The Erythrinidae family (Teleostei: Characiformes) is a small Neotropical fish group with a wide distribution throughout South America, where Hoplias malabaricus corresponds to the most widespread and cytogenetically studied taxon. This species possesses significant genetic variation, as well as huge karyotype diversity among populations, as reflected by its seven major karyotype forms (i.e., karyomorphs A-G) identified up to now. Although morphological differences in their bodies are not outstanding, H. malabaricus karyomorphs are easily identified by differences in 2n, morphology and size of chromosomes, as well as by distinct evolutionary steps of sex chromosomes development. Here, we performed comparative genomic hybridization (CGH) to analyse both the intra- and inter-genomic status in terms of repetitive DNA divergence among all but one (E) H. malabaricus karyomorphs. Our results indicated that they have close relationships, but with evolutionary divergences among their genomes, yielding a range of non-overlapping karyomorph-specific signals. Besides, male-specific regions were uncovered on the sex chromosomes, confirming their differential evolutionary trajectories. In conclusion, the hypothesis that H. malabaricus karyomorphs are result of speciation events was strengthened.

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

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

Secretaria de Estado de Educação de Mato Grosso Cuiabá Brazil

Zobrazit více v PubMed

de Almeida-Toledo L. F., Foresti F. (2001). Morphologically differentiated sex chromosomes in neotropical freshwater fish. Genetica 111, 91–100. 10.1023/A:1013768104422 PubMed DOI

Altmanová M., Rovatsos M., Kratochvíl L., Johnson Pokorná M. (2016). Minute Y chromosomes and karyotype evolution in Madagascan iguanas (Squamata: Iguania: Opluridae). Biol. J. Linn. Soc. 118, 618–633. 10.1111/bij.12751 DOI

Arai R. (2011). Fish Karyotypes: A Check List, 1st Edn. Tokyo: Springer.

Bachtrog D., Mank J. E., Peichel C. L., Kirkpatrick M., Otto S. P., Ashman T. L., et al. . (2014). Sex determination: why so many ways of doing it? PLoS Biol. 12:e1001899. 10.1371/journal.pbio.1001899 PubMed DOI PMC

Badenhorst D., Stanyon R., Engstrom T., Valenzuela N. (2013). A ZZ/ZW microchromosome system in the spiny softshell turtle, Apalone spinifera, reveals an intriguing sex chromosome conservation in Trionychidae. Chromosome Res. 21, 137–147. 10.1007/s10577-013-9343-2 PubMed DOI

Bertollo L. A. C. (2007). Chromosome evolution in the Neotropical Erythrinidae fish family: an overview, in Fish Cytogenetics, eds Pisano E., Ozouf-Costaz C., Foresti F., Kapoor B. G. (Enfield, NH: Science Publishers; ), 195–211.

Bertollo L. A. C., Mestriner C. A. (1998). The X1X2Y sex chromosome system in the fish Hoplias malabaricus II Meiotic analyses. Chromosome Res. 6, 141–147. 10.1023/A:1009243114124 PubMed DOI

Bertollo L. A., Born G. G., Dergam J. A., Fenocchio A. S., Moreira-Filho O. (2000). A biodiversity approach in the neotropical Erythrinidae fish, Hoplias malabaricus. Karyotypic survey, geographic distribution of cytotypes and cytotaxonomic considerations. Chromosome Res. 8, 603–613. 10.1023/A:1009233907558 PubMed DOI

Bertollo L. A. C., Fontes M. S., Fenocchio A. S., Cano J. (1997). The X1X2Y sex chromosome system in the fish Hoplias malabaricus. I. G-, C- and chromosome replication banding. Chromosome Res. 5, 493–499. 10.1023/A:1018477232354 PubMed DOI

Bertollo L. A. C., Moreira-Filho O., Cioffi M. B. (2015). Direct chromosome preparations from freshwater teleost fishes, in Fish Techniques, Ray-Fin Fishes and Chondrichthyans, eds Ozouf-Costaz C., Pisano E., Foresti F., de Almeida Toledo L. F. (Boca Ranton, FL: CRC Press; ), 21–26.

