Lebiasinidae is a Neotropical freshwater family widely distributed throughout South and Central America. Due to their often very small body size, Lebiasinidae species are cytogenetically challenging and hence largely underexplored. However, the available but limited karyotype data already suggested a high interspecific variability in the diploid chromosome number (2n), which is pronounced in the speciose genus Nannostomus, a popular taxon in ornamental fish trade due to its remarkable body coloration. Aiming to more deeply examine the karyotype diversification in Nannostomus, we combined conventional cytogenetics (Giemsa-staining and C-banding) with the chromosomal mapping of tandemly repeated 5S and 18S rDNA clusters and with interspecific comparative genomic hybridization (CGH) to investigate genomes of four representative Nannostomus species: N. beckfordi, N. eques, N. marginatus, and N. unifasciatus. Our data showed a remarkable variability in 2n, ranging from 2n = 22 in N. unifasciatus (karyotype composed exclusively of metacentrics/submetacentrics) to 2n = 44 in N. beckfordi (karyotype composed entirely of acrocentrics). On the other hand, patterns of 18S and 5S rDNA distribution in the analyzed karyotypes remained rather conservative, with only two 18S and two to four 5S rDNA sites. In view of the mostly unchanged number of chromosome arms (FN = 44) in all but one species (N. eques; FN = 36), and with respect to the current phylogenetic hypothesis, we propose Robertsonian translocations to be a significant contributor to the karyotype differentiation in (at least herein studied) Nannostomus species. Interspecific comparative genome hybridization (CGH) using whole genomic DNAs mapped against the chromosome background of N. beckfordi found a moderate divergence in the repetitive DNA content among the species' genomes. Collectively, our data suggest that the karyotype differentiation in Nannostomus has been largely driven by major structural rearrangements, accompanied by only low to moderate dynamics of repetitive DNA at the sub-chromosomal level. Possible mechanisms and factors behind the elevated tolerance to such a rate of karyotype change in Nannostomus are discussed.

Departamento de Genética e Evolução Universidade Federal de São Carlos São Carlos São Paulo 13565 905 Brazil

Instituto Nacional de Pesquisas da Amazônia Coordenação de Biodiversidade Av André Araújo 2936 Petrópolis Manaus 69067 375 Brazil

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 78049 909 Brazil

Universidade Federal da Paraíba Laboratório de Sistemática e Morfologia de Peixes João Pessoa 58051 090 Brazil

Zobrazit více v PubMed

Albert J.S., Reis R.E. Historical Biogeography of Neotropical Freshwater Fishes. 1st ed. University of California Press; Berkeley, CA, USA: 2011.

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

Reis R.E., Albert J.S., Di Dario F., Mincarone M.M., Petry P., Rocha L.A. Fish biodiversity and conservation in South America. J. Fish Biol. 2016;89:12–47. doi: 10.1111/jfb.13016. PubMed DOI

Pereira L.H.G., Hanner R., Foresti F., Oliveira C. Can DNA barcoding accurately discriminate megadiverse Neotropical freshwater fish fauna? BMC Genet. 2013;14:20. doi: 10.1186/1471-2156-14-20. PubMed DOI PMC

Ferreira M., Kavalco K.F., de Almeida-Toledo L.F., Garcia C. Cryptic diversity between two Imparfinis species (Siluriformes, Heptapteridae) by cytogenetic analysis and DNA barcoding. Zebrafish. 2014;11:306–317. doi: 10.1089/zeb.2014.0981. PubMed DOI

Ferreira M., Garcia C., Matoso D.A., de Jesus I.S., Cioffi M.B., Bertollo L.A.C., Zuanon J., Feldberg E. The Bunocephalus coracoideus species complex (Siluriformes, Aspredinidae). Signs of a speciation process through chromosomal, genetic and ecological diversity. Front. Genet. 2017;8:1–12. doi: 10.3389/fgene.2017.00120. PubMed DOI PMC

