, Volume 142, Issue 2, pp 119–126 | Cite as

Origin of the X1X1X2X2/X1X2Y sex chromosome system of Harttia punctata (Siluriformes, Loricariidae) inferred from chromosome painting and FISH with ribosomal DNA markers

  • Daniel Rodrigues Blanco
  • Marcelo Ricardo Vicari
  • Roberto Laridondo Lui
  • Roberto Ferreira Artoni
  • Mara Cristina de Almeida
  • Josiane Baccarin Traldi
  • Vladimir Pavan Margarido
  • Orlando Moreira-Filho


Harttia is a genus in the subfamily Loricariinae that accommodates fishes popularly known as armored catfishes. They show extensive karyotypic diversity regarding interspecific numerical/structural variation of the karyotypes, with the presence of the XX/XY1Y2 multiple sex chromosome system, as found in H. carvalhoi. In this context, this study aimed to characterize Harttia punctata chromosomally, for the first time, and to infer the rearrangements that originated the X1X1X2X2/X1X2Y multiple sex chromosome system present in this species. The data obtained in this study, with classical (Giemsa, C-banding and AgNORs) and molecular methodologies (fluorescence in situ hybridization) and chromosome microdissection, indicated that a translocation between distinct acrocentric chromosomes bearing rRNA genes, accompanied by deletions in both chromosomes, might have originated the neo-Y chromosome in this species. The data also suggest that the multiple sex chromosome systems present in H. carvalhoi and H. punctata had an independent origin, evidencing the recurrence of chromosome alterations in species from this genus.


Karyotypic diversification Chromosomal translocation Sex chromosomes 



The authors are grateful to Osvaldo T. Oyakawa (MZUSP) for the identification of the specimens; to Luis H. da Silva and Pedro L. Gallo for help with the sampling; to the Instituto Brasileiro do Meio Ambiente e dos Recursos Naturais Renováveis (IBAMA—License Number: 10538-1) and the Instituto Estadual de Florestas (IEF/MG) for authorization to collect the material. This study was financed by the Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP), Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) and the Fundação Araucária (Fundação Araucária de Apoio ao Desenvolvimento Científico e Tecnológico do Estado do Paraná).


