologia. 2018;73:295–298. doi: 10.2478/s11756-018-0031-8. DOI

Cabral-de-Mello D.C., Valente G.T., Nakajima R.T., Martins C. Genomic organization and comparative chromosome mapping of the U1 snRNA gene in cichlid fish, with an emphasis in Oreochromis niloticus. Chromosome Res. 2012;20:279–292. doi: 10.1007/s10577-011-9271-y. PubMed DOI

Carvalho P.C., Oliveira E.A., Bertollo L.A.C., Yano C.F., Al-Rikabi A.B.H., Cioffi M.B. First chromosomal analysis in Hepsetidae (Actinopterygii, Characiformes): Insights into relationship between African and Neotropical fish groups. Front. Genet. 2017;8:203. doi: 10.3389/fgene.2017.00203. PubMed DOI PMC

García-Souto D., Troncoso T., Pérez M., Pasantes J.J. Molecular cytogenetic analysis of the european hake Merluccius merluccius (Merlucciidae, Gadiformes): U1 and U2 snRNA gene clusters map to the same location. PLoS ONE. 2015;10:e0146150. doi: 10.1371/journal.pone.0146150. PubMed DOI PMC

Piscor D., Paiz L.M., Baumgärtner L., Cerqueira F.J., Fernandes C.A., Lui R.L., Parise-Maltempi P.P., Margarido V.P. Chromosomal mapping of repetitive sequences in Hyphessobrycon eques (Characiformes, Characidae): A special case of the spreading of 5S rDNA clusters in a genome. Genetica. 2020;148:25–32. doi: 10.1007/s10709-020-00086-3. PubMed DOI

Usso M.C., dos Santos A.R., Gouveia J.G., Frantine-Silva W., Araya-Jaime C., Oliveira M.L.M., Foresti F., Giuliano-Caetano L., Dias A.L. Genetic and chromosomal differentiation of Rhamdia quelen (Siluriformes, Heptapteridae) revealed by repetitive molecular markers and DNA barcoding. Zebrafish. 2019;16:87–97. doi: 10.1089/zeb.2018.1576. PubMed DOI

Cremer M., Von Hase J., Volm T., Brero A., Kreth G., Walter J., Fischer C., Solovei I., Cremer C., Cremer T. Non-random radial higher-order chromatin arrangements in nuclei of diploid human cells. Chromosome Res. 2001;9:541–567. doi: 10.1023/A:1012495201697. PubMed DOI

Úbeda-Manzanaro M., Merlo M.A., Palazón J.L., Cross I., Sarasquete C., Rebordinos L. Chromosomal mapping of the major and minor ribosomal genes, (GATA)n and U2 snRNA gene by double-colour FISH in species of the Batrachoididae family. Genetica. 2010;138:787–794. doi: 10.1007/s10709-010-9460-1. PubMed DOI

Malimpensa G.C., Traldi J.B., Toyama D., Henrique-Silva F., Vicari M.R., Moreira-Filho O. Chromosomal mapping of repeat DNA in Bergiaria westermanni (Pimelodidae, Siluriformes): Localization of 45S rDNA in B chromosomes. Cytogenet. Genome Res. 2018;154:99–106. doi: 10.1159/000487652. PubMed DOI

Manchado M., Zuasti E., Cross I., Merlo A., Infante C., Rebordinos L. Molecular characterization and chromosomal mapping of the 5S rRNA gene in Solea senegalensis: A new linkage to the U1, U2, and U5 small nuclear RNA genes. Genome. 2006;49:79–86. doi: 10.1139/g05-068. PubMed DOI

Ruiz-Herrera A., Nergadze S.G., Santagostino M., Giulotto E. Telomeric repeats far from the ends: Mechanisms of origin and role in evolution. Cytogenet. Genome Res. 2009;122:219–228. doi: 10.1159/000167807. PubMed DOI

Zhou M., Kang Y., Li Y.C., Zhou T. Studies on silver-stained karyotypes of 7 species in Cyprinidae (Pisces) Zool. Res. 1988;9:225–229. (In Chinese)

Ren X.H., Yu X.J. Characterization of nucleolar organizer regions of twelve species of Chinese cyprinid fishes. Caryologia. 1993;46:201–207. doi: 10.1080/00087114.1993.10797260. DOI

Li Y.C., Li K., Hong Y.H., Gui J.F., Zhou T. Studies on karyotypes of Chinese cyprinid fishes. VII. Karyotypic analyses of seven species in the subfamily Leuciscinae with a consideration for the phylogenetic relationships of some cyprinid fishes concerned. Acta Genet. Sin. 1985;12:367–372. (In Chinese)

Li K., Li Y.C., Zhou M., Zhou T. Studies on the karyotypes of Chinese cyprinid fishes. II. Karyotypes of four species of Xenocyprininae. Acta Zool. Sin. 1983;29:207–213. (In Chinese)

Zan R.G., Song Z. Analysis and comparison between the karyotypes of Ctenopharyngodon idella and Megalobrama amblycephala. Acta Genet. Sin. 1979;6:205–210. (In Chinese)

Lu R.H., Li Y.J., Xu K.S. A chromosome study of Megalobrama amblycephala. Oceanol. Limnol. Sin. 1984;15:487–492. (In Chinese)

Liu Y.U. On the karyotype of the grass-carp Ctenopharyngodon Idella. Acta Zool. Sin. 1980;26:14–16. (In Chinese)

Lou Y., Zhang K., Wu Y., Wang Y. Studies on karyotype of black carp (Mylopharyngodon piceus) J. Fish. China. 1983;7:77–81. (In Chinese)

Arai R. Fish Karyotypes: A Check List. 1st ed. Springer; Tokyo, Japan: 2011.

