Advertisement

Reviews in Fish Biology and Fisheries

, Volume 21, Issue 3, pp 613–621 | Cite as

Chromosomal characterization of two species of genus Steatogenys (Gymnotiformes: Rhamphichthyoidea: Steatogenini) from the Amazon basin: sex chromosomes and correlations with Gymnotiformes phylogeny

  • Adauto Lima Cardoso
  • Julio Cesar Pieczarka
  • Eliana Feldberg
  • Susana Suely Rodrigues Milhomem
  • Thiago Moreira-Almeida
  • Danillo dos Santos Silva
  • Patrícia Corrêa da Silva
  • Cleusa Yoshiko Nagamachi
Research Paper

Abstract

Gymnotiformes are an important component of the Neotropical ichthyofauna and they are known for their ability to generate and detect electrical discharges. Phylogenetic relationships of Gymnotiformes are still not well understood. However, the monophyly of the superfamily Rhamphichthyoidea is well accepted, despite the position of tribe Steatogenini (Steatogenys, Hypopygus and Stegostenopos) within this superfamily is unclear. The genus Steatogenys includes three species that, together with Hypopygus and Stegostenopos, form tribe Steatogenini. Cytogenetic information is currently only available for Hypopygus lepturus. Here, we describe the karyotypes of Steatogenys elegans from four localities and S. duidae from two localities. S. elegans was found to have 2n = 50, ZZ/ZW (12m-sm/38st-a), while S. duidae had 2n = 50 (50m-sm). In S. elegans, constitutive heterochromatin (CH) was observed in the centromeric regions of all chromosomes, in the interstitial region of 1q, and in two blocks of Wq. In S. duidae, CH was observed in the centromeric and pericentromeric regions of all chromosomes, and in the interstitial regions of 2q, 3q, 5q, and 7q. Nucleolar organizer regions (NORs) were identified in the distal regions of one chromosome pair in each species. The CMA3 fluorochrome (specific to G-C rich regions) coincided with the NORs in both species, and with the HC of S. elegans except on chromosome pair 5 and the W. The DAPI fluorochrome (specific to A-T rich regions) coincided with the CH of both species, and was very intense for chromosome pair 5 and the W of S. elegans. Our observations suggest that the ZZ/ZW system observed in S. elegans likely evolved through CH addition followed by a paracentric inversion. The chromosomal data described herein are consistent with the phylogenetic hypothesis that tribe Steatogenini should be positioned within family Ramphychthyidae.

Keywords

Electric fish Sex chromosomes Fluorochromes Chromosome rearrangements Karyotypic evolution 

Notes

Acknowledgments

We acknowledge Dr. José Alves Gomes (Instituto Nacional de Pesquisas da Amazônia) and Dr. William Gareth Richard Crampton (Department of Biology, University of Central Florida, Orlando, USA) for helping with the taxonomic identification of some specimens of S. duidae and S. elegans, respectively; the technician Jonas Alves Oliveira for helping to collected sample from Mamirauá; the IDSM (Instituto de Desenvolvimento Sustentável Mamirauá) for logistic support to collect sample. Funds were supported by CNPq, FAPESPA, CAPES, UFPA, INPA. Collecting was authorized by IBAMA (Instituto Brasileiro do Meio Ambiente) permit 13248-1 (IBAMA Registration 242396).