  1. Alves AL, Oliveira C, Foresti F (2003) Karyotype variability in eight species of the subfamilies Loricariinae and Ancistrinae (Teleostei, Siluriformes, Loricariidae). Caryologia 56:57–63CrossRefGoogle Scholar
  2. Andreata AA, Almeida-Toledo LF, Oliveira C, Toledo-Filho AS (1993) Chromosome studies in Hypoptopomatinae (Pisces, Siluriformes, Loricariidae): II ZZ/ZW sex chromosome system, B-chromosomes, and constitutive heterochromatin differentiation in Microlepdogaster leucofrenatus. Cytogenet Cell Genet 63:215–220PubMedCrossRefGoogle Scholar
  3. Artoni RF, Bertollo LAC (2001) Trends in the karyotype evolution of Loricariidae fish (Siluriformes). Hereditas 134:201–210PubMedCrossRefGoogle Scholar
  4. Artoni RF, Bertollo LAC (2002) Evolutionary aspects of the ZZ/ZW sex chromosome system in the Characidae fish, genus Triportheus. A monophyletic state and NOR location on the W chromosome. Heredity 89:15–19PubMedCrossRefGoogle Scholar
  5. Artoni RF, Falcão JN, Moreira-Filho O, Bertollo LAC (2001) An uncommon condition for a sex chromosome system in Characidae fish. Distribution and differentiation of the ZZ/ZW system in Triportheus. Chromosom Res 9:449–456CrossRefGoogle Scholar
  6. Bertollo LAC, Takahashi CS, Moreira-Filho O (1978) Cytotaxonomic considerations on Hoplias lacerdae (Pisces, Erythrinidae). Braz J Genet 2:103–120Google Scholar
  7. Blanco DR, Vicari MR, Lui RL, Traldi JB, Bertollo LA, Moreira-Filho O (2013) The role of the Robertsonian rearrangements in the origin of the XX/XY1Y2 sex chromosome system and in the chromosomal differentiation in Harttia species (Siluriformes, Loricariidae). Rev Fish Biol Fish 23:127–134CrossRefGoogle Scholar
  8. 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 8:111–118CrossRefGoogle Scholar
  9. Centofante L, Bertollo LAC, Moreira-Filho O (2006) Cytogenetic characterization and description of an XX/XY1Y2 sex chromosome system in catfish Harttia carvalhoi (Siluriformes, Loricariidae). Cytogenet Genome Res 12:320–324CrossRefGoogle Scholar
  10. Charlesworth D, Charlesworth B, Marais G (2005) Steps in the evolution of heteromorphic sex chromosomes. Heredity 95:118–128PubMedCrossRefGoogle Scholar
  11. Cioffi MB, Martins C, Bertollo LAC (2010) 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 10:271PubMedCentralPubMedCrossRefGoogle Scholar
  12. Costa-Silva GJ (2009) Análise filogenética entre gêneros da subfamília loricariinae (Siluriformes: Loricariidae) com ênfase no gênero Harttia, baseada em caracteres moleculares. MSc dissertation (in Portuguese) Botucatu, Brazil: Programa de Pós-Graduação em Ciências BiológicasGoogle Scholar
  13. de Oliveira RR, Souza IL, Venere PC (2006) Karyotype description of three species of Loricariidae (Siluriformes) and occurrence of the ZZ/ZW sexual system in Hemiancistrus spilomma Cardoso & Lucinda, 2003. Neotrop Ichthyol 4:93–97Google Scholar
  14. de Oliveira RR, Feldberg F, Anjos MB, Zuanon J (2007) Karyotype characterization and ZZ/ZW sex chromosome heteromorphism in two species of the catfish genus Ancistrus Kner, 1854 (Siluriformes: Loricariidae) from the Amazon basin. Neotrop Ichthyol 5:301–306Google Scholar
  15. de Oliveira RR, Feldberg F, 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 134:243–249PubMedCrossRefGoogle Scholar
  16. Diniz D, Moreira-Filho O, Bertollo LAC (2007) Molecular cytogenetics and characterization of a ZZ/ZW sex chromosome system in Triportheus nematurus (Characiformes, Characidae). Genetica 133:85–91PubMedCrossRefGoogle Scholar
  17. Epplen JT, McCarrey JR, Sutou S, Ohno S (1982) Base sequence of a; cloned snake W chromosome DNA fragment and identification of a male-specific putative mRNA in the mouse. Proc Natl Acad Sci USA 79:3798–3802PubMedCentralPubMedCrossRefGoogle Scholar
  18. Ferreira IA, Bertollo LAC, Martins C (2007) Comparative chromosome mapping of 5S rDNA and 5S Hind III repetitive sequences in Erythrinidae fishes (Characiformes) with emphasis on the Hoplias malabaricus ‘species complex’. Cytogenet Genome Res 118:78–83PubMedCrossRefGoogle Scholar