Ramirez J.L., Birindelli J.L., Carvalho D.C., Affonso P.R.A.M., Venere P.C., Ortega H., Carrillo-Avila M., Rodríguez-Pulido J.A., Galetti P.M., Jr. Revealing hidden diversity of the underestimated neotropical ichthyofauna: DNA barcoding in the recently described genus Megaleporinus (Characiformes: Anostomidae) Front. Genet. 2017;8:1–11. doi: 10.3389/fgene.2017.00149. PubMed DOI PMC

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

Cioffi M.B., Moreira-Filho O., Ráb P., Sember A., Molina W.F., Bertollo L.A.C. Conventional cytogenetic approaches—Useful and indispensable tools in discovering fish biodiversity. Curr. Genet. Med. Rep. 2018;6:176–186. doi: 10.1007/s40142-018-0148-7. DOI

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. In: Tirunilai P., editor. Recent Trends in Cytogenetic Studies—Methodologies Applications. 1st ed. Volume 1. INTECH; London, UK: 2012. pp. 125–146.

Cioffi M.B., Yano C.F., Sember A., Bertollo L.A.C. Chromosomal evolution in lower vertebrates: Sex chromosomes in Neotropical fishes. Genes. 2017;8:258. doi: 10.3390/genes8100258. PubMed DOI PMC

Bertollo L.A.C. Chromosome evolution in the neotropical Erythrinidae fish family: An overview. In: Pisano E., editor. Fish Cytogenetics. 1st ed. CRC Press; Boca Raton, FL, USA: 2007. pp. 195–211.

Catalog of Fishes: Genera, Species, References. [(accessed on 1 October 2019)]; Available online: http://researcharchive.calacademy.org/research/ichthyology/catalog/fishcatmain.asp.

Netto-Ferreira A.L. Ph.D. Thesis. Universidade de São Paulo; São Paulo, Brazil: 2010. Revisão taxonômica e relações interespecíficas de Lebiasininae (Ostariophysi: Characiformes: Lebiasinidae)

Benzaquem D.C., Oliveira C., da Silva Batista J., Zuanon J., Porto J.I.R. DNA barcoding in pencilfishes (Lebiasinidae: Nannostomus) reveals cryptic diversity across the brazilian Amazon. PLoS ONE. 2015;10:e0112217. doi: 10.1371/journal.pone.0112217. PubMed DOI PMC

Scheel J.J. Fish Chromosomes and Their Evolution. Danmarks Akvarium; Charlottenlund, Denmark: 1973.

Oliveira C., Andreata A., Almeida-Toledo L.F., Toledo Filho S.A. Karyotype and nucleolus organizer regions of Pyrrhulina cf. australis (Pisces, Characiformes, Lebiasinidae) Rev. Bras. Genet. 1991;14:685–690.

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

Moraes R.L.R., Bertollo L.A.C., Marinho M.M.F., Yano C.F., Hatanaka T., Barby F.F., Troy W.P., Cioffi M.B. Evolutionary relationships and cytotaxonomy considerations in the genus Pyrrhulina (Characiformes, Lebiasinidae) Zebrafish. 2017;14:536–546. doi: 10.1089/zeb.2017.1465. PubMed DOI

Moraes R.L., Sember A., Bertollo L.A.C., de Oliveira E.A., Ráb P., Hatanaka T., Marinho M.M.F., Liehr T., Al-Rikabi A.B.H., Feldberg E., et al. Comparative cytogenetics and neo-Y formation in small-sized fish species of the genus Pyrrhulina (Characiformes, Lebiasinidae) Front. Genet. 2019;10:1–13. doi: 10.3389/fgene.2019.00678. PubMed DOI PMC

Sassi F.M.C., de Oliveira E.A., Bertollo L.A.C., Nirchio M., Hatanaka T., Marinho M.M.F., Moreira-Filho O., Aroutiounian R., Liehr T., Al-Rikabi A.B.H., et al. Chromosomal evolution and evolutionary relationships of Lebiasina species (Characiformes, Lebiasinidae) Int. J. Mol. Sci. 2019;20:2944. doi: 10.3390/ijms20122944. PubMed DOI PMC