References

  1. Albert JS (2001) Species diversity and phylogenetics systematics of American knifefish (Gymnotiformes, Teleostei). Misc Publi Mus Zool., University of Michigan 190:1–129Google Scholar
  2. Albert JS, Campos-da-Paz R (1998) Phylogenetic systematic of Gymnotiformes with diagnoses of 58 clades: a review of available data. In: Malabarba LR, Reis RR, Vari RP, Lucena ZMS, Lucena CAS (eds) Phylogeny and classification of Neotropical fishes. Edpucrs, Porto Alegre, p 419Google Scholar
  3. Almeida-Toledo LF (1978) Contribuição à citogenética de Gymnotoidei (Pisces, Osthariophysi). São Paulo. Tese (Doutorado), Instituto de Biociências—Universidade de São PauloGoogle Scholar
  4. Almeida-Toledo LF, Foresti F (2001) Morphologically differentiated sex chromosome in neotropical freshwater fish. Genetica 11:91–100CrossRefGoogle Scholar
  5. Almeida-Toledo LF, Foresti F, Toledo-Filho SA (1981) Constitutive heterochromatin and nucleolus organizer region in knifefish, Apteronotus albifrons (Pisces, Apteronotidae). Cell Mol Life Sci 37:953–954CrossRefGoogle Scholar
  6. Almeida-Toledo LF, Foresti F, Toledo-Filho SA (1985) Spontaneus triploidy and NOR activity in Eigenmannia sp. (Pisces, Sternopygidae) from the Amazon basin. Genetica 66:85–88CrossRefGoogle Scholar
  7. Almeida-Toledo LF, Daniel-Silva MFZ, Lopes CE, Toledo-Filho SA (2000) Sex chromosome evolution in fish: II. Second occurrence of an X1X2Y sex chromosome system in Gymnotiformes. Chromosome Res 8:335–340PubMedCrossRefGoogle Scholar
  8. Almeida-Toledo LF, Foresti F, Péquignot EV, Daniel-Silva MFZ (2001) XX:XY sex chromosome system with X heterochromatinization: an early stage of sex chromosome differentiation in the Neotropic electric eel Eigenmannia virescens. Cytogenet Cell Genet 95:73–78PubMedCrossRefGoogle Scholar
  9. Almeida-Toledo LF, Daniel-Silva MFZ, Moysés CB, Fonteles SBA, Lopes CE, Akama A, Foresti F (2002) Chromosome evolution in fish: sex chromosome variability in Eigenmannia virescens (Gymnotiformes, Sternopygidae). Cytogenet Genome Res 99:164–169PubMedCrossRefGoogle Scholar
  10. Alves-Gomes JA, Ortí AG, Haygood M, Heiligenberg W, Meyer A (1995) Phylogenetic analysis of the South American electric fishes (Order Gymnotiformes) and the evolution of their electrogenic system: a synthesis based on morphology, electrophysiology, and mitochondrial sequence data. Mol Biol Evol 12:298–318PubMedGoogle Scholar
  11. Andreata AA, Almeida-Toledo LF, Oliveira C, Toledo-filho SA (1993) Chromosome studies in Hypoptopomatinae (Pisces, Siluriformes, Loricariidae). II. ZZ/ZW sex-chromosome system, B chromosomes, and constitutive heterochromatin differentiation in Microlepidogaster leucofrenatus. Cytogenet Cell Genet 63:215–220PubMedCrossRefGoogle Scholar
  12. Bertollo LAC, Takashi CS, Moreira-Filho O (1978) Citotaxonomic considerations on Hoplias lacerdae (Pisces, Erythrinidae). Braz J Genet 2:103–120Google Scholar
  13. Brum MJI, Galetti PM Jr (1997) Teleostei ground plan karyotype. J Comp Biol 2:91–102Google Scholar
  14. Capriglione T, Odierna G, Caputo V, Canapa A, Olmo E (2002) Characterization of a Tc1-like transposon in the Antarctic ice-fish, Chionodraco hamatus. Gene 295:193–198PubMedCrossRefGoogle Scholar
  15. Centofante L, Bertollo LAC, Moreira-filho O (2002) A ZZ/ZW sex chromosome system in a new species of the genus Parodon (Pisces, Parodontidae). Caryologia 55:139–150Google Scholar
