Salmonids are extremely important economically and scientifically; therefore, dynamic developments in their research have occurred and will continue occurring in the future. At the same time, their complex phylogeny and taxonomy are challenging for traditional approaches in research. Here, we first provide discoveries regarding the hitherto completely unknown cytogenetic characteristics of the Anatolian endemic flathead trout, Salmo platycephalus, and summarize the presently known, albeit highly complicated, situation in the genus Salmo. Secondly, by outlining future directions of salmonid cytogenomics, we have produced a prototypical virtual karyotype of Salmo trutta, the closest relative of S. platycephalus. This production is now possible thanks to the high-quality genome assembled to the chromosome level in S. trutta via soft-masking, including a direct labelling of repetitive sequences along the chromosome sequence. Repetitive sequences were crucial for traditional fish cytogenetics and hence should also be utilized in fish cytogenomics. As such virtual karyotypes become increasingly available in the very near future, it is necessary to integrate both present and future approaches to maximize their respective benefits. Finally, we show how the presumably repetitive sequences in salmonids can change the understanding of the overall relationship between genome size and G+C content, creating another outstanding question in salmonid cytogenomics waiting to be resolved.

Department of Bioinformatics Wissenschaftszentrum Weihenstephan Technische Universität München 85354 Freising Germany

Department of Molecular Biology and Genetics Faculty of Science Bartin University Bartin 74000 Turkey

Department of Molecular Biology and Genetics Faculty of Science University of Ahi Evran Kirsehir 40200 Turkey

Laboratory of Fish Genetics Institute of Animal Physiology and Genetics Czech Academy of Sciences 27721 Liběchov Czech Republic

Physics and Biology Unit Okinawa Institute of Science and Technology Graduate University Onna Okinawa 904 0495 Japan

Zobrazit více v PubMed

Delling B., Doario I. Systematics of the trouts endemic to Moroccan lakes, with description of a new species (Teleostei: Salmonidae) Ichthyol. Explor. Freshw. 2005;16:49–64.

Doadrio I., Perea S., Yahyaoui A. Two new species of atlantic trout (Actynopterygii, Salmonidae) from Morocco. Graellsia. 2015;71:e031. doi: 10.3989/graellsia.2015.v71.142. DOI

Doadrio I. Ictiofauna Continental Española: Bases Para Su Seguimiento. Ministerio de Medio Ambiente y Medio Rural y Marino, Centro de Publicaciones; Madrid, Spain: 2011.

Kottelat M., Freyhof J. Handbook of European Freshwater Fishes. Publications Kottelat; Cornol, Switzerland: 2007.

Delling B. Diversity of western and southern Balkan trouts, with the description of a new species from the Louros River, Greece (Teleostei: Salmonidae) Ichthyol. Explor. Freshw. 2010;21:331.

Turan D., Kottelat M., Engin S. Two new species of trouts, resident and migratory, sympatric in streams of northern Anatolia (Salmoniformes: Salmonidae) Ichthyol. Explor. Freshw. 2009;20:333–364.

Turan D., Kottelat M., Bektas Y. Salmo tigridis, a new species of trout from the Tigris River, Turkey (Teleostei: Salmonidae) Zootaxa. 2011;2993:23–33. doi: 10.11646/zootaxa.2993.1.2. DOI

Turan D., Kottelat M., Engin S. The trouts of the Mediterranean drainages of southern Anatolia, Turkey, with description of three new species (Teleostei: Salmonidae) Ichthyol. Explor. Freshw. 2012;23:219.

Turan D., Doğan E., Kaya C., Kanyılmaz M. Salmo kottelati, a new species of trout from Alakır Stream, draining to the Mediterranean in southern Anatolia, Turkey (Teleostei, Salmonidae) ZooKeys. 2014:135–151. doi: 10.3897/zookeys.462.8177. PubMed DOI PMC

Turan D., Kottelat M., Kaya C. Salmo munzuricus, a new species of trout from the Euphrates River drainage, Turkey (Teleostei: Salmonidae) Ichthyol. Explor. Freshw. 2017;28:55–63.

