, Volume 127, Issue 1, pp 115–128 | Cite as

Tracking the evolutionary pathway of sex chromosomes among fishes: characterizing the unique XX/XY1Y2 system in Hoplias malabaricus (Teleostei, Characiformes)

  • Ezequiel Aguiar de Oliveira
  • Alexandr Sember
  • Luiz Antonio Carlos Bertollo
  • Cassia Fernanda Yano
  • Tariq Ezaz
  • Orlando Moreira-Filho
  • Terumi Hatanaka
  • Vladimir Trifonov
  • Thomas Liehr
  • Ahmed Basheer Hamid Al-Rikabi
  • Petr Ráb
  • Hugmar Pains
  • Marcelo de Bello Cioffi
Original Article


The Neotropical fish, Hoplias malabaricus, is one of the most cytogenetically studied fish taxon with seven distinct karyomorphs (A–G) comprising varying degrees of sex chromosome differentiation, ranging from homomorphic to highly differentiated simple and multiple sex chromosomes. Therefore, this fish offers a unique opportunity to track evolutionary mechanisms standing behind the sex chromosome evolution and differentiation. Here, we focused on a high-resolution cytogenetic characterization of the unique XX/XY1Y2 multiple sex chromosome system found in one of its karyomorphs (G). For this, we applied a suite of conventional (Giemsa-staining, C-banding) and molecular cytogenetic approaches, including fluorescence in situ hybridization FISH (with 5S and 18S rDNAs, 10 microsatellite motifs and telomeric (TTAGGG) n sequences as probes), comparative genomic hybridization (CGH), and whole chromosome painting (WCP). In addition, we performed comparative analyses with other Erythrinidae species to discover the evolutionary origin of this unique karyomorph G-specific XY1Y2 multiple sex chromosome system. WCP experiments confirmed the homology between these multiple sex chromosomes and the nascent XX/XY sex system found in the karyomorph F, but disproved a homology with those of karyomorphs A–D and other closely related species. Besides, the putative origin of such XY1Y2 system by rearrangements of several chromosome pairs from an ancestral karyotype was also highlighted. In addition, clear identification of a male-specific region on the Y1 chromosome suggested a differential pattern of repetitive sequences accumulation. The present data suggested the origin of this unique XY1Y2 sex system, revealing evidences for the high level of plasticity of sex chromosome differentiation within the Erythrinidae.


Fish cytogenetics Male-specific region Whole chromosome painting Comparative genomic hybridization Repetitive sequences 



We would like to thank Mr. Valdivino Pereira da Silva (Renascer farm) for helping during the sampling process.

Funding information

This study was supported by Conselho Nacional de Desenvolvimento Científico e Tecnológico - CNPq (Proc. Nos. 304992/2015-1, 306896/2014-1, and 152105/2016-6) and Fundação de Amparo à Pesquisa do Estado de São Paulo- FAPESP (Proc. No. 2016/21411-7) and further by the projects EXCELLENCE CZ.02.1.01/0.0/0.0/15_003/0000460 OP RDE and RVO: 67985904.

Compliance with ethical standards

The experiments followed ethical and anesthesia conducts, in accordance with the Ethics Committee on Animal Experimentation of the Universidade Federal de São Carlos (Process Number CEUA 1853260315).

Conflict of interest

The authors declare that they have no conflict of interest.

Informed consent

Informed consent was obtained from all individual participants included in the study.