  19. Foresti F, Oliveira C, Almeida-Toledo LF (1993) A method for chromosome preparations from large specimens of fishes using ‘in vitro’ short treatment with colchicine. Experientia 49:810–813CrossRefGoogle Scholar
  20. Galetti PM Jr, Foresti F (1986) Evolution of the ZZ/ZW system in Leporinus (Pisces, Anostomidae). Cytogenet Cell Genet 43:43–46CrossRefGoogle Scholar
  21. Griffiths SP (2000) The use of clove oil as an anaesthetic and method for sampling intertidal rockpool fishes. J Fish Biol 57:1453–1464CrossRefGoogle Scholar
  22. Haaf T, Schmid M (1984) An early stage of ZZ/ZW sex chromosomes differentiation in Poecilia sphenops var. melanistica (Poeciliidae, Cyprinodontiformes). Chromosoma 89:37–41CrossRefGoogle Scholar
  23. Hatanaka T, Galetti PM Jr (2004) Mapping of the 18S and 5S ribosomal RNA genes in the fish Prochilodus argenteus Agassiz, 1829 (Characiformes, Prochilodontidae). Genetica 122:239–244PubMedCrossRefGoogle Scholar
  24. Howell WM, Black DA (1979) Location of the nucleolus organizer regions on the sex chromosomes of the banded killifish, Fundulus diaphanus. Copeia 3:544–546CrossRefGoogle Scholar
  25. Howell WM, Black DA (1980) Controlled silver-staining of nucleolus organizer regions with a protective colloidal developer: a 1-step method. Experientia 36:1014–1015PubMedCrossRefGoogle Scholar
  26. Ijdo JW, Wells RA, Baldini A, Reeders ST (1991) Improved telomere detection using a telomere repeat probe (TTAGGG)n generated by PCR. Nucl Acids Res 19:4780PubMedCentralPubMedCrossRefGoogle Scholar
  27. Jones KW, Singh L (1985) Snakes and the evolution of sex chromosomes. Trends Genet 2:55–60CrossRefGoogle Scholar
  28. Kavalco KF, Pazza R, Bertollo LAC, Moreira-Filho O (2004) Heterochromatin characterization of four fish species of the family Loricariidae (Siluriformes). Heredity 141:237–242CrossRefGoogle Scholar
  29. Kavalco KF, Pazza R, Bertollo LAC, Moreira-Filho O (2005) Karyotypic diversity and evolution of Loricariidae (Pisces, Siluriformes). Heredity 94:180–186PubMedCrossRefGoogle Scholar
  30. Kitano J, Peichel CL (2011) Turnover of sex chromosomes and speciation is fishes. Environ Biol Fish 94:549–558CrossRefGoogle Scholar
  31. Levan A, Fredga K, Sandberg AA (1964) Nomenclature for centromeric position on chromosomes. Hereditas 52:201–220CrossRefGoogle Scholar
  32. Lucchesi JC (1999) On the origin of sex chromosomes. Bioessays 21:188–190PubMedCrossRefGoogle Scholar
  33. Lui RL, Blanco DR, Margarido VP, Moreira-Filho O (2009) First description of B chromosomes in the family Auchenipteridae, Parauchenipterus galeatus (Siluriformes) of the São Francisco River basin (MG, Brazil). Micron 40:552–559PubMedCrossRefGoogle Scholar
  34. Machado TC, Pansonato-Alves JC, Pucci MB, Nogaroto V, Almeida MC, Oliveira C, Foresti F, Bertollo LAC, Moreira-Filho O, Artoni RF, Vicari MR (2011) Chromosomal painting and ZW sex chromosomes differentiation in Characidium (Characiformes, Crenuchidae). BMC Genet 12:65PubMedCentralPubMedCrossRefGoogle Scholar
  35. Mariotto S, Artoni RF, Miyazawa CS (2004) Occurrence of sexual chromosome, of the type ZZ/ZW in Ancistrus cf. dubius (Loricariidae, Ancistrinae) of the Paraguay River Basin, Mato Grosso, Brazil. Caryologia 57:327–331CrossRefGoogle Scholar
  36. Mariotto S, Centofante L, Vicari MR, Artoni RF, Moreira-Filho O (2011) Chromosomal diversification in ribosomal DNA sites in Ancistrus Kner, 1854 (Loricariidae, Ancistrini) from three hydrographic basins of Mato Grosso, Brazil. Comp Cytogenet 5:289–300PubMedCentralPubMedCrossRefGoogle Scholar
  37. Martins C, Galetti PM Jr (1999) Chromosomal localization of 5S DNA genes in Leporinus fish (Anostomidae, Characiformes). Chromosom Res 7:363–367CrossRefGoogle Scholar
  38. Moran P, Martinez JL, Garcia-Vazquez E, Pendas AM (1996) Sex chromosome linkage of 5S rDNA in rainbow trout (Oncorhynchus mykiss). Cytogenet Genome Res 75:2–3CrossRefGoogle Scholar
  39. Moreira-Filho O, Bertollo LAC, Galetti PM Jr (1993) Distribution of sex chromosome mechanisms in neotropical fish and description of a ZZ/ZW system in Parodon hilarii (Parodontidae). Caryologia 46:115–125CrossRefGoogle Scholar