Çiçek E., Fricke R., Sungur S., Eagderi S. Endemic freshwater fishes of Turkey. FishTaxa. 2018;3:1–39.

Lobón-Cerviá J., Sanz N. Brown trout: Biology, ecology and management. John Wiley & Sons; Hoboken, NJ, USA: 2017.

Lobón-Cerviá J., Esteve M., Berrebi P., Duchi A., Lorenzoni M., Young K.A. Trout and char of the world. American Fisheries Society; Bethesda, MA, USA: 2019. Trout and char of central and Southern Europe and Northern Africa.

Behnke R.J. A new subgenus and species of trout, Salmo (Platysalmo) platycephalus, from southcentral Turkey, with comments on the classification of the subfamily Salmoninae. Mitt. Hamburg. Zool. Mus. Inst. 1968;66:1–15.

Kara C., Alp A., Gürlek M.E. Morphological variations of the trouts (Salmo trutta and Salmo platycephalus) in the rivers of Ceyhan, Seyhan and Euphrates, Turkey. Turk. J. Fish. Aquat. Sci. 2011;11:77–85.

Kara C., Alp A., Can M.F. Growth and reproductive properties of flathead trout (Salmo platycephalus Bhenke, 1968) population from Zamantı Stream, Seyhan River, Turkey. Turk. J. Fish. Aquat. Sci. 2011;11:367–375.

Tarkan A.N., Tarkan A.S., Bilge G., Gaygusuz Ö., Gürsoy Ç. Threatened fishes of the world: Salmo platycephalus Behnke, 1968 (Salmonidae) Environ. Biol. Fishes. 2008;81:371–372. doi: 10.1007/s10641-007-9213-x. DOI

Phillips R., 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

Mazzuchelli J., Kocher T.D., Yang F., Martins C. Integrating cytogenetics and genomics in comparative evolutionary studies of cichlid fish. BMC Genom. 2012;13:463. doi: 10.1186/1471-2164-13-463. PubMed DOI PMC

De Oliveira E.A., Bertollo L.A.C., Ráb P., Ezaz T., Yano C.F., Hatanaka T., Jegede O.I., Tanomtong A., Liehr T., Sember A., et al. Cytogenetics, genomics and biodiversity of the South American and African Arapaimidae fish family (Teleostei, Osteoglossiformes) PLoS ONE. 2019;14:e0214225. doi: 10.1371/journal.pone.0214225. PubMed DOI PMC

Pennell W., Prouzet K. Salmonid fish: Bology, conservation status, and economic importance of wild and cultured stocks. Fish. Aquac. P Safran Enciclopedia Life Suport Syst. 2009;3:42–65.

Gregory T.R. Animal Genome Size Database. [(accessed on 6 December 2020)];2020 Available online: http://www.genomesize.com.

Koop B.F., Davidson W.S. Genomics and the genome duplication in Salmonids. In: Tsukamoto K., Kawamura R., Takeuchi T., Beard T.D. Jr., Kaiser M.J., editors. Fisheries for Global Welfare and Environment. 5th World Fisheries Congress; Tokyo, Japan: 2008. pp. 77–86.

Davidson W.S., Koop B.F., Jones S.J., Iturra P., Vidal R., Maass A., Jonassen I., Lien S., Omholt S.W. Sequencing the genome of the Atlantic salmon (Salmo salar) Genome Biol. 2010;11:403. doi: 10.1186/gb-2010-11-9-403. PubMed DOI PMC

Hunt S.E., McLaren W., Gil L., Thormann A., Schuilenburg H., Sheppard D., Parton A., Armean I.M., Trevanion S.J., Flicek P., et al. Ensembl variation resources. Database. 2018;2018 doi: 10.1093/database/bay119. PubMed DOI PMC