Bi K., Bogart J. P. (2006). Identification of intergenomic recombinations in unisexual salamanders of the genus Ambystoma by genomic in situ hybridization (GISH). Cytogenet. Genome Res. 112, 307–312. 10.1159/000089885 PubMed DOI

Blanco D. R., Lui R. L., Vicari M. R., Bertollo L. A., Moreira-Filho O. (2011). Comparative cytogenetics of giant trahiras Hoplias aimara and H. intermedius (Characiformes, Erythrinidae): chromosomal characteristics of minor and major ribosomal DNA and cross-species repetitive centromeric sequences mapping differ among morphologically identical karyotypes. Cytogenet. Genome Res. 132, 71–78. 10.1159/000320923 PubMed DOI

Born G. G., Bertollo L. A. (2000). An XX/XY sex chromosome system in a fish species, Hoplias malabaricus, with a polymorphic NOR-bearing X chromosome. Chromosome Res. 8, 111–118. 10.1023/A:1009238402051 PubMed DOI

Brykov V. A. (2014). Mechanisms of sex determination in fish: evolutionary and practical aspects. Russ. J. Mar. Biol. 40, 407–417. 10.1134/S1063074014060145 DOI

Carvalho P. C., de Oliveira E. A., Bertollo L. A. C., Yano C. F., Oliveira C., Decru E., et al. . (2017). First chromosomal analysis in Hepsetidae (Actinopterygii, Characiformes): insights into relationship between African and Neotropical fish groups. Front. Genet. 8:203. 10.3389/fgene.2017.00203 PubMed DOI PMC

Charlesworth B., Sniegowski P., Stephan W. (1994). The evolutionary dynamics of repetitive DNA in eukaryotes. Nature 371, 215–220. 10.1038/371215a0 PubMed DOI

Chester M., Leitch A. R., Soltis P. S., Soltis D. E. (2010). Review of the application of modern cytogenetic methods (FISH/GISH) to the study of reticulation (polyploidy/hybridisation). Genes 1, 166–192. 10.3390/genes1020166 PubMed DOI PMC

Cioffi M. B., Bertollo L. A. (2010). Initial steps in XY chromosome differentiation in Hoplias malabaricus and the origin of an X1X2Y sex chromosome system in this fish group. Heredity 105, 554–561. 10.1038/hdy.2010.18 PubMed DOI

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

Cioffi M. B., Liehr T., Trifonov V., Molina W. F., Bertollo L. A. C. (2013). Independent sex chromosome evolution in lower vertebrates: a molecular cytogenetic overview in the erythrinidae fish family. Cytogenet. Genome Res. 141, 186–194. 10.1159/000354039 PubMed DOI

Cioffi M. B., Martins C., Bertollo L. A. C. (2009). Comparative chromosome mapping of repetitive sequences. Implications for genomic evolution in the fish, Hoplias malabaricus. BMC Genet. 10:34. 10.1186/1471-2156-10-34 PubMed DOI PMC

Cioffi M. B., Martins C., Vicari M. R., Rebordinos L., Bertollo L. A. (2010). Differentiation of the XY sex chromosomes in the fish Hoplias malabaricus (Characiformes, Erythrinidae). Unusual accumulation of repetitive sequences on the X chromosome. Sex. Dev. 4, 176–185. 10.1159/000309726 PubMed DOI

Cioffi M. B., Molina W. F., Artoni R. F., Bertollo L. A. (2012). Chromosomes as tools for discovering biodiversity – the case of Erythrinidae fish family, in Recent Trends in Cytogenetic Studies – Methodologies and Applications, ed Tirunilai P. (Rijeka: InTech Publisher; ), 125–146.