Toma G.A., Moraes R.L.R., Sassi F.M.C., Bertollo L.A.C., de Oliveira E.A., Ráb P., Sember A., Liehr T., Hatanaka T., Viana P.F., et al. Cytogenetics of the small-sized fish, Copeina guttata (Characiformes, Lebiasinidae): Novel insights into the karyotype differentiation of the family. PLoS ONE. 2019;14:e0226746. doi: 10.1371/journal.pone.0226746. PubMed DOI PMC

Arefjev V.A. Karyotypic diversity of characid families (Pisces, Characidae) Caryologia. 1990;43:291–304. doi: 10.1080/00087114.1990.10797008. DOI

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) 1st ed. Volume 1. CRC Press; Boca Raton, FL, USA: 2015. pp. 21–26.

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

Martins C., Ferreira I.A., Oliveira C., Foresti F., Galetti P.M., Jr. A tandemly repetitive centromeric DNA sequence of the fish Hoplias malabaricus (Characiformes: Erythrinidae) is derived from 5S rDNA. Genetica. 2006;127:133–141. doi: 10.1007/s10709-005-2674-y. PubMed DOI

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

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. 429–444.

Sambrook J., Russell D.W. Molecular Cloning: A Laboratory Manual. 3rd ed. Cold Spring Harbor Laboratory Press; New York, NY, USA: 2001.

Zwick M.S., Hanson R.E., Islam-Faridi M.N., Stelly D.M., Wing R.A., Price H.J., McKnight T.D. A rapid procedure for the isolation of C0t-1 DNA from plants. Genome. 1997;40:138–142. doi: 10.1139/g97-020. PubMed DOI

Sember A., Bertollo L.A.C., Ráb P., Yano C.F., Hatanaka T., de Oliveira E.A., Cioffi M.B. Sex chromosome evolution and genomic divergence in the fish Hoplias malabaricus (Characiformes, Erythrinidae) Front. Genet. 2018;9:1–12. doi: 10.3389/fgene.2018.00071. PubMed DOI PMC

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

King M. Species Evolution: The Role of Chromosome Change. 1st ed. Cambridge University Press; Cambridge, UK: 1993.

Dobigny G., Ducroz J.-F., Robinson T.J., Volobouev V. Cytogenetics and cladistics. Syst. Biol. 2004;53:470–484. doi: 10.1080/10635150490445698. PubMed DOI

Oliveira C., Almeida-Toledo L.F., Foresti F. Karyotypic evolution in Neotropical fishes. In: Pisano E., Ozouf-Costaz C., Foresti F., Kapoor B.G., editors. Fish Cytogenetics. 1st ed. Science Publishers; Enfield, CT, USA: 2007. pp. 111–164.

Souza e Sousa J.F., Viana P.F., Bertollo L.A.C., Cioffi M.B., Feldberg E. Evolutionary relationships among Boulengerella species (Ctenoluciidae, Characiformes): Genomic organization of repetitive DNAs and highly conserved karyotypes. Cytogenet. Genome Res. 2017;152:194–203. doi: 10.1159/000480141. PubMed DOI

Betancur-R R., Arcila D., Vari R.P., Hughes L.C., Oliveira C., Sabaj M.H., Ortí G. Phylogenomic incongruence, hypothesis testing, and taxonomic sampling: The monophyly of characiform fishes. Evolution. 2019;73:329–345. doi: 10.1111/evo.13649. PubMed DOI

De Barros A.V., Wolski M.A.V., Nogaroto V., Almeida M.C., Moreira-Filho O., Vicari M.R. Fragile sites, dysfunctional telomere and chromosome fusions: What is 5S rDNA role? Gene. 2017;608:20–27. doi: 10.1016/j.gene.2017.01.013. PubMed DOI