Matoulek D., Borůvková V., Ocalewicz K., Symonová R. GC and repeats profiling along chromosomes — The future of fish compositional cytogenomics. Genes. 2020;11 this special issue. PubMed PMC

Canapa A., Barucca M., Biscotti M.A., Forconi M., Olmo E. Transposons, genome size, and evolutionary insights in animals. Cytogenet. Genome Res. 2015;147:217–239. doi: 10.1159/000444429. PubMed DOI

Lien S., Koop B.F., Sandve S.R., Miller J.R., Kent M.P., Nome T., Hvidsten T.R., Leong J.S., Minkley D.R., Zimin A., et al. The Atlantic salmon genome provides insights into rediploidization. Nature. 2016;533:200–205. doi: 10.1038/nature17164. PubMed DOI PMC

Symonová R., Suh A. Nucleotide composition of transposable elements likely contributes to AT/GC compositional homogeneity of teleost fish genomes. Mobile DNA. 2019;10:49. doi: 10.1186/s13100-019-0195-y. PubMed DOI PMC

Borůvková V., Howell W., Matoulek D., Symonová R. Quantitative approach to fish cytogenetics in the context of vertebrate genome evolution. Genes. 2020;11 this special issue. PubMed PMC

Ráb P., Roth P. Cold-blooded vertebrates. In: Balíček P., Forejt J., Rubeš J., editors. Methods of Chromosome Analysis. Cytogenetic Section of Czechoslovakian Biological Society Publishers; Brno, Czech Republic: 1988. pp. 115–124.

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. Cytogen. 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

Rábová M., Völker M., Pelikánová Š., Ráb P. Sequential chromosome banding in fishes. In: Ozouf-Costaz C., Pisano E., Foresti F., de Almeida Toledo L.F., editors. Fish Cytogenetic Techniques. CRC Press; Boca Raton, FL, USA: 2015. pp. 92–102.

Komiya H., Takemura S. Nucleotide sequence of 5S ribosomal RNA from rainbow trout (Salmo gairdnerii) liver. J. Biochem. 1979;86:1067–1080. doi: 10.1093/oxfordjournals.jbchem.a132601. PubMed DOI

White T.J., Bruns T., Lee S., Taylor J. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis M., Gelfand J., Sninsky J., White T., editors. PCR Protocols: A Guide to Methods and Applications. Academic Press; Orlando, FL, USA: 1990. pp. 315–322.

Symonová R., Sember A., Majtánová Z., Ráb P. Characterization of fish genomes by GISH and CGH. In: Ozouf-Costaz C., Pisano E., Foresti F., de Almeida L., editors. Fish Cytogenetic Techniques. CRC Press; Boca Raton, FL, USA: 2015. pp. 118–131.

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’évolution de la formule chromosomiale chez les vertébrés. Experientia. 1945;1:78–86. doi: 10.1007/BF02156807. DOI

Team R.C. R: A Language and Environment for Statistical Computing, version 2.6.2. R Foundation for Statistical Computing; Vienna, Austria: 2013.

Sušnik S., Schöffmann J., Snoj A. Phylogenetic position of Salmo (Platysalmo) platycephalus Behnke 1968 from south-central Turkey, evidenced by genetic data. J. Fish. Biol. 2004;64:947–960. doi: 10.1111/j.1095-8649.2004.0363.x. DOI

Bănărescu P. Zoogeography of Fresh Waters. Volume 2: Distribution and Dispersal of Freshwater Animals in North America and Eurasia. Aula-Verlag; Wiebelsheim, Germany: 1991.

Budy P., Gaeta J.W. Brown trout: Biology, ecology, and management. John Wiley and Sons Ltd.; Hoboken, NJ, USA: 2018. Brown trout as an invader: A Synthesis of problems and perspectives in North America; pp. 525–534.

Jones P., Closs G. Brown Trout: Biology, Ecology, and Management. John Wiley and Sons Ltd.; Hoboken, NJ, USA: 2018. The introduction of brown trout to New Zealand and their impact on native fish communities; pp. 545–567.