  1. Almeida-Toledo LF, Foresti F (2001) Morphologically differentiated sex chromosomes in neotropical freshwater fish. Genetica 111:91–100. CrossRefPubMedGoogle Scholar
  2. Arai R (2011) Fish karyotypes: a check list. 1st edn. Springer, TokyoCrossRefGoogle Scholar
  3. Bachtrog D, Charlesworth B (2001) Towards a complete sequence of the human Y chromosome. Genome Biol 2:1–5. CrossRefGoogle Scholar
  4. 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. Chromosom Res 21:137–147. CrossRefGoogle Scholar
  5. Barros AV, Wolski MAV, Nogaroto V, Almeida MC, Moreira-Filho O, Vicari MC (2017) Fragile sites, dysfunctional telomere and chromosome fusions: what is 5S rDNA role? Gene 608:20–27. CrossRefPubMedGoogle Scholar
  6. Bertollo LAC (2007) Chromosome evolution in the Neotropical Erythrinidae fish family: an overview. In: Pisano E, Ozouf-Costaz C, Foresti F, Kapoor BG (eds) Fish cytogenetics. Science Publishers, Enfield, pp 195–211Google Scholar
  7. Bertollo LAC, Takahashi CS, Moreira-Filho O (1983) Multiple sex chromosomesin the genus Hoplias (Pisces, Erythrinidae). Cytologia 48:1–12. CrossRefGoogle Scholar
  8. Bertollo LAC, Fontes MS, Fenocchio AS, 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.Google Scholar
  9. Bertollo LAC, Born GG, Dergam JA, Fenocchio AS, Moreira-Filho O (2000) A biodiversity approach in the neotropical Erythrinidae fish, Hoplias malabaricus. Karyotypic survey, geographic distribution of cytotypes and cytotaxonomic considerations. Chromosom Res 8:603–613. CrossRefGoogle Scholar
  10. Bertollo LAC, Moreira-Filho O, Cioffi MB (2015) Direct chromosome preparations from freshwater teleost fishes. In: Ozouf-Costaz C, Pisano E, Foresti F, Almeida Toledo LF (eds) Fish techniques, Ray-Fin Fishes and Chondrichthyans. CRC Press, Boca Raton, pp 21–26CrossRefGoogle Scholar
  11. Bitencourt JA, Sampaio I, Ramos RTC, Vicari MR, Affonso PRAM (2016) First report of sex chromosomes in Achiridae (Teleostei: Pleuronectiformes) with inferences about the origin of the multiple X1X1X2X2/X1X2Y system and dispersal of ribosomal genes in Achirus achirus. Zebrafish 14:90–95. CrossRefPubMedGoogle Scholar
  12. Blanco DR, Lui RL, Bertollo LAC, Diniz D, Moreira Filho O (2010a) Characterization of invasive fish species in a river transposition region: evolutionary chromosome studies in the genus Hoplias (Characiformes, Erythrinidae). Rev Fish Biol Fish 20:1–8. CrossRefGoogle Scholar
  13. Blanco DR, Lui RL, Bertollo LAC, Margarido VP, Moreira-Filho O (2010b) Karyotypic diversity between allopatric populations of the group Hoplias malabaricus (Characiformes: Erythrinidae): evolutionary and biogeographic considerations. Neotrop Ichthyol 8:361–368. CrossRefGoogle Scholar
  14. Blanco DR, Lui RL, Vicari MR, Bertollo LAC, 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. CrossRefPubMedGoogle Scholar
  15. Blanco DR, Vicari MR, Lui RL, Artoni RF, de Almeida MC, Traldi JB, Margarido VP (2014) Origin of the X1X1X2X2/X1X2Y sex chromosome system of Harttia punctata (Siluriformes, Loricariidae) inferred from chromosome painting and FISH with ribosomal DNA markers. Genetica 142:119–126. PubMedGoogle Scholar
  16. Born GG, Bertollo LAC (2000) An XX/XY sex chromosome system in a fish species, Hoplias malabaricus, with a polymorphic NOR-bearing X chromosome. Chromosom Res 8:111–118. CrossRefGoogle Scholar
  17. Chalopin D, Volff J-N, Galiana D, Anderson JL, Schartl M (2015) Transposable elements and early evolution of sex chromosomes in fish. Chromosom Res 23:545–560. CrossRefGoogle Scholar
  18. Charlesworth D, Charlesworth B, Marais G (2005) Steps in the evolution of heteromorphic sex chromosomes. Heredity 95:118–128. CrossRefPubMedGoogle Scholar
  19. Charlesworth D, Mank J (2010) The birds and the bees and the flowers and the trees: lessons from genetic mapping of sex determination in plants and animals. Genetics 186:9–31. CrossRefPubMedPubMedCentralGoogle Scholar
  20. Charlesworth B, Wall JD (1999) Inbreeding, heterozygote advantage and the evolution of neo-X and neo-Y sex chromosomes. Proc R Soc Lond B 266:51–56. CrossRefGoogle Scholar
  21. Cioffi MB, Martins C, Centofante L, Jacobina U, Bertollo LAC (2009) Chromosomal variability among allopatric populations of Erythrinidae fish Hoplias malabaricus: mapping of three classes of repetitive DNAs. Cytogenet Genome Res 125:132–141. CrossRefPubMedGoogle Scholar