Cavalcante M.G., Eduardo C., Carvalho M., Nagamachi Y., Pieczarka J.C., Vicari M.R., Noronha R.C.R. Physical mapping of repetitive DNA suggests 2n reduction in Amazon turtles Podocnemis (Testudines: Podocnemididae) PLoS ONE. 2018;13:e0197536. doi: 10.1371/journal.pone.0197536. PubMed DOI PMC

Glugoski L., Giuliano-Caetano L., Moreira-Filho O., Vicari M.R., Nogaroto V. Co-located hAT transposable element and 5S rDNA in an interstitial telomeric sequence suggest the formation of Robertsonian fusion in armored catfish. Gene. 2018;650:49–54. doi: 10.1016/j.gene.2018.01.099. PubMed DOI

Schweizer D., Loidl J. A model for heterochromatin dispersion and the evolution of C-band patterns. In: Stahl A., Luciani J.M., Vagner-Capodano A.M., editors. Chromosomes Today. 1st ed. Volume 9. Springer; Paris, France: 1987. pp. 61–74. DOI

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

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

Santos-Pereira J.M., Aguilera A. R loops: New modulators of genome dynamics and function. Nat. Rev. Genet. 2015;16:583–597. doi: 10.1038/nrg3961. PubMed DOI

Sawyer I.A., Dundr M. Chromatin loops and causality loops: The influence of RNA upon spatial nuclear architecture. Chromosoma. 2017;126:541–557. doi: 10.1007/s00412-017-0632-y. PubMed DOI

Blokhina Y.P., Nguyen A.D., Draper B.W., Burgess S.M. The telomere bouquet is a hub where meiotic double-strand breaks, synapsis, and stable homolog juxtaposition are coordinated in the zebrafish, Danio rerio. PLoS Genet. 2019;15:e1007730. doi: 10.1371/journal.pgen.1007730. PubMed DOI PMC

Potapova T.A., Gerton J.L. Ribosomal DNA and the nucleolus in the context of genome organization. Chromosome Res. 2019;27:109–127. doi: 10.1007/s10577-018-9600-5. PubMed DOI

Giles V., Thode G., Alvarez M.C. A new Robertsonian fusion in the multiple chromosome polymorphism of a mediterranean population of Gobius paganellus (Gobiidae, Perciformes) Heredity. 1985;55:255–260. doi: 10.1038/hdy.1985.99. DOI

Molina W.F., Galetti P.M., Jr. Robertsonian rearrangements in the reef fish Chromis (Perciformes, Pomacentridae) involving chromosomes bearing 5S rRNA genes. Genet. Mol. Biol. 2002;25:373–377. doi: 10.1590/S1415-47572002000400004. DOI

Rosa K.O., Ziemniczak K., de Barros A.V., Nogaroto V., Almeida M.C., Cestari M.M., Artoni R.F., Vicari M.R. Numeric and structural chromosome polymorphism in Rineloricaria lima (Siluriformes: Loricariidae): Fusion points carrying 5S rDNA or telomere sequence vestiges. Rev. Fish Biol. Fish. 2012;22:739–749. doi: 10.1007/s11160-011-9250-6. 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

Getlekha N., Molina W.F., Cioffi M.B., Yano C.F., Maneechot N., Bertollo L.A.C., Supiwong W., Tanomtong A. Repetitive DNAs highlight the role of chromosomal fusions in the karyotype evolution of Dascyllus species (Pomacentridae, Perciformes) Genetica. 2016;144:203–211. doi: 10.1007/s10709-016-9890-5. PubMed DOI

Salvadori S., Deiana A.M., Deidda F., Lobina C., Mulas A., Coluccia E. XX/XY sex chromosome system and chromosome markers in the snake eel Ophisurus serpens (Anguilliformes: Ophichtidae) Mar. Biol. Res. 2018;14:158–164. doi: 10.1080/17451000.2017.1406665. DOI