  16. Crampton WGR, Thorsen DH, Albert JS (2004) Steatogenys ocellatus: a new species of neotropical eletric fish (Gymnotiformes: Hypopomidae) from the lowland Amazon basin. Copeia 1:78–91CrossRefGoogle Scholar
  17. Feldberg E, Bertollo LAC, Almeida-Toledo LF, Foresti F, Moreira-Filho O, Santos AF (1987) Biological aspects of Amazonian fishes. IX. Cytogenetic studies in two species of the genus Semaprochilodus (Pisces, Prochilodontidae). Genome 29:1–4CrossRefGoogle Scholar
  18. Fernandes-Matioli FMC, Almeida-Toledo LF (2001) A molecular phylogenetic analysis in Gymnotus species (Pisces: Gymnotiformes) with inferences on chromosome evolution. Caryologia 54(1):23–30Google Scholar
  19. Fernandes-Matioli FMC, Almeida-Toledo LF, Toledo-Filho AS (1998) Natural triploidy in the neotropical specie Gymnotus carapo (Pisces: Gymnotiformes). Caryologia 51(3):319–322Google Scholar
  20. Fink SV, Fink WL (1996) Interrelationships of ostariophysan fishes (Teleostei). In: Stiassny M, Parenti L, Johnson GD (eds) Interrelationships of fishes. Academic Press, Inc, San Diego, CA, pp 209–249CrossRefGoogle Scholar
  21. Foresti F, Almeida-Toledo LF, Toledo-Filho AS (1984) Chromosome studies in Gymnotus carapo and Gymnotus sp (Pisces, Gymnotidae). Caryologia 37:141–146Google Scholar
  22. Harvey SC, Boonphakdee C, Campos-Ramos R, Ezaz MT, Griffin DK, Bromage NR, Penman DJ (2003) Analysis of repetitive DNA sequences in the sex chromosomes of Oreochromis niloticus. Cytogenet Genome Res 101:314–319PubMedCrossRefGoogle Scholar
  23. Hatanaka T, Galetti PM Jr (2004) Mapping of 18S and 5S ribosomal RNA genes in the fish Prochilodus argenteus Agassiz, 1829 (Characiformes, Prochilodontidae). Genetica 122:239–244PubMedCrossRefGoogle Scholar
  24. Hernadez-Verdun D (1991) The nucleolus today. J Cell Sci 99:465–471Google 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. Levan A, Fredga K, Sandberg AA (1964) Nomenclature for centromeric position on chromosomes. Hereditas 52:201–220CrossRefGoogle Scholar
  27. Lowrey A (1913) A study of the submental filaments considered as probable electric organs in the gymnotid eel, Steatogenys elegans (Steindachner). J Morph 24:685–694CrossRefGoogle Scholar
  28. Martins-Santos IC, Tavares MG (1996) Chromosomal analysis of Roeboides paranensis (Pisces, Characidae) from the Paraná river. Braz J Genet 19(2):271–274Google Scholar
  29. Mendes VP (2005) Análise citogenética em espécies das famílias Apteronotidae, Hypopomidae e Rhamphichthyidae (Pisces, Gymnotiformes) da Planície de Inundação do Alto Rio Paraná. Mastership Dissertation. Universidade Estadual de Maringá—Paraná, BrasilGoogle Scholar
  30. Milhomem SSR, Pieczarka JC, Crampton WGR, Souza ACP, Carvalho JR Jr, Nagamachi CY (2007) Differences in karyotype between two sympatric species of Gymnotus (Gymnotiformes: Gymnotidae) from the eastern amazon of Brazil. Zootaxa 1397:55–62Google Scholar
  31. Milhomem SSR, Pieczarka JC, Crampton WGR, Silva DS, Souza ACP, Carvalho JRC Jr, Nagamachi CY (2008) Chromosomal evidence for a putative cryptic species in the Gymnotus carapo species-complex (Gymnotiformes, Gymnotidae). BMC Genet 9:75–84PubMedCrossRefGoogle Scholar
  32. 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 46:115–125Google Scholar