  22. Cioffi MB, Bertollo LAC (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. CrossRefPubMedGoogle Scholar
  23. Cioffi MB, Martins C, Bertollo LAC (2010a) Chromosome spreading of associated transposable elements and ribosomal DNA in the fish Erythrinus erythrinus. Implications for genome change and karyoevolution in fish. BMC Evol Biol 10:271. CrossRefPubMedPubMedCentralGoogle Scholar
  24. Cioffi MB, Martins C, Vicari MR, Rebordinos L, Bertollo LAC (2010b) 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. CrossRefPubMedGoogle Scholar
  25. Cioffi MB, Camacho JPM, Bertollo LAC (2011) Repetitive DNAs and differentiation of sex chromosomes in neotropical fishes. Cytogenet Genome Res 132:188–194. CrossRefPubMedGoogle Scholar
  26. Cioffi MB, Molina WF, Artoni RF, Bertollo LAC (2012) Chromosomes as tools for discovering biodiversity—the case of Erythrinidae fish family. In: Tirunilai P (ed) Recent trends in cytogenetic studies—methodologies and applications. InTech Publisher, pp 125–146Google Scholar
  27. Cioffi MB, Liehr T, Trifonov V, Molina WF, Bertollo LAC (2013) Independent sex chromosome evolution in lower vertebrates: a molecular cytogenetic overview in the Erythrinidae fish family. Cytogenet Genome Res 141:186–194. CrossRefPubMedGoogle Scholar
  28. Cocca E, Petraccioli A, Morescalchi MA, Odierna G, Capriglione T (2015) Laser microdissection-based analysis of the Y sex chromosome of the Antarctic fish Chionodraco hamatus (Notothenioidei, Channichthyidae). Comp Cytogenet 9:1–15. CrossRefPubMedPubMedCentralGoogle Scholar
  29. Devlin RH, Nagahama Y (2002) Sex determination and sex differentiation in fish: an overview of genetic, physiological, and environmental influences. Aquaculture 208:191–364. CrossRefGoogle Scholar
  30. Ezaz T, Valenzuela N, Grützner F, Miura I, Georges A, Burke RL, Graves JAM (2006) An XX/XY sex microchromosome system in a freshwater turtle, Chelodina longicollis (Testudines: Chelidae) with genetic sex determination. Chromosom Res 14:139–150. CrossRefGoogle Scholar
  31. Ferreira IA, Bertollo LAC, Martins C (2007) Comparative chromosome mapping of 5S rDNA and 5SHindIII repetitive sequences in Erythrinidae fishes (Characiformes) with emphasis on the Hoplias malabaricus “species complex”. Cytogenet Genome Res 118:78–83. CrossRefPubMedGoogle Scholar
  32. Ferreira M, Garcia C, Matoso DA, de Jesus IS, Feldberg E (2016) A new multiple sex chromosome system X1X1X2X2/X1Y1X2Y2 in Siluriformes: cytogenetic characterization of Bunocephalus coracoideus (Aspredinidae). Genetica 144:591–599. CrossRefPubMedGoogle Scholar
  33. Freitas NL, Al-Rikabi ABH, Bertollo LAC, Ezaz T, Yano CF, de Oliveira EA, Hatanaka T et al (2017) Early stages of XY sex chromosomes differentiation in the fish Hoplias malabaricus (Characiformes, Erythrinidae) revealed by DNA repeats accumulation. Curr Genomics.
  34. Ijdo JW, Wells RA, Baldini A, Reeders ST (1991) Improved telomere detection using a telomere repeat probe (TTAGGG)n generated by PCR. Nucleid Acids Res 19:4780CrossRefGoogle Scholar
  35. 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. CrossRefPubMedGoogle Scholar
  36. King M (1993) Species evolution: the role of chromosome change. University Press, CambridgeGoogle Scholar
  37. Kitano J, Peichel CL (2012) Turnover of sex chromosomes and speciation in fishes. Environ Biol Fish 94:549–558. CrossRefGoogle Scholar
  38. Kejnovsky E, Hobza R, Cermak T, Z Kubat Z, Vyskot B (2009) The role of repetitive DNA in structure and evolution of sex chromosomes in plants. Heredity 102:533–541. CrossRefPubMedGoogle Scholar
  39. Kejnovský E, Michalovová M, Šteflova P, Kejnovská I, Manzano S, Hobza R, Kubát Z (2013) Expansion of microsatellites on evolutionary young Y chromosome. PLoS One 8:e45519. CrossRefPubMedPubMedCentralGoogle Scholar
  40. Kraemer C, Schmidt ER (1993) The sex determining region of Chironomus thummi is associated with highly repetitive DNA and transposable elements. Chromosoma 102:553–562. CrossRefPubMedGoogle Scholar
  41. Kubát Z, Hobza R, Vyskot B, Kejnovsky E (2008) Microsatellite accumulation in the Y chromosome of Silene Latifolia. Genome 51:350–356. CrossRefPubMedGoogle Scholar
  42. Levan A, Fredga K, Sandberg AA (1964) Nomenclature for centromeric position on chromosomes. Hereditas 52:201–220. CrossRefGoogle Scholar