Cioffi M. B., Molina W. F., Moreira-Filho O., Bertollo L. A. (2011a). Chromosomal distribution of repetitive DNA sequences highlights the independent differentiation of multiple sex chromosomes in two closely related fish species. Cytogenet. Genome Res. 134, 295–302. 10.1159/000329481 PubMed DOI

Cioffi M. B., Sánchez A., Marchal J. A., Kosyakova N., Liehr T., Trifonov V., et al. . (2011b). Cross-species chromosome painting tracks the independent origin of multiple sex chromosomes in two cofamiliar Erythrinidae fishes. BMC Evol. Biol. 11:186. 10.1186/1471-2148-11-186 PubMed DOI PMC

Cioffi M. B., Sánchez A., Marchal J. A., Kosyakova N., Liehr T., Trifonov V., et al. (2011c). Whole chromosome painting reveals independent origin of sex chromosomes in closely related forms of a fish species. Genetica 139, 1065–1072. 10.1007/s10709-011-9610-0 PubMed DOI

Cnaani A. (2013). The tilapias' chromosomes influencing sex determination. Cytogenet. Genome Res. 141, 195–205. 10.1159/000355304 PubMed DOI

Dergam J. A., Paiva S. R., Schaefer C. E., Godinho A. L., Vieira F. (2002). Phylogeography and RAPD-PCR variation in Hoplias malabaricus (Bloch, 1974) (Pisces, Teleostei) in southeastern Brazil. Genet. Mol. Biol. 25, 379–387. 10.1590/S1415-47572002000400005 DOI

Dergam J. A., Suzuki H. I., Shibatta O. A., Duboc L. F., Júlio H. F., Jr., Giuliano-Caetano L., et al. (1998). Molecular biogeography of the neotropical fish Hoplias malabaricus (Erythrinidae, Characiformes) in the Iguaçu, Tibagi, and Paraná rivers. Genet. Mol. Biol. 21, 493–496. 10.1590/S1415-47571998000400015 DOI

Devlin R. H., Nagahama Y. (2002). Sex determination and sex differentiation in fish: an overview of genetic, physiological, and environmental influences. Aquaculture 208, 191–364. 10.1016/S0044-8486(02)00057-1 DOI

Doležálková M., Sember A., Marec F., Ráb P., Plötner J., Choleva L. (2016). Is premeiotic genome elimination an exclusive mechanism for hemiclonal reproduction in hybrid males of the genus Pelophylax? BMC Genet. 17:100. 10.1186/s12863-016-0408-z PubMed DOI PMC

Ezaz T., Deakin J. E. (2014). Repetitive sequence and sex chromosome evolution in vertebrates. Adv. Evol. Biol. 2014, 1–9. 10.1155/2014/104683 DOI

Ezaz T., Valenzuela N., Grützner F., Miura I., Georges A., Burke R. L., et al. . (2006). An XX/XY sex microchromosome system in a freshwater turtle, Chelodina longicollis (Testudines: Chelidae) with genetic sex determination. Chromosome Res. 14, 139–150. 10.1007/s10577-006-1029-6 PubMed DOI

Faria R., Navarro A. (2010). Chromosomal speciation revisited: rearranging theory with pieces of evidence. Trends Ecol. Evol. 25, 660–669. 10.1016/j.tree.2010.07.008 PubMed DOI

Freitas N. L., Al-Rikabi A. B. H., Bertollo L. A. C., Ezaz T., Yano C. F., Oliveira E. A., et al. (2017). Early stages of XY sex chromosomes differentiation in the fish Hoplias malabaricus (Characiformes, Erythrinidae) revealed by DNA repeats accumulation. Curr. Genomics 19, 216–226. 10.2174/1389202918666170711160528 PubMed DOI PMC

Gazoni T., Haddad C. F. B., Narimatsu H., Cabral-de-Mello D. C., Lyra M. L., Parise-Maltempi P. P. (2018). More sex chromosomes than autosomes in the Amazonian frog Leptodactylus pentadactylus. Chromosoma. [Epub ahead of print]. 10.1007/s00412-018-0663-z PubMed DOI