  33. Nagamachi CY, Pieczarka JC, Milhomem SSR, O’Brien PCM, de Souza ACP, Ferguson-Smith MA (2010) Multiple rearrangements in cryptic species of electric knifefish, Gymnotus carapo (Gymnotidae, Gymnotiformes) revealed by chromosome painting. BMC Genet 11:28–36PubMedCrossRefGoogle Scholar
  34. Oliveira C, Chew JSK, Porto-Foresti F, Dobson MJ, Wright JM (1999) A line2 repetitive element from the cichlid fish, Oreochromis niloticus: sequence analysis and chromosomal distribution. Chromosoma 108:457–468PubMedCrossRefGoogle Scholar
  35. Pieczarka JC, Nagamachi CY, Souza ACP, Milhomem SSR, Castro RR, Nascimento AL (2006) An adaptation to DAPI-banding to fishes chromosomes. Caryologia 59(1):43–46Google Scholar
  36. Rosa R, Bellafronte E, Moreira-Filho O, Margarido VP (2006) Constituive heterochromatin, 5S and 18S rDNA genes in Apareiodon sp. (Characiformes, Parodontidae) with a ZZ/ZW sex chromosome system. Genetica 128:159–166PubMedCrossRefGoogle Scholar
  37. Schweizer D (1980) Simultaneous fluorescent staining of R bands and specific heterochromatic regions (DA/DAPI Bands) in human chromosomes. Cytogenet Cell Genet 27:190–193PubMedCrossRefGoogle Scholar
  38. Silva PC (2010) Estudos cromossômicos de peixes elétricos da família Rhamphichthydae (Pisces: Gymnotiformes). Mastership Dissertation, Universidade Federal do ParáGoogle Scholar
  39. Silva EB, Margarido VP (2005) An X1X1X2X2/X1X2Y multiple sex chromosome system in a new species of the genus Gymnotus (Pisces, Gymnotiformes). Environ Biol Fish 73:293–297CrossRefGoogle Scholar
  40. Silva DS, Milhomem SSR, Souza ACP, Pieczarka JC, Nagamachi CY (2008) A conserved karyotype of Sternopygus macrurus (Sternopygidae, Gymnotiformes) in the Amazon region: differences from other hidrographic basins suggest cryptic speciation. Micron 39:1251–1254CrossRefGoogle Scholar
  41. Silva DS, Milhomem SSR, Pieczarka JC, Nagamachi CY (2009) Cytogenetic studies in Eigenmannia virescens (Sternopygidae, Gymnotiformes) and new inferences on the origin of sex chromosomes in the Eigenmannia genus. BMC Genet 10:74–81PubMedCrossRefGoogle Scholar
  42. Sullivan JP (1997) A phylogenetic study of the Neotropical hypopomid electric fishes (Gymnotiformes: Rhamphichthyoidea). Unpublished Ph.D. Thesis, Duke UniversityGoogle Scholar
  43. Sumner AT (1972) A simple technique for demonstrating centromeric heterochromatin. Exp Cell Res 75:304–306PubMedCrossRefGoogle Scholar
  44. Venere PC, Ferrreira IA, Martins C, Galetti PM Jr (2004) ZZ/ZW sex chromosome system for the genus Leporinus (Pisces, Anostomidae, Characiformes). Genetica 121:75–80PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2011

Authors and Affiliations

  • Adauto Lima Cardoso
    • 1
    • 4
  • Julio Cesar Pieczarka
    • 1
    • 3
  • Eliana Feldberg
    • 2
    • 3
  • Susana Suely Rodrigues Milhomem
    • 1
  • Thiago Moreira-Almeida
    • 2
  • Danillo dos Santos Silva
    • 1
    • 3
  • Patrícia Corrêa da Silva
    • 1
    • 3
  • Cleusa Yoshiko Nagamachi
    • 1
    • 3
  1. 1.Laboratório de Citogenética, Instituto de Ciências BiológicasUniversidade Federal do ParáBelémBrazil
  2. 2.Laboratório de Genética AnimalInstituto Nacional de Pesquisas da AmazôniaManausBrazil
  3. 3.CNPqBrasiliaBrazil
  4. 4.IC-CNPqBrasiliaBrazil

Personalised recommendations