Jellyman P.G., McHugh P.A., Simon K.S., Thompson R.M., McIntosh A.R. Brown Trout: Biology, Ecology and Management. John Wiley and Sons Ltd.; Hoboken, NJ, USA: 2017. The effects of brown trout on the trophic webs of New Zealand streams; pp. 569–598.

Casalinuovo M.A., Alonso M.F., Macchi P.J., Kuroda J.A. Brown Trout: Biology, Ecology, and Management. John Wiley and Sons Ltd.; Hoboken, NJ, USA: 2018. Brown trout in Argentina: History, interactions, and perspectives; pp. 599–622.

Weyl O.L., Ellender B.R., Ivey P., Jackson M.C., Tweddle D., Wasserman R.J., Woodford D.J., Zengeya T.A. Brown trout: Biology, ecology, and management. John Wiley and Sons Ltd.; Hoboken, NJ, USA: 2018. Africa: Brown trout introductions, establishment, current status, impacts and conflicts; pp. 623–639.

FAO Fisheries and Aquaculture—Statistics—Introduction. [(accessed on 6 November 2020)]; Available online: http://www.fao.org/fishery/statistics/en.

GAs M. Revue bibliographique sur la caryologie des Téléostéens. Etude critique des méthodes employées et des résultats obtenus. Biologie Médical. 1970;54:54–81. PubMed

Dettai A., Pruvost P. Fish Cytogenetic Techniques: Ray-Fin Fishes and Chondrichthyans. CRC Press Taylor and Francis Group; London, UK: 2015. Storage of Karyotyped Voucher Specimens and their Molecular Identification; p. 11.

Kohout J., Jašková I., Papoušek I., Šedivá A., Šlechta V. Effects of stocking on the genetic structure of brown trout, Salmo trutta, in Central Europe inferred from mitochondrial and nuclear DNA markers. Fish Manag. Ecol. 2012;19:252–263. doi: 10.1111/j.1365-2400.2011.00828.x. DOI

Leitwein M., Gagnaire P.A., Desmarais E., Guendouz S., Rohmer M., Berrebi P., Guinand B. Genome-wide nucleotide diversity of hatchery-reared Atlantic and Mediterranean strains of brown trout Salmo trutta compared to wild M editerranean populations. J. Fish. Biol. 2016;89:2717–2734. doi: 10.1111/jfb.13131. PubMed DOI

Mazik E.J., Toktosunov A.T. Karyotype of the Amu Darya trout Salmo trutta oxianus (Salmoniformes, Salmonidae) from Kyzylsu River. J. Zool. 1986;65:1582–1586.

Merlo S. Osservazioni cariologiche su Salmo carpio: (Con 1 tavola fuori testo) Ital. J. Zool. 1957;24:253–258.

Caputo V., Giovannotti M., Cerioni P.N., Splendiani A., Olmo E. Chromosomal study of native and hatchery trouts from Italy (Salmo trutta complex, Salmonidae): Conventional and FISH analysis. Cytogen. Gen. Res. 2009;124:51–62. doi: 10.1159/000200088. PubMed DOI

Karakousis Y., Paschos J., Triantaphyllidis C. Chromosomal studies in brown trout (Salmo trutta L.) populations. Cytobios. 1992;72:117–124.

Dimovska A. Chromosome complement of Ochrid trout (Salmo letnica Karaman) Godisen zb. Prirodno-matem. Fak. Univ. Skopje. 1959;12:115–135.

Al-Sabti K. Karyotypical studies in three Salmonidaae in Slovenia using leukocyte culture technique. Ichthyologia. 1983;15:41–46.

Al-Sabti K. Chromosomal studies by blood leukocyte culture technique on three salmonids from Yugoslavian waters. J. Fish. Biol. 1985;26:5–12. doi: 10.1111/j.1095-8649.1985.tb04234.x. DOI

Berberovic L., Curic M., Hadziselimovic R., Sofradzija A. Chromosome complement of Salmothymus obtusirostris oxyrhynchus (Steindachner) Acta Biol. Jug. Genet. 1970;2:55–63.