Green J. E., Dalíková M., Sahara K., Marec F., Akam M. (2016). XX/XY system of sex determination in the geophilomorph centipede Strigamia maritima. PLoS ONE 11:e0150292. 10.1371/journal.pone.0150292 PubMed DOI PMC

Griffin D. K., Harvey S. C., Campos-Ramos R., Ayling L.-J., Bromage N. R., Masabanda J. S., et al. (2002). Early origins of the X and Y chromosome: lessons from tilapia. Cytogenet. Genome Res. 99, 157–163. 10.1159/000071588 PubMed DOI

Henning F., Trifonov V., Ferguson-Smith M. A., de Almeida-Toledo L. F. (2008). Non-homologous sex chromosomes in two species of the genus Eigenmannia (Teleostei: Gymnotiformes). Cytogenet Genome Res. 121, 55–58. 10.1159/000124382 PubMed DOI

Heule C., Salzburger W., Böhne A. (2014). Genetics of sexual development: an evolutionary playground for fish. Genetics 196, 579–591. 10.1534/genetics.114.161158 PubMed DOI PMC

Hurley I. A., Mueller R. L., Dunn K. A., Schmidt E. J., Friedman M., Ho R. K., et al. . (2007). A new time-scale for ray-finned fish evolution. Proc. R. Soc. B Biol. Sci. 274, 489–498. 10.1098/rspb.2006.3749 PubMed DOI PMC

Kallioniemi A., Kallioniemi O. P., Sudar D., Rutovitz D., Gray J. W., Waldman F., et al. . (1992). Comparative genomic hybridization for molecular cytogenetic analysis of solid tumors. Science 258, 818–821. 10.1126/science.1359641 PubMed DOI

Kamiya T., Kai W., Tasumi S., Oka A., Matsunaga T., Mizuno N., et al. . (2012). A trans-species missense SNP in Amhr2 is associated with sex determination in the tiger pufferfish, Takifugu rubripes (Fugu). PLoS Genet. 8:e1002798. 10.1371/journal.pgen.1002798 PubMed DOI PMC

Kato A., Vega J. M., Han F., Lamb J. C., Bircher J. A. (2005). Advances in plant chromosome identification and cytogenetic techniques. Curr. Opin. Plant. Biol. 8, 148–154. 10.1016/j.pbi.2005.01.014 PubMed DOI

Kawai A., Nishida-Umehara C., Ishijima J., Tsuda Y., Ota H., Matsuda Y. (2007). Different origins of bird and reptile sex chromosomes inferred from comparative mapping of chicken Z-linked genes. Cytogenet. Genome Res. 117, 92–102. 10.1159/000103169 PubMed DOI

Kikuchi K., Hamaguchi S. (2013). Novel sex-determining genes in fish and sex chromosome evolution. Dev. Dyn. 242, 339–353. 10.1002/dvdy.23927 PubMed DOI

King M. (1993). Species Evolution: The Role of Chromosome Change. Cambridge, GB: University Press.

Kitano J., Peichel C. L. (2012). Turnover of sex chromosomes and speciation in fishes. Environ. Biol. Fishes. 94, 549–558. 10.1007/s10641-011-9853-8 PubMed DOI PMC

Kitano J., Ross J. A., Mori S., Kume M., Jones F. C., Chan Y. F., et al. . (2009). A role for a neo-sex chromosome in stickleback speciation. Nature 461, 1079–1083. 10.1038/nature08441 PubMed DOI PMC

Knytl M., Kalous L., Symonová R., Rylková K., Ráb P. (2013). Chromosome studies of European cyprinid fishes: cross-species painting reveals natural allotetraploid origin of a Carassius female with 206 chromosomes. Cytogenet. Genome Res. 139, 276–283. 10.1159/000350689 PubMed DOI