  43. Machado TC, Pansonato-Alves JC, Pucci MB, Nogaroto V, Almeida MC, Oliveira C, Foresti F et al (2011) Chromosomal painting and ZW sex chromosomes differentiation in Characidium (Characiformes, Crenuchidae). BMC Genet 12:65. CrossRefPubMedPubMedCentralGoogle Scholar
  44. Mank JE, Avise JC (2009) Evolutionary diversity and turn-over of sex determination in teleost fishes. Sex Dev 3:60–67. CrossRefPubMedGoogle Scholar
  45. Mank JE, Promislow DEL, Avise JC (2006) Evolution of alternative sex-determining mechanisms in teleost fishes. Biol J Linn Soc 87:83–93. CrossRefGoogle Scholar
  46. Martins C (2007) Chromosomes and repetitive DNAs: a contribution to the knowledge of the fish genome. In: Pisano E, Ozouf-Costaz C, Foresti F, Kapoor BG (eds) Fish cytogenetics. Science Publishers, Enfield, pp 421–453Google Scholar
  47. Martins C, Ferreira IA, Oliveira C, Foresti F, Galetti Jr PM (2006) A tandemly repetitive centromeric DNA sequence of the fish Hoplias malabaricus (Characiformes: Erythrinidae) is derived from 5S rDNA. Genetica 127:133–141. CrossRefPubMedGoogle Scholar
  48. Martins NF, Bertollo LAC, Troy WP, Feldberg E, Valentin FCS, Cioffi MB (2013) Differentiation and evolutionary relationships in Erythrinus erythrinus (Characiformes, Erythrinidae): comparative chromosome mapping of repetitive sequences. Rev Fish Biol Fish 23:261–269. CrossRefGoogle Scholar
  49. Noronha RCR, Nagamachi CY, O’Brien PCM, Ferguson-Smith MA, Pieczarka JCN (2009) Neo-XY body: an analysis of XY1Y2 meiotic behavior in Carollia (Chiroptera, Phyllostomidae) by chromosome painting. Cytogenet Genome Res 124:37–43. CrossRefPubMedGoogle Scholar
  50. Ohno S (1967) Sex chromosomes and sex-linked genes. Springer-Verlag, Berlin. Heidelberg. New YorkCrossRefGoogle Scholar
  51. Oliveira C, Almeida-Toledo LF, Foresti F (2007) Karyotypic evolution in Neotropical fishes. In: Pisano E, Ozouf-Costaz C, Foresti F, Kapoor BG (eds) Fish cytogenetics. Science Publishers, Enfield, pp 111–164Google Scholar
  52. Oliveira C, Foresti F, Hilsdorf AWS (2009) Genetics of neotropical fish: from chromosomes to populations. Fish Physiol Biochem 35:81–100. CrossRefPubMedGoogle Scholar
  53. Oliveira RR, Feldberg E, dos Anjos MB, Zuanon J (2008) Occurrence of multiple sexual chromosomes (XX/XY1Y2 and Z1Z1Z2Z2/Z1Z2W1W2) in catfishes of the genus Ancistrus (Siluriformes: Loricariidae) from the Amazon basin. Genetica 134:243–249. CrossRefPubMedGoogle Scholar
  54. Oyakawa OT (2003) Family Erythrinidae. In: Reis RE, Kullander SO, Ferraris Jr CJ (eds) Check list of the freshwater fishes of South and Central America. Edipucrs, Porto Alegre, pp 238–240Google Scholar
  55. Oyakawa OT, Mattox GMT (2009) Revision of the Neotropical trahiras of the Hoplias lacerdae species-group (Ostariophysi: Characiformes: Erythrinidae) with descriptions of two new species. Neotrop Ichthyol 7:117–140CrossRefGoogle Scholar
  56. Palacios-Gimenez OM, Castillo ER, Marti DA, Cabral-de-Mello DC (2013) Tracking the evolution of sex chromosome systems in Melanoplinae grasshoppers through chromosomal mapping of repetitive DNA sequences. BMC Evol Biol 13:167. CrossRefPubMedPubMedCentralGoogle Scholar
  57. Parise-Maltempi PP, Martins C, Oliveira C, Foresti F (2007) Identification of a new repetitive element in the sex chromosomes of Leporinus elongatus (Teleostei: Characiformes: Anostomidae): new insights into the sex chromosomes of Leporinus. Cytogenet Genome Res 116:218–223. CrossRefPubMedGoogle Scholar
  58. Pennell MW, Kirkpatrick M, Otto SP, Vamosi JC, Peichel CL, Valenzuela N, Kitano J (2015) Y fuse? Sex chromosome fusions in fishes and reptiles. PLoS Genet 11:e1005237. pgen.1005237 CrossRefPubMedPubMedCentralGoogle Scholar
  59. Poltronieri J, Marquioni V, Bertollo LAC, Kejnovsky E, Molina WF, Liehr T, Cioffi MB (2014) Comparative chromosomal mapping of microsatellites in Leporinus species (Characiformes, Anostomidae): unequal accumulation on the W chromosomes. Cytogenet Genome Res 142:40–45. CrossRefPubMedGoogle Scholar
  60. Pokorná M, Kratochvíl L, Kejnovský E (2011) Microsatellite distribution on sex chromosomes at different stages of heteromorphism and heterochromatinization in two lizard species (Squamata: Eublepharidae: Coleonyx elegans and Lacertidae: Eremias velox). BMC Genet 12:90. CrossRefPubMedPubMedCentralGoogle Scholar