Sofradzija A. The chromosomes of the trout Salmo trutta m. fario and Salmo gairdneri. Godisnajak Bioloskog Instituta Univerziteta u Sarajevu. 1982;35:117–128.

Kaidanova T.I. Karyotype study of brown trout Salmo trutta morpha fario from Ropsha population. Voprosy Ichtiologii. 1975;15:1124–1128.

Jankun M. Standard karyotype of sea trout (Salmo trutta morpha trutta) based on replication banding patterns. Cytobios. 2000;103:79–89. PubMed

Woznicki P., Jankun M., Kucharczyk D., Boron A., Luczynski M. Cytogenetic characterization of sea trout (Salmo trutta) from Poland. Copeia. 1999;1999:501–505. doi: 10.2307/1447499. DOI

Woznicki P., Sanchez L., Martinez P., Pardo B.G., Jankun M. A population analysis of the structure and variability of NOR in Salmo trutta by Ag, CMA3 and ISH. Genetica. 2000;108:113–118. doi: 10.1023/A:1004055125295. PubMed DOI

Woznicki P., Jankun M., Luczynski M. Chromosome studies in brown trout (Salmo trutta m. fario) from Poland: Hypothetical evolution of the 11th, 12th and 14th chromosome pairs in the Salmo karyotype. Cytobios. 1997;91:2017–2214.

Dorofeeva E.A., Ruhkjan R.G. Divergence of Salmo ischchan Kessler in light of karyological and morphological characteristics. Voprosy Ichtiologii. 1982;22:36–48.

Ruhkjan R.G. Karyology and Origin of the Transcaucasian Trouts. Academy of Sciences Armenian SSR Press; Yerevan, Armenia: 1989. p. 166. (In Russian)

Raicu P., Taisescu E. Cytogenetic study in Salmo irideus and S. trutta fario. Cytologia. 1977;42:311–314. doi: 10.1508/cytologia.42.311. DOI

Dorofeeva E.A. Karyology and systematic status of Caspian and Black Sea salmons (Salmo trutta caspius Kessler, Salmo trutta labrax Pallas) Voprosy Ichtiologii. 1965;5:28–45.

Ruhkjan R.G. A comparative analysis of the karyotypes of the Sevan trout Salmo ischchan Kessler. Citologia. 1982;24:66–77.

Ruhkjan R.G. On the origin and species identity of alabalach trout (genus Salmo, Salmonidae) based on its karyological characteristics) Voprosy Ichtiologi. 1984;23:368–373.

Ruhkjan R.G. Karyotypes of brown trouts of Armenia Salmo trutta m. fario. Biol. J. Armenii. 1981;34:412–417.

Mořan P., Pendas A.M., García-Vázquez E., Linde A.R. Chromosomal and morphological analysis of two populations of Salmo trutta sbp. fario employed in repopulation. J. Fish Biol. 1989;35:839–843. doi: 10.1111/j.1095-8649.1989.tb03035.x. DOI

Martinez P., Vinas A., Bouza C., Arias J., Amaro R., Sánchez L. Cytogenetical characterization of hatchery stocks and natural populations of sea and brown trout from northwestern Spain. Heredity. 1991;66:9–17. doi: 10.1038/hdy.1991.2. DOI

Mayr B., Ráb P., Kalat M. Localisation of NORs and counterstain-enhanced fluorescence studies in Salmo gairdneri and Salmo trutta (Pisces, Salmonidae) Theoret. Appl. Genet. 1986;71:703–707. doi: 10.1007/BF00263267. PubMed DOI

Castro J., Rodríguez S., Arias J., Sánchez L., Martínez P. A population analysis of Robertsonian and Ag-NOR polymorphisms in brown trout (Salmo trutta) Theoret. Appl. Genetics. 1994;89:105–111. doi: 10.1007/BF00226990. PubMed DOI