Koubová M., Pokorná M. J., Rovatsos M., Farkacová K., Altmanová M., Kratochvíl L. (2014). Sex determination in Madagascar geckos of the genus Paroedura (Squamata: Gekkonidae): are differentiated sex chromosomes indeed so evolutionary stable? Chromosome Res. 22, 441–452. 10.1007/s10577-014-9430-z PubMed DOI

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

Liu H., Pang M., Yu X., Zhou Y., Tong J., Fu B. (2018). 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. [Epub ahead of print]. 10.1093/dnares/dsx054 PubMed DOI PMC

López-Flores I., Garrido-Ramos M. A. (2012). The repetitive DNA content of eukaryotic genomes. Genome Dyn. 7, 1–28. 10.1159/000337118 PubMed DOI

Majka J., Majka M., Kwiatek M., Wiśniewska H. (2016). Similarities and differences in the nuclear genome organization within Pooideae species revealed by comparative genomic in situ hybridization (GISH). J. Appl. Genet. 58, 151–161. 10.1007/s13353-016-0369-y PubMed DOI PMC

Majtánová Z., Choleva L., Symonová R., Ráb P., Kotusz J., Pekárik L., et al. (2016). Asexual reproduction does not apparently increase the rate of chromosomal evolution: karyotype stability in diploid and triploid clonal hybrid fish ( Cobitis, Cypriniformes, Teleostei). PLoS ONE 11:e0146872. 10.1371/journal.pone.0146872 PubMed DOI PMC

Mank J. E., Avise J. C. (2009). Evolutionary diversity and turn-over of sex determination in teleost fishes. Sex Dev. 3, 60–67. 10.1159/000223071 PubMed DOI

Mank J. E., Promislow D. E. L., Avise J. C. (2006). Evolution of alternative sex-determining mechanisms in teleost fishes. Biol. J. Linn. Soc. 87, 83–93. 10.1111/j.1095-8312.2006.00558.x DOI

Marques D. F., Santos F. A., da Silva S. S., Sampaio I., Rodrigues L. R. R. (2013). Cytogenetic and DNA barcoding reveals high divergence within the trahira, Hoplias malabaricus (Characiformes: Erythrinidae) from the lower Amazon River. Neotrop. Ichthyol. 11, 459–466. 10.1590/S1679-62252013000200015 DOI

Martinez J. F., Lui R. L., Traldi J. B., Blanco D. R., Moreira-Filho O. (2016). Comparative cytogenetics of Hoplerythrinus unitaeniatus (Agassiz, 1829) (Characiformes, Erythrinidae) species complex from different brazilian hydrographic basins. Cytogenet. Genome Res. 149, 191–200. 10.1159/000448153 PubMed DOI

Martinez J. F., Lui R. L., Traldi J. B., Blanco D. R., Moreira-Filho O. (2015). Occurrence of natural hybrids among sympatric karyomorphs in Hoplerythrinus unitaeniatus (Characiformes, Erythrinidae). Zebrafish 12, 281–287. 10.1089/zeb.2015.1083 PubMed DOI

Martínez P., Viñas A. M., Sánchez L., Díaz N., Ribas L., Piferrer F. (2014). Genetic architecture of sex determination in fish: applications to sex ratio control in aquaculture. Front. Genet. 5:340. 10.3389/fgene.2014.00340 PubMed DOI PMC

Matsuda M., Nagahama Y., Shinomiya A., Sato T., Matsuda C., Kobayashi T., et al. . (2002). DMY is a Y specific DM-domain gene required for male development in the medaka fish. Nature 417, 559–563. 10.1038/nature751 PubMed DOI

Montiel E. E., Badenhorst D., Tamplin J., Burke R. L., Velanzuela N. (2017). Discovery of the youngest sex chromosomes reveals first case of convergent co-option of ancestral autosomes in turtles. Chromosoma 126, 105–113. 10.1007/s00412-016-0576-7 PubMed DOI

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

Nanda I., Kondo M., Hornung U., Asakawa S., Winkler C., Shimizu A., et al. . (2002). A duplicated copy of DMRT1 in the sex-determining region of the Y chromosome of the medaka, Oryzias latipes. Proc. Natl. Acad. Sci. U.S.A. 99, 11778–11783. 10.1073/pnas.182314699 PubMed DOI PMC