  61. Pokorná M, Rábová M, Ráb P, Ferguson-Smith MA, Rens W, Kratochvíl L (2010) Differentiation of sex chromosomes and karyotypic evolution in the eye-lid geckos (Squamata: Gekkota: Eublepharidae), a group with different modes of sex determination. Chromosom Res 18:809–820. CrossRefGoogle Scholar
  62. Reed KM, Phillips RB (1997) Polymorphism of the nucleolus organizer region (NOR) on the putative sex chromosomes of Arctic char (Salvelinus alpinus) is not sex related. Chromosom Res 5:221–227. CrossRefGoogle Scholar
  63. Rosa R, Laforga Vanzela AL, Rubert M, Martins-Santos IC, 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. CrossRefPubMedGoogle Scholar
  64. Sambrook J, Russell DW (2001) Molecular cloning: a laboratory manual, 3rd edn. Cold Spring Harbor, New YorkGoogle Scholar
  65. Santos U, Völcker CM, Belei FA, Cioffi MB, Bertollo LAC, Paiva SR, Dergam JA (2009) Molecular and karyotypic phylogeography in the Neotropical Hoplias malabaricus (Erythrinidae) fish in eastern Brazil. J Fish Biol 75:2326–2343. CrossRefPubMedGoogle Scholar
  66. Scacchetti PC, Utsunomia R, Pansonato-Alves JC, da Costa Silva GJ, Vicari MR, Artoni RF, Oliveira C (2015) Repetitive DNA sequences and evolution of ZZ/ZW sex chromosomes in Characidium (Teleostei: Characiformes). PLoS One 10:e0137231. CrossRefPubMedPubMedCentralGoogle Scholar
  67. Schartl M, Schmid M, Nanda I (2016) Dynamics of vertebrate sex chromosome evolution: from equal size to giants and dwarfs. Chromosoma 125:553–571. CrossRefPubMedGoogle Scholar
  68. Sember A, Bohlen J, Šlechtová V, Altmanová M, Symonová R, Ráb P (2015) 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 15:251. CrossRefPubMedPubMedCentralGoogle Scholar
  69. Sumner AT (1972) A simple technique for demonstrating centromeric heterochromatin. Exp Cell Res 75:304–306. CrossRefPubMedGoogle Scholar
  70. Symonová R, Sember A, Majtánová Z, Ráb P (2015) Characterization of fish genomes by GISH and CGH. In: Ozouf-Costaz C, Pisano E, Foresti F, Almeida-Toledo LF (eds) Fish cytogenetic techniques (Chondrichthyans and Teleosts). CRC Press, Inc., Enfield, pp 118–131CrossRefGoogle Scholar
  71. Terencio ML, Schneider CH, Gross MC, Vicari MR, Farias IP, Passos KB, Feldberg E (2013) Evolutionary dynamics of repetitive DNA in Semaprochilodus (Characiformes, Prochilodontidae): a fish model for sex chromosome differentiation. Sex Dev 7:325–333. CrossRefPubMedGoogle Scholar
  72. Wang X, Zhang Q, Ren J, Jiang Z, Wang C, Zhuang W, Zhai T (2009) The preparation of sex-chromosome-specific painting probes and construction of sex chromosome DNA library in half-smooth tongue sole (Cynoglossus semilaevis). Aquaculture 297:78–84. CrossRefGoogle Scholar
  73. Willhoeft U, Franz G (1996) Identification of the sex-determining region of the Ceratitis Capitata Y chromosome by deletion mapping. Genetics 144:737–745PubMedPubMedCentralGoogle Scholar
  74. Woram RA, Gharbi K, Sakamoto T, Hoyheim B, Holm L-E, Naish K, McGowan C et al (2003) Comparative genome analysis of the primary sex-determining locus in salmonid fishes. Genome Res 13:272–280. CrossRefPubMedPubMedCentralGoogle Scholar
  75. Xu D, Lou B, Bertollo LAC, Cioffi MB (2013) Chromosomal mapping of microsatellite repeats in the rock bream fish Oplegnathus fasciatus, with emphasis of their distribution in the neo-Y chromosome. Mol Cytogenet 6:12. CrossRefPubMedPubMedCentralGoogle Scholar
  76. Yang F, Trifonov V, Ng BL, Kosyakova N, Carter NP (2009) Generation of paint probes by flowsorted and microdissected chromosomes. In: Liehr T (ed) Fluorescence in situ hybridization (FISH)—application guide, 2nd edn. Springer, Berlin, pp 35–52CrossRefGoogle Scholar
  77. Yano CF, Bertollo LAC, Cioffi MB (2017a) Fish-FISH: molecular cytogenetics in fish species. In: Liehr T (ed) Fluorescence in situ hybridization (FISH)—application guide, 2nd edn. Springer, Berlin, pp 429–444CrossRefGoogle Scholar
  78. Yano CF, Bertollo LAC, Ezaz T, Trifonov V, Sember A, Liehr T, Cioffi MB (2017b) Highly conserved Z and molecularly diverged W chromosomes in the fish genus Triportheus (Characiformes, Triportheidae). Heredity 118:276–283. CrossRefPubMedGoogle Scholar
  79. Zwick MS, Hanson RE, McKnight TD, Islam-Faridi MN, Stelly DM, Wing RA, Price HJ (1997) A rapid procedure for the isolation of C0t-1 DNA from plants. Genome 40:138–142. CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany 2017