Schmid M., Steinlein C., Bogart J.P., Feichtinger W., León P., La Marca E., Díaz L.M., Sanz A., Chen S.H., Hedges S.B. The chromosomes of terraran frogs: Insights into vertebrate cytogenetics. Cytogenet. Genome Res. 2016;130–131:1–568. doi: 10.1159/000301339. PubMed DOI

Da Costa M.J.R., do Amaral P.J.S., Pieczarka J.C., Sampaio M.I., Rossi R.V., Mendes-Oliveira A.C., Noronha R.C.R., Nagamachi C.Y. Cryptic species in Proechimys goeldii (Rodentia, Echimyidae)? A case of molecular and chromosomal differentiation in allopatric populations. Cytogenet. Genome Res. 2016;148:199–210. doi: 10.1159/000446562. PubMed DOI

Houck M.L., Teri L., Lear T.L., Charter S.J. Animal cytogenetics. In: Arsham M.S., Barch M.J., Lawce H.J., editors. The AGT Cytogenetics Laboratory Manual. 4th ed. John Wiley & Sons; Hoboken, NJ, USA: 2017. pp. 1055–1102.

Sousa R.P.C., Oliveira-Filho A.B., Vallinoto M., Cioffi M.B., Molina W.F., de Oliveira E.H., Silva-Oliveira G.C. Cytogenetics description in Batrachoides surinamensis, (Batrachoididae: Batrachoidiformes): What does the estuary have to say? Estuar. Coast. Shelf Sci. 2018;213:253–259. doi: 10.1016/j.ecss.2018.08.008. DOI

Molina W.F., Martinez P.A., Bertollo L.A.C., Bidau C.J. Evidence for meiotic drive as an explanation for karyotype changes in fishes. Mar. Genom. 2014;15:29–34. doi: 10.1016/j.margen.2014.05.001. PubMed DOI

Krysanov E., Demidova T. Extensive karyotype variability of African fish genus Nothobranchius (Cyprinodontiformes) Comp. Cytogenet. 2018;12:387–402. doi: 10.3897/CompCytogen.v12i3.25092. PubMed DOI PMC

Völker M., Sonnenberg R., Ráb P., Kullmann H. Karyotype differentiation in Chromaphyosemion killifishes (Cyprinodontiformes, Nothobranchiidae) II: Cytogenetic and mitochondrial DNA analyses demonstrate karyotype differentiation and its evolutionary direction in C. riggenbachi. Cytogenet. Genome Res. 2006;115:70–83. doi: 10.1159/000094803. PubMed DOI

Völker M., Ráb P., Kullmann H. Karyotype differentiation in Chromaphyosemion killifishes (Cyprinodontiformes, Nothobranchiidae): Patterns, mechanisms, and evolutionary implications. Biol. J. Linn. Soc. 2008;94:143–153. doi: 10.1111/j.1095-8312.2008.00967.x. DOI

Ene A.-C. Chromosomal polymorphism in the goby Neogobius eurycephalus (Perciformes: Gobiidae) Mar. Biol. 2002;142:583–588. doi: 10.1007/s00227-002-0978-3. DOI

Amores A., Wilson C.A., Allard C.A.H., Detrich H.W., Postlethwait J.H. Cold fusion: Massive karyotype evolution in the Antarctic bullhead notothen Notothenia coriiceps. G3 (Bethesda) 2017;7:2195–2207. doi: 10.1534/g3.117.040063. PubMed DOI PMC

Crossman E.J., Ráb P. Chromosome-banding study of the Alaska blackfish, Dallia pectoralis (Euteleostei: Esocae) with implications for karyotype evolution and relationships of esocoid fishes. Can. J. Zool. 1996;74:147–156. doi: 10.1139/z96-019. DOI

Crossman E.J., Ráb P. Chromosomal NOR phenotype and C-banded karyotype of Olympic mudminnow, Novumbra hubbsi (Euteleostei: Umbridae) Copeia. 2001;3:860–865. doi: 10.1643/0045-8511(2001)001[0860:CNPACB]2.0.CO;2. 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