Nguyen P., Sýkorová M., Šíchová J., Kuta V., Dalíková M., Capková Frydrychová R., et al. . (2013). Neo-sex chromosomes and adaptive potential in tortricid pests. Proc. Natl. Acad. Sci. U.S.A. 110, 6931–6936. 10.1073/pnas.1220372110 PubMed DOI PMC

de Oliveira E. A., Bertollo L. A. C., Yano C. F., Liehr T., Cioffi M. B. (2015). Comparative cytogenetics in the genus Hoplias (Characiformes, Erythrinidae) highlights contrasting karyotype evolution among congeneric species. Mol. Cytogenet. 8:56. 10.1186/s13039-015-0161-4 PubMed DOI PMC

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

Oyakawa O. T. (2003). Family Erythrinidae, in Check List of the freshwater fishes of South and Central America, eds Reis R. E., Kullander S. O., Ferraris C. J., Jr (Porto Alegre: Edipucrs; ), 238–240.

Oyakawa O. T., Mattox G. M. T. (2009). Revision of the Neotropical trahiras of the Hoplias lacerdae species-group (Ostariophysi: Characiformes: Erythrinidae) with descriptions of two new species. Neotrop. Ichthyol. 7, 117–140. 10.1590/S1679-62252009000200001 DOI

Pennell M. W., Kirkpatrick M., Otto S. P., Vamosi J. C., Peichel C. L., Valenzuela N., et al. . (2015). Y fuse? Sex chromosome fusions in fishes and reptiles. PLoS Genet. 11:e1005237. 10.1371/journal.pgen.1005237 PubMed DOI PMC

Pokorná M., Altmanová M., Kratochvíl L. (2014). Multiple sex chromosomes in the light of female meiotic drive in amniote vertebrates. Chromosome Res. 22, 35–44. 10.1007/s10577-014-9403-2 PubMed DOI

Portela-Bens S., Merlo M. A., Rodríguez M. E., Cross I., Manchado M., Kosyakova N., et al. (2017). Integrated gene mapping and synteny studies give insights into the evolution of a sex protochromosome in Solea senegalensis. Chromosoma 126, 261–277. 10.1007/s00412-016-0589-2 PubMed DOI

Rantin F. T., Glass M. L., Kalinin A. L., Verzola R. M. M., Fernandes M. N. (1993). Cardio-respiratory responses in two ecologically distinct erythrinids (Hoplias malabaricus and Hoplias lacerdae) exposed to graded environmental hypoxia. Environ. Biol. Fish. 36, 93–97. 10.1007/BF00005983 DOI

Rantin F. T., Kalinin A. L., Glass M. L., Fernandes M. N. (1992). Respiratory responses to hypoxia in relation to mode of life of two erythrinid species (Hoplias malabaricus and Hoplias lacerdae). J. Fish. Biol. 41, 805–812. 10.1111/j.1095-8649.1992.tb02708.x DOI

Ravi V., Venkatesh B. (2008). Rapidly evolving fish genomes and teleost diversity. Curr. Opin. Genet. Dev. 18:544–550. 10.1016/j.gde.2008.11.001 PubMed DOI

Reichwald K., Petzold A., Koch P., Downie B. R., Hartmann N., Pietsch S., et al. . (2015). Insights into sex chromosome evolution and aging from the genome of a short-lived fish. Cell 163, 1527–1538. 10.1016/j.cell.2015.10.071 PubMed DOI

Rios F. S., Kalinin A. L., Rantin F. T. (2002). The effects of long-term food deprivation on respiration and hematology of the neotropical fish Hoplias malabaricus. J. Fish. Biol. 61, 85–95. 10.1111/j.1095-8649.2002.tb01738.x DOI