Castro J., Viñas A., Sánchez L., Martínez P. Characterization of an atypical NOR site polymorphism in brown trout (Salmo trutta) with Ag- and CMA3-staining, and fluorescent in situ hybridization. Cytogenet. Genome Res. 1996;75:234–239. doi: 10.1159/000134491. PubMed DOI

Sánchez L., Martínez P., Bouza C., Viñas A. Chromosomal heterochromatin differentiation in Salmo trutta with restriction enzymes. Heredity. 1991;66:241–249. doi: 10.1038/hdy.1991.30. DOI

Hartley S.E., Horne M.T. Chromosome relationships in the genus Salmo. Chromosoma. 1984;90:229–237. doi: 10.1007/BF00292401. PubMed DOI

Gjedrem T., Eggum Å., Refstie T. Chromosomes of some salmonids and salmonid hybrids. Aquaculture. 1977;11:335–348. doi: 10.1016/0044-8486(77)90083-7. DOI

Zenzes M.T., Voiculescu I. C-banding patterns in Salmo trutta, a species of tetraploid origin. Genetica. 1975;45:531–536. doi: 10.1007/BF01772875. DOI

Nygren A., Nilsson B., Jahnke M. Cytological studies in Salmo trutta and Salmo alpinus. Hereditas. 1971;67:259–267. doi: 10.1111/j.1601-5223.1971.tb02378.x. PubMed DOI

Pendás A.M., Morán P., García-Vázquez E. Multi-chromosomal location of ribosomal RNA genes and heterochromatin association in brown trout. Chromosome Res. 1993;1:63–67. doi: 10.1007/BF00710608. 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 doi: 10.1159/000354832. 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

Majtánová Z., Unmack P.J., Prasongmaneerut T., Shams F., Srikulnath K., Ráb P., Ezaz T. Evidence of Interspecific Chromosomal Diversification in Rainbowfishes (Melanotaeniidae, Teleostei) Genes. 2020;11:818. doi: 10.3390/genes11070818. PubMed DOI PMC

Ráb P., Rábová M., Pereira C.S., Collares-Pereira M.J., Pelikánová Š. Chromosome studies of European cyprinid fishes: Interspecific homology of leuciscine cytotaxonomic marker—the largest subtelocentric chromosome pair as revealed by cross-species painting. Chromosome Res. 2008;16:863–873. doi: 10.1007/s10577-008-1245-3. PubMed DOI

Sušnik S., Snoj A., Wilson I.F., Mrdak D., Weiss S. Historical demography of brown trout (Salmo trutta) in the Adriatic drainage including the putative S. letnica endemic to Lake Ohrid. Mol. Phylogen. Evol. 2007;44:63–76. doi: 10.1016/j.ympev.2006.08.021. PubMed DOI

Phillips R.B., Matsuoka M.P., Konon I., Reed K.M., McEachran M. Phylogenetic Analysis of Mitochondrial and Nuclear Sequences Supports Inclusion of Acantholingua ohridana in the Genus Salmo. Copeia. 2000;2000:546–550. doi: 10.1643/0045-8511(2000)000[0546:PAOMAN]2.0.CO;2. DOI

Kottelat M. Freshwater fishes of western and central Europe. Biologia. 1997;52:1–271.

Behnke R.J. Native trout of western North America. Am. Fish. Soc. Monogr. USA. 1992;6:233–256.

FishBase. A Global Information System on Fishes. [(accessed on 6 November 2020)]; Available online: https://www.fishbase.se/home.htm.