Authors and Affiliations

  • Ezequiel Aguiar de Oliveira
    • 1
    • 2
  • Alexandr Sember
    • 3
  • Luiz Antonio Carlos Bertollo
    • 1
  • Cassia Fernanda Yano
    • 1
  • Tariq Ezaz
    • 4
  • Orlando Moreira-Filho
    • 1
  • Terumi Hatanaka
    • 1
  • Vladimir Trifonov
    • 5
  • Thomas Liehr
    • 6
  • Ahmed Basheer Hamid Al-Rikabi
    • 6
  • Petr Ráb
    • 3
  • Hugmar Pains
    • 7
  • Marcelo de Bello Cioffi
    • 1
  1. 1.Departamento de Genética e EvoluçãoUniversidade Federal de São CarlosSão CarlosBrazil
  2. 2.Secretaria de Estado de Educação de Mato Grosso – SEDUC-MTCuiabáBrazil
  3. 3.Laboratory of Fish Genetics, Institute of Animal Physiology and GeneticsCzech Academy of SciencesLiběchovCzech Republic
  4. 4.Institute for Applied EcologyUniversity of CanberraCanberraAustralia
  5. 5.Institute of Molecular and Cellular Biology SB RASNovosibirskRussia
  6. 6.Jena University Hospital, Universitatsklinikum Jena, Institute of Human GeneticsJenaGermany
  7. 7.Universidade Estadual de Maringá (UEM)MaringáBrazil

Personalised recommendations