Rosa R., Laforga Vanzela A. L., Rubert M., Martins-Santos I. C., Giuliano-Caetano L. (2009). Differentiation of Y chromosome in the X1X1X2X2/X1X2Y sex chromosome system of Hoplias malabaricus (Characiformes, Erythrinidae). Cytogenet. Genome Res. 127, 54–60. 10.1159/000269736 PubMed DOI

Rosa R., Rubert M., Martins-Santos I., Giuliano-Caetano L. (2012). Evolutionary trends in Hoplerythrinus unitaeniatus (Agassiz 1829) (Characiformes, Erythrinidae). Rev. Fish Biol. Fish. 22, 467–475. 10.1007/s11160-011-9237-3 DOI

Ross J. A., Urton J. R., Boland J., Shapiro M. D., Peichel C. L. (2009). Turnover of sex chromosomes in the stickleback fishes (Gasterosteidae). PLoS Genet. 5:e1000391. 10.1371/journal.pgen.1000391 PubMed DOI PMC

Rovatsos M., Johnson Pokorná M., Altmanová M., Kratochvíl L. (2016). Mixed-up sex chromosomes: identification of sex chromosomes in the X1X1X2X2/X1X2Y system of the legless lizards of the genus Lialis (Squamata: Gekkota: Pygopodidae). Cytogenet. Genome Res. 149, 282–289. 10.1159/000450734 PubMed DOI

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

Sambrook J., Russell D. W. (2001). Molecular Cloning: A Laboratory Manual, 3rd Edn. New York, NY: Cold Spring Harbor Laboratory Press.

Santos U., Völcker C. M., Belei F. A., Cioffi M. B., Bertollo L. A., Paiva S. R., et al. . (2009). Molecular and karyotypic phylogeography in the Neotropical Hoplias malabaricus (Erythrinidae) fish in eastern. Brazil. J. Fish Biol. 75, 2326–2343. 10.1111/j.1095-8649.2009.02489.x PubMed DOI

Schartl M. (2004). Sex chromosome evolution in non-mammalian vertebrates. Curr. Opin. Genet. Dev. 14, 634–641. 10.1016/j.gde.2004.09.005 PubMed DOI

Schartl M., Schmid M., Nanda I. (2016). Dynamics of vertebrate sex chromosome evolution: from equal size to giants and dwarfs. Chromosoma 125, 553–571. 10.1007/s00412-015-0569-y PubMed DOI

Schoumans J., Nielsen K., Jeppesen I., Anderlid B. M., Blennow E., Brøndum-Nielsen K., et al. . (2004). A comparison of different metaphase CGH methods for the detection of cryptic chromosome aberrations of defined size. Eur. J. Hum. Genet. 12, 447–454. 10.1038/sj.ejhg.5201175 PubMed DOI

Sutherland B. J. G., Rico C., Audet C., Bernatchez L. (2017). Sex chromosome evolution, heterochiasmy, and physiological QTL in the salmonid brook charr Salvelinus fontinalis. G3 7, 2749–2762. 10.1534/g3.117.040915 PubMed DOI PMC

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

Symonová R., Majtánová Z., Sember A., Staaks G. B., Bohlen J., Freyhof J., et al. . (2013b). 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. 13:42. 10.1186/1471-2148-13-42 PubMed DOI PMC

Symonová R., Sember A., Majtánová Z., Ráb P. (2015). Characterization of fish genomes by GISH and CGH, in Fish techniques, Ray-Fin Fishes and Chondrichthyans, eds Ozouf-Costaz C., Pisano E., Foresti F., de Almeida Toledo L. F. (Boca Ranton, FL: CRC Press; ), 118–131.