Ráb P., Crossman E.J. Chromosomal NOR phenotypes in North American pikes and pickerels, genus Esox with notes on Umbridae (Euteleostei: Esocae) Can. J. Zool. 1994;72:1951–1956. doi: 10.1139/z94-265. DOI

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

Phillips R.B., Ráb P. Chromosome evolution in the Salmonidae (Pisces): An update. Biol. Rev. Camb. Philos. Soc. 2001;76:1–25. doi: 10.1017/S1464793100005613. PubMed DOI

Dion-Côté A.-M., Symonová R., Lamaze F., Pelikánová Š., Ráb P., Bernatchez L. Standing chromosomal variation in Lake Whitefish species pairs: The role of historical contingency and relevance for speciation. Mol. Ecol. 2017;26:178–192. doi: 10.1111/mec.13816. PubMed DOI

Barby F.F., Bertollo L.A.C., Oliveira E.A., Yano C.F., Hatanaka T., Ráb P., Sember A., Ezaz T., Artoni R.F., Liehr T., et al. Emerging patterns of genome organization in Notopteridae species (Teleostei, Osteoglossiformes) as revealed by Zoo-FISH and Comparative Genomic Hybridization (CGH) Sci. Rep. 2019;9:1112. doi: 10.1038/s41598-019-38617-4. PubMed DOI PMC

Molina W.F. Chromosomal changes and stasis in marine fish groups. In: Pisano E., Ozouf-Costaz C., Foresti F., Kapoor B.G., editors. Fish Cytogenetics. 1st ed. Science Publishers; Enfield, CT, USA: 2007. pp. 69–110.

Motta-Neto C.C., Cioffi M.B., Bertollo L.A.C., Molina W.F. Extensive chromosomal homologies and evidence of karyotypic stasis in Atlantic grunts of the genus Haemulon (Perciformes) J. Exp. Mar. Biol. Ecol. 2011;401:75–79. doi: 10.1016/j.jembe.2011.02.044. DOI

Motta-Neto C.C., Cioffi M.B., Bertollo L.A.C., Molina W.F. Molecular cytogenetic analysis of Haemulidae fish (Perciformes): Evidence of evolutionary conservation. J. Exp. Mar. Biol. Ecol. 2011;407:97–100. doi: 10.1016/j.jembe.2011.07.014. DOI

Motta-Neto C.C., Lima-Filho P.A., Araújo W.C., Bertollo L.A.C., Molina W.F. Differentiated evolutionary pathways in Haemulidae (Perciformes): Karyotype stasis versus morphological differentiation. Rev. Fish Biol. Fish. 2012;22:457–465. doi: 10.1007/s11160-011-9236-4. DOI

Motta-Neto C.C., Cioffi M.B., Costa G.W.W.F., Amorim K.D.J., Bertollo L.A.C., Artoni R.F., Molina W.F. Overview on karyotype stasis in Atlantic grunts (Eupercaria, Haemulidae) and the evolutionary extensions for other marine fish groups. Front. Mar. Sci. 2019;6:628. doi: 10.3389/fmars.2019.00628. DOI

Ellegren H. Evolutionary stasis: The stable chromosomes of birds. Trends Ecol. Evol. 2010;25:283–291. doi: 10.1016/j.tree.2009.12.004. PubMed DOI

Tian Y., Nie W., Wang J., Ferguson-Smith M.A., Yang F. Chromosome evolution in bears: Reconstructing phylogenetic relationships by cross-species chromosome painting. Chromosome Res. 2004;12:55–63. doi: 10.1023/B:CHRO.0000009299.59969.fa. PubMed DOI

Razin S.V., Gavrilov A.A., Vassetzky Y.S., Ulianov S.V. Topologically-associating domains: Gene warehouses adapted to serve transcriptional regulation. Transcription. 2016;7:84–90. doi: 10.1080/21541264.2016.1181489. PubMed DOI PMC

Rosin L.F., Crocker O., Isenhart R.L., Nguyen S.C., Xu Z., Joyce E.F. Chromosome territory formation attenuates the translocation potential of cells. eLife. 2019;8:e49553. doi: 10.7554/eLife.49553. PubMed DOI PMC

Alves M.J., Coelho M.M., Collares-Pereira M.J. Evolution in action through hybridization and polyploid in an Iberain freshwater fish: A genetic review. Genetica. 2001;111:375–385. doi: 10.1023/A:1013783029921. PubMed DOI

FISH mapping in Xenopus pygmaeus refines understanding of genomic rearrangements and reveals jumping NORs in African clawed frogs

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

Cytogenetic Analysis of the Fish Genus Carassius Indicates Divergence, Fission, and Segmental Duplication as Drivers of Tandem Repeat and Microchromosome Evolution

Consequences of polyploidy and divergence as revealed by cytogenetic mapping of tandem repeats in African clawed frogs (Xenopus, Pipidae)

A Fish of Multiple Faces, Which Show Us Enigmatic and Incredible Phenomena in Nature: Biology and Cytogenetics of the Genus Carassius

Measurement of Chromosomal Arms and FISH Reveal Complex Genome Architecture and Standardized Karyotype of Model Fish, Genus Carassius

Present and Future Salmonid Cytogenetics