Cortey M., Pla C., García-Marín J.-L. Historical biogeography of Mediterranean trout. Mol. Phylogenetics Evol. 2004;33:831–844. doi: 10.1016/j.ympev.2004.08.012. PubMed DOI

Marić S., Sušnik S., Simonović P., Snoj A. Phylogeographic study of brown trout from Serbia, based on mitochondrial DNA control region analysis. Genet. Sel. Evol. 2006;38:411. doi: 10.1186/1297-9686-38-4-411. PubMed DOI PMC

McKeown N.J., Hynes R.A., Duguid R.A., Ferguson A., Prodöhl P.A. Phylogeographic structure of brown trout Salmo trutta in Britain and Ireland: Glacial refugia, postglacial colonization and origins of sympatric populations. J. Fish. Biol. 2010;76:319–347. doi: 10.1111/j.1095-8649.2009.02490.x. PubMed DOI

Snoj A., Marić S., Bajec S.S., Berrebi P., Janjani S., Schöffmann J. Phylogeographic structure and demographic patterns of brown trout in North-West Africa. Mol. Phylogenetics Evol. 2011;61:203–211. doi: 10.1016/j.ympev.2011.05.011. PubMed DOI

Ninua L., Tarkhnishvili D., Gvazava E. Phylogeography and taxonomic status of trout and salmon from the Ponto-Caspian drainages, with inferences on European Brown Trout evolution and taxonomy. Ecol. Evol. 2018;8:2645–2658. doi: 10.1002/ece3.3884. PubMed DOI PMC

Tougard C., Justy F., Guinand B., Douzery E.J.P., Berrebi P. Salmo macrostigma (Teleostei, Salmonidae): Nothing more than a brown trout (S. trutta) lineage? J. Fish. Biol. 2018;93:302–310. doi: 10.1111/jfb.13751. PubMed DOI

Schöffmann J., Sušnik S., Snoj A. Phylogenetic origin of Salmo trutta L. 1758 from Sicily, based on mitochondrial and nuclear DNA analyses. Hydrobiologia. 2007;575:51–55. doi: 10.1007/s10750-006-0281-2. DOI

Apostolidis A.P., Loukovitis D., Tsigenopoulos C.S. Genetic characterization of brown trout (Salmo trutta) populations from the Southern Balkans using mtDNA sequencing and RFLP analysis. Hydrobiologia. 2008;600:169–176. doi: 10.1007/s10750-007-9229-4. DOI

Gratton P., Allegrucci G., Gandolfi A., Sbordoni V. Genetic differentiation and hybridization in two naturally occurring sympatric trout Salmo spp. forms from a small karstic lake. J. Fish. Biol. 2013;82:637–657. doi: 10.1111/jfb.12022. PubMed DOI

Berrebi P., Retif X., Bouhbouh S. Genetic evidence of unisexual reproduction in the Moroccan hexaploid barbel Labeobarbus fritschi. Folia Zoo. 2013;62:257–263. doi: 10.25225/fozo.v62.i4.a2.2013. DOI

Delling B., Sabatini A., Muracciole S., Tougard C., Berrebi P. Morphologic and genetic characterisation of Corsican and Sardinian trout with comments on Salmo taxonomy. Knowl. Manag. Aquat. Ecosyst. 2020:21. doi: 10.1051/kmae/2020013. DOI

Dion-Côté A.-M., Symonová R., Lamaze F.C., 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

Mandáková T., Heenan P.B., Lysak M.A. Island species radiation and karyotypic stasis in Pachycladon allopolyploids. BMC Evol. Biol. 2010;10:367. doi: 10.1186/1471-2148-10-367. PubMed DOI PMC

Bomfleur B., McLoughlin S., Vajda V. Fossilized nuclei and chromosomes reveal 180 million years of genomic stasis in royal ferns. Science. 2014;343:1376–1377. doi: 10.1126/science.1249884. PubMed DOI

Samad N.A., Dagher-Kharrat M.B., Hidalgo O., Zein R.E., Douaihy B., Siljak-Yakovlev S. Unlocking the karyological and cytogenetic diversity of Iris from Lebanon: Oncocyclus section shows a distinctive profile and relative stasis during its continental radiation. PLoS ONE. 2016;11:e0160816. doi: 10.1371/journal.pone.0160816. PubMed DOI PMC

Sessions S.K., Kezer J. Chapter 5—Evolutionary cytogenetics of Bolitoglossine Salamanders (Family Plethodontidae) In: Green D.M., Sessions S.K., editors. Amphibian Cytogenetics and Evolution. Academic Press; San Diego, CA, USA: 1991. pp. 89–130.