Takehana Y., Naruse K., Hamaguchi S., Sakaizumi M. (2007). Evolution of ZZ/ZW and XX/XY sex-determination systems in the closely related medaka species, Oryzias hubbsi and O. dancena. Chromosoma 116, 463–470. 10.1007/s00412-007-0110-z PubMed DOI

Traut W., Winking H. (2001). Meiotic chromosomes and stages of sex chromosome evolution in fish: zebrafish, platyfish and guppy. Chromosome Res. 9, 659–672. 10.1023/A:1012956324417 PubMed DOI

Utsunomia R., Pansonato-Alves J. C., Paiva L. R. S., Costa Silva G. J., Oliveira C., Bertollo L. A. C., et al. . (2014). Genetic differentiation among distinct karyomorphs of the wolf fish Hoplias malabaricus species complex (Characiformes, Erythrinidae) and report of unusual hybridization with natural triploidy. J. Fish Biol. 85, 1682–1692. 10.1111/jfb.12526 PubMed DOI

Valente T. G., Schneider C. H., Gross M. C., Feldberg E., Martins C. (2009). Comparative cytogenetics of cichlid fishes through genomic in-situ hybridization (GISH) with emphasis on Oreochromis niloticus. Chromosome Res. 17, 791–799. 10.1007/s10577-009-9067-5 PubMed DOI

Woram R. A., Gharbi K., Sakamoto T., Hoyheim B., Holm L. E., Naish K., et al. . (2003). Comparative genome analysis of the primary sex-determining locus in salmonid fishes. Genome Res. 13, 272–280. 10.1101/gr.578503 PubMed DOI PMC

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

Zhou Q., Braasch I., Froschauer A., Böhne A. (2010). A novel marker for the platyfish (Xiphophorus maculatus) W chromosome is derived from a Polinton transposon. J. Genet. Genomics 37, 181–188. 10.1016/S1673-8527(09)60036-9 PubMed DOI

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

Repetitive DNAs and differentiation of the ZZ/ZW sex chromosome system in the combtail fish Belontia hasselti (Perciformes: Osphronemidae)

Satellite DNAs and the evolution of the multiple X1X2Y sex chromosomes in the wolf fish Hoplias malabaricus (Teleostei; Characiformes)

Cross-species chromosome painting and repetitive DNA mapping illuminate the karyotype evolution in true crocodiles (Crocodylidae)

Against the mainstream: exceptional evolutionary stability of ZW sex chromosomes across the fish families Triportheidae and Gasteropelecidae (Teleostei: Characiformes)

Adding New Pieces to the Puzzle of Karyotype Evolution in Harttia (Siluriformes, Loricariidae): Investigation of Amazonian Species

Multiple sex chromosomes in teleost fishes from a cytogenetic perspective: state of the art and future challenges

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

Jekyll or Hyde? The genome (and more) of Nesidiocoris tenuis, a zoophytophagous predatory bug that is both a biological control agent and a pest

Patterns of Sex Chromosome Differentiation in Spiders: Insights from Comparative Genomic Hybridisation

Centric Fusions behind the Karyotype Evolution of Neotropical Nannostomus Pencilfishes (Characiforme, Lebiasinidae): First Insights from a Molecular Cytogenetic Perspective

Interspecific Genetic Differences and Historical Demography in South American Arowanas (Osteoglossiformes, Osteoglossidae, Osteoglossum)

Deciphering the Evolutionary History of Arowana Fishes (Teleostei, Osteoglossiformes, Osteoglossidae): Insight from Comparative Cytogenomics

Comparative Cytogenetics and Neo-Y Formation in Small-Sized Fish Species of the Genus Pyrrhulina (Characiformes, Lebiasinidae)

Deciphering the Origin and Evolution of the X1X2Y System in Two Closely-Related Oplegnathus Species (Oplegnathidae and Centrarchiformes)

Genomic Organization of Repetitive DNA Elements and Extensive Karyotype Diversity of Silurid Catfishes (Teleostei: Siluriformes): A Comparative Cytogenetic Approach

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

Emerging patterns of genome organization in Notopteridae species (Teleostei, Osteoglossiformes) as revealed by Zoo-FISH and Comparative Genomic Hybridization (CGH)

Chromosomal Evolution in Lower Vertebrates: Sex Chromosomes in Neotropical Fishes