Brown J.D., O’Neill R.J. Chromosomes, conflict, and epigenetics: Chromosomal speciation revisited. Annu. Rev. Genom. Hum. Genet. 2010;11:291–316. doi: 10.1146/annurev-genom-082509-141554. PubMed DOI

Guerrero R.F., Kirkpatrick M. Local adaptation and the evolution of chromosome fusions. Evolution. 2014;68:2747–2756. doi: 10.1111/evo.12481. PubMed DOI

Lanctôt C., Cheutin T., Cremer M., Cavalli G., Cremer T. Dynamic genome architecture in the nuclear space: Regulation of gene expression in three dimensions. Nat. Rev. Genet. 2007;8:104–115. doi: 10.1038/nrg2041. PubMed DOI

Meaburn K.J., Misteli T., Soutoglou E. Spatial genome organization in the formation of chromosomal translocations. Semin. Cancer Biol. 2007;17:80–90. doi: 10.1016/j.semcancer.2006.10.008. PubMed DOI PMC

Meaburn K.J., Misteli T. Cell biology: Chromosome territories. Nature. 2007;445:379–781. doi: 10.1038/445379a. PubMed DOI

Cremer T., Cremer M. Chromosome territories. Cold Spring Harb. Perspect. Biol. 2010;2:1–23. doi: 10.1101/cshperspect.a003889. PubMed DOI PMC

Roukos V., Misteli T. The biogenesis of chromosome translocations. Nat. Cell Biol. 2014;16:293–300. doi: 10.1038/ncb2941. PubMed DOI PMC

Fraser J., Williamson I., Bickmore W.A., Dostie J. An overview of genome organization and how we got there: From FISH to Hi-C. Microbiol. Mol. Biol. Rev. 2015;79:347–372. doi: 10.1128/MMBR.00006-15. 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

Ghavi-Helm Y., Jankowski A., Meiers S., Viales R.R., Korbel J.O., Furlong E.E.M. Highly rearranged chromosomes reveal uncoupling between genome topology and gene expression. Nat. Genet. 2019;51:1272–1282. doi: 10.1038/s41588-019-0462-3. PubMed DOI PMC

Mank J.E., Avise J.C. Phylogenetic conservation of chromosome numbers in Actinopterygiian fishes. Genetica. 2006;127:321–327. doi: 10.1007/s10709-005-5248-0. PubMed 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

García-Souto D., Qarkaxhija V., Pasantes J.J. Resolving the taxonomic status of Chamelea gallina and C. striatula (Veneridae, Bivalvia): A combined molecular cytogenetic and phylogenetic approach. Biomed. Res. Int. 2017;2017:7638790. doi: 10.1155/2017/7638790. PubMed DOI PMC

Weeks A.R., Marec F., Breeuwer J.A.J. A mite species that consists entirely of haploid females. Science. 2001;292:2479–2482. doi: 10.1126/science.1060411. PubMed DOI

Lukhtanov V.A., Dincă V., Friberg M., Šíchová J., Olofsson M., Vila R., Marec F., Wiklund C. Versatility of multivalent orientation, inverted meiosis, and rescued fitness in holocentric chromosomal hybrids. PNAS. 2018;115:E9610–E9619. doi: 10.1073/pnas.1802610115. PubMed DOI PMC

Do Nascimento V.D., Coelho K.A., Nogaroto V., Almeida R.B., Ziemniczak K., Centofante L., Pavanelli C.S., Torres R.A., Moreira-Filho O., Vicari M.R. Do multiple karyomorphs and population genetics of freshwater darter characines (Apareiodon affinis) indicate chromosomal speciation? Zool. Anz. 2018;272:93–103. doi: 10.1016/j.jcz.2017.12.006. DOI