Odierna G., Aprea G., Capriglion T., Castellano S., Balletto E. Evidence for chromosome and Pst I satellite DNA family evolutionary stasis in the Bufo viridis group (Amphibia, Anura) Chromosome Res. 2004;12:671–681. doi: 10.1023/B:CHRO.0000045746.59805.58. PubMed 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

Ráb P., Crossman E.J. Chromosomal NOR phenotypes in North American pikes and pickerels, genus Esox, with notes on the Umbridae (Euteleostei: Esocae) Canadian J. Zool. 2011 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

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

Bianco P.G., Aprea G., Balletto E., Capriglione T., Fulgione D., Odierna G. The karyology of the cyprinid genera Scardinius and Rutilus in southern Europe. Ichthyol. Res. 2004;51:274–278. doi: 10.1007/s10228-004-0221-y. 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

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

Sember A., Pelikánová Š., de Bello Cioffi M., Šlechtová V., Hatanaka T., Do Doan H., Knytl M., Ráb P. Taxonomic diversity not associated with gross karyotype differentiation: The case of bighead carps, Genus Hypophthalmichthys (Teleostei, Cypriniformes, Xenocyprididae) Genes. 2020;11:479. doi: 10.3390/genes11050479. 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. Science Publishers; Enfield, NH, USA: 2007. pp. 69–110.

Motta Neto C.C., Cioffi M.D.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 doi: 10.3389/fmars.2019.00628. DOI

Neto C.C.M., 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

Neto C.C.M., 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

da Costa G.W.W.F., de Bello Cioffi M., Bertollo L.A.C., Molina W.F. 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

Majtánová Z., Indermaur A., Bitja Nyom A.R., Ráb P., Musilová Z. Adaptive radiation from a chromosomal perspective: Evidence of chromosome set stability in cichlid fishes (Cichlidae: Teleostei) from the Barombi Mbo Lake, Cameroon. Int. J. Mol. Sci. 2019;20:4994. doi: 10.3390/ijms20204994. PubMed DOI PMC

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

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

Nelson J.S., Grande T.C., Wilson M.V.H. Fishes of the World. 5th ed. Wiley; Hoboken, NJ, USA: 2016.

Fujiwara A., Abe S., Yamaha E., Yamazaki F., Yoshida M.C. Chromosomal localization and heterochromatin association of ribosomal RNA gene loci and silver-stained nucleolar organizer regions in salmonid fishes. Chrom. Res. 1998;6:463–471. doi: 10.1023/A:1009200428369. PubMed DOI

Symonová R., Majtánová Z., Sember A., Staaks G.B.O., 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

Dion-Côté A.-M., Symonová R., Ráb P., Bernatchez L. Reproductive isolation in a nascent species pair is associated with aneuploidy in hybrid offspring. Proc. Royal Soc. B. 2015;282:20142862. doi: 10.1098/rspb.2014.2862. PubMed DOI PMC

Bernardi G. Structural and Evolutionary Genomics: Natural Selection in Genome Evolution. Elsevier; Amsterdam, The Netherlands: 2005.

Symonová R. Integrative rDNAomics—Importance of the oldest repetitive fraction of the Eukaryote genome. Genes. 2019;10:345. doi: 10.3390/genes10050345. 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

Abandoning the Isochore Theory Can Help Explain Genome Compositional Organization in Fish

Advances in Vertebrate (Cyto)Genomics Shed New Light on Fish Compositional Genome Evolution

Revisiting the Karyotypes of Alligators and Caimans (Crocodylia, Alligatoridae) after a Half-Century Delay: Bridging the Gap in the Chromosomal Evolution of Reptiles

Quantitative Approach to Fish Cytogenetics in the Context of Vertebrate Genome Evolution