  40. Nanda I, Schartl M, Feichtinger W, Epplen JT, Schmid M (1992) Early stages of sex chromosome differentiation in fish as analysed by simple repetitive DNA sequences. Chromosoma 101:301–310PubMedCrossRefGoogle Scholar
  41. Oliveira C, Foresti F, Hilsdorf AWS (2009) Genetics of neotropical fish: from chromosomes to populations. Fish Physiol Biochem 35:81–100PubMedCrossRefGoogle Scholar
  42. Phillips RB, Ihssen PE (1985) Identification of sex chromosomes in lake trout (Salvelinus namaycush). Cytogenet Cell Genet 39:14–18PubMedCrossRefGoogle Scholar
  43. Pinkel D, Straume T, Gray JW (1986) Cytogenetic analysis using quantitative, highsensitivity, fluorescence hybridization. Proc Natl Acad Sci USA 83:2934–2938PubMedCentralPubMedCrossRefGoogle Scholar
  44. Rapp Py-Daniel LH, Oliveira EC (2001) Seven new species of Harttia from the Amazonian-Guyana region (Siluriformes: Loricariidae). Ichthyol Explor Freshw 12:79–96Google Scholar
  45. Reed KM, Phillips RB (1995) Molecular cytogenetic analysis of the double-CMA3 chromosome of lake trout, Salvelinus namaycush. Cytogenet Cell Genet 70:104–107PubMedCrossRefGoogle Scholar
  46. Rodrigues RM (2010) Estudos cromossômicos e moleculares em Loricariinae com ênfase em species de Rineloricaria (Siluriformes, Loricariidae): uma perspective evolutiva. MSc dissertation (In portuguese). Instituto de Biociências da Universidade de São Paulo, Brazil, p 2018Google Scholar
  47. Rosa R, Bellafronte E, Moreira-Filho O, Margarido VP (2006) Constitutive heterochromatin, 5S and 18 rDNA genes in Apareiodon sp. (Characiformes, Parodontidae) with a ZZ/ZW sex chromosome system. Genetica 128:159–166PubMedCrossRefGoogle Scholar
  48. Rosa KO, Ziemniczak K, Barros AV, Nogaroto V, Almeida MC, Cestari MM, Artoni RF, Vicari MR (2012) Numeric and structural chromosome polymorphism in Rineloricaria lima (Siluriformes: Loricariidae): fusion points carrying 5S rDNA or telomere sequence vestiges. Rev Fish Biol Fish 22:739–749CrossRefGoogle Scholar
  49. Schemberger MO, Bellafronte E, Nogaroto V, Almeida MC, Schühli GS, Artoni RF, Moreira-Filho O, Vicari MR (2011) Differentiation of repetitive DNA sites and sex chromosome systems reveal closely related group in Parodontidae (Actinopterygii: Characiformes). Genetica 139:1499–1508PubMedCrossRefGoogle Scholar
  50. Sumner AT (1972) A simple technique for demonstrating centromeric heterochromatin. Exp Cell Res 75:304–306PubMedCrossRefGoogle Scholar
  51. Traldi JB, Blanco DR, Vicari MR, Martinez JF, Lui RL, Artoni RF, Moreira-Filho O (2013) Physical mapping of (GATA)n and (TTAGGG)n sequences in species of Hypostomus (Siluriformes, Loricariidae). J Genet 92:127–130PubMedCrossRefGoogle Scholar
  52. Vicari MR, Moreira-Filho O, Artoni RF, Bertollo LAC (2006) ZZ/ZW sex chromosome system in an undescribed species of the genus Apareiodon (Characiformes, Parodontidae). Cytogenet Genome Res 114:163–168PubMedCrossRefGoogle Scholar
  53. Ziemniczak K, Barros AV, Rosa KO, Nogaroto V, Almeida MC, Cestari MM, Moreira-Filho O, Artoni RF, Vicari MR (2012) Comparative cytogenetics of Loricariidae (Actinopterygii: Siluriformes): emphasis in Neoplecostominae and Hypoptopomatinae. Ital J Zool 79:492–501CrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2014

Authors and Affiliations

  • Daniel Rodrigues Blanco
    • 1
  • Marcelo Ricardo Vicari
    • 2
  • Roberto Laridondo Lui
    • 3
  • Roberto Ferreira Artoni
    • 2
  • Mara Cristina de Almeida
    • 2
  • Josiane Baccarin Traldi
    • 4
  • Vladimir Pavan Margarido
    • 3
  • Orlando Moreira-Filho
    • 4
  1. 1.Universidade Tecnológica Federal do ParanáSanta HelenaBrazil
  2. 2.Departamento de Biologia Estrutural, Molecular e GenéticaUniversidade Estadual de Ponta GrossaPonta GrossaBrazil
  3. 3.Centro de Ciências Biológicas e da SaúdeUniversidade Estadual do Oeste do ParanáCascavelBrazil
  4. 4.Departamento de Genética e EvoluçãoUniversidade Federal de São CarlosSão CarlosBrazil

Personalised recommendations