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

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

Soto M.Á., Castro J.P., Walker L.I., Malabarba L.R., Santos M.H., Almeida M.C., Moreira-Filho O., Artoni R.F. Evolution of trans-Andean endemic fishes of the genus Cheirodon (Teleostei: Characidae) are associated with chromosomal rearrangements. Rev. Chil. Hist. Nat. 2018;91:8. doi: 10.1186/s40693-018-0078-5. DOI

Yano C.F., Bertollo L.A.C., Ezaz T., Trifonov V., Sember A., Liehr T., Cioffi M.B. Highly conserved Z and molecularly diverged W chromosomes in the fish genus Triportheus (Characiformes, Triportheidae) Heredity. 2017;118:276–283. doi: 10.1038/hdy.2016.83. PubMed DOI PMC

De Oliveira E.A., Sember A., Bertollo L.A.C., Yano C.F., Ezaz T., Moreira-Filho O., Hatanaka T., Trifonov V., Liehr T., Al-Rikabi A.B.H., 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

Xu D., Sember A., Zhu Q., de Oliveira E.A., Liehr T., Al-Rikabi A.B.H., Xiao Z., Song H., Cioffi M.B. Deciphering the origin and evolution of the X1X2Y system in two closely-related Oplegnathus species (Oplegnathidae and Centrarchiformes) J. Mol. Sci. 2019;20:3571. doi: 10.3390/ijms20143571. PubMed DOI PMC

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

Da Silva A.F., Feldberg E., Carvalho N.D.M., Rangel S.M.H., Schneider C.H., Carvalho-Zilse G.A., da Silva V.F., 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

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

Milhomem S.S.R., Scacchetti P.C., Pieczarka J.C., Ferguson-Smith M.A., Pansonato-Alves J.C., O’Brien P.C.M., Foresti F., Nagamachi C.Y. Are NORs always located on homeologous chromosomes? A FISH investigation with rDNA and whole chromosome probes in Gymnotus fishes (Gymnotiformes) PLoS ONE. 2013;8:e55608. doi: 10.1371/journal.pone.0055608. PubMed DOI PMC

Lim K.Y., Kovařík A., Matyášek R., Chase M.W., Clarkson J.J., Grandbastien M.A., Leitch A.R. Sequence of events leading to near-complete genome turnover in allopolyploid Nicotiana within five million years. New Phytol. 2007;175:756–763. doi: 10.1111/j.1469-8137.2007.02121.x. PubMed DOI

Majka J., Majka M., Kwiatek M., Wiśniewska H. Similarities and differences in the nuclear genome organization within Pooideae species revealed by comparative genomic in situ hybridization (GISH) J. Appl. Genet. 2017;58:151–161. doi: 10.1007/s13353-016-0369-y. PubMed DOI PMC

Barby F.F., Bertollo L.A.C., de 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

Kandul N.P., Lukhtanov V.A., Pierce N.E. Karyotypic diversity and speciation in Agrodiaetus butterflies. Evolution. 2007;61:546–559. doi: 10.1111/j.1558-5646.2007.00046.x. PubMed DOI

Luo J., Sun X., Cormack B.P., Boeke J.D. Karyotype engineering by chromosome fusion leads to reproductive isolation in yeast. Nature. 2018;560:392–396. doi: 10.1038/s41586-018-0374-x. PubMed DOI PMC

Ortiz-Barrientos D., Engelstädter J., Rieseberg L.H. Recombination rate evolution and the origin of species. Trends Ecol. Evol. 2016;31:226–236. doi: 10.1016/j.tree.2015.12.016. PubMed DOI

Homeology of sex chromosomes in Amazonian Harttia armored catfishes supports the X-fission hypothesis for the X1X2Y sex chromosome system origin

Small Body, Large Chromosomes: Centric Fusions Shaped the Karyotype of the Amazonian Miniature Fish Nannostomus anduzei (Characiformes, Lebiasinidae)

An Insight into the Chromosomal Evolution of Lebiasinidae (Teleostei, Characiformes)