Skip to main content
SpringerLink
Log in

Cytogenetic Analysis of Two Species of Brachyhypopomus (Hypopomidae): New Inferences about Karyotypic Diversification of Grass Knifefish

  • Published:
Journal of Ichthyology Aims and scope Submit manuscript

Abstract

Among the bluntnose knifefish of the Hypopomidae family, Brachyhypopomus is the most specious genus, with 28 species widespread in hydrographic watersheds of South America. It is considered a monophyletic clade; however, some groups remain species complex and require taxonomic revision. In this study, Brachyhypopomus cf. draco and Brachyhypopomus gauderio were analyzed through cytogenetics to identify species-specific markers and propose evolutionary trends of the genus. Brachyhypopomus cf. draco had 2n = 26 (2m + 24a) and 18S terminal rDNA sites on pair 23. Brachyhypopomus gauderio exhibited a multiple sex chromosomes system, females had 2n = 42 (X1X1X2X2) and males had 2n = 41 (X1X2Y), both revealing a multiple nucleolus organizer regions system. The two species presented a similar heterochromatic pattern: pericentromeric, interstitial, and terminal blocks coincident with the nucleolus organizer regions. ChromEvol software evidenced 2n = 44 as a plesiomorphic characteristic of Brachyhypopomus. The karyotype evolution of this group is a dynamic process based on Robertsonian translocations, pericentric inversions, and intense reorganization of the heterochromatic elements.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1.
Fig. 2.
Fig. 3.
Fig. 4.
Fig. 5.

Similar content being viewed by others

REFERENCES

  1. Albert, J.S. and Crampton, W.G.R., Family Hypopomidae (bluntnose knifefishes), Checklist of the Freshwater Fishes of South and Central America, Reis, R.E., Eds., Porto Alegre: Edipucrs, 2003, pp. 494−496.

    Google Scholar 

  2. Almeida-Toledo, L.F., Foresti, F., and Toledo-Filho, S.A., Constitutive heterochromatin and nucleolus organizer region in knifefish, Apteronotus albifrons (Pisces, Apteronotidae), Cell. Mol. Life Sci., 1981, vol. 37, pp. 953−954. https://doi.org/10.1007/BF01971773

    Article  Google Scholar 

  3. Almeida-Toledo, L.F., Daniel-Silva, M.F., Lopes, C.E., et al., Sex chromosome evolution in fish. II. Second occurrence of an X1X2Y sex chromosome system in Gymnotiformes, Chrom. Res., 2000, vol. 8, no. 4, pp. 335−340. https://doi.org/10.1023/a:1009287630301

    Article  Google Scholar 

  4. Baumgärtner, L., Paiz, L.M., Takagui, F.H., et al., Comparative cytogenetics analysis on five genera of thorny catfish (Siluriformes, Doradidae): chromosome review in the family and inferences about chromosomal evolution integrated with phylogenetics proposals, Zebrafish, 2018, vol. 15, no. 3, pp. 270−278. https://doi.org/10.1089/zeb.2017.1554

    Article  PubMed  Google Scholar 

  5. Bertollo, L.A.C., Takahashi, C.S., and Moreira-Filho, O., Cytotaxonomic considerations on Hoplias lacerdae (Pisces, Erythrinidae), Rev. Brasil. Genet., 1978, vol. 1, pp.103−120.

    Google Scholar 

  6. Bitencourt, J.A., Affonso, P.R.A.M., Giuliano-Caetano, L., et al., Identification of distinct evolutionary units in allopatric populations of Hypostomus cf. wuchereri Günther, 1864 (Siluriformes: Loricariidae): karyotypic evidence, Neotrop. Ichthyol., 2011, vol. 9, no. 2, pp. 317−324. https://doi.org/10.1590/S1679?62252011000200008

    Article  Google Scholar 

  7. Cardoso, A.L., Pieczarka, J.C., Feldberg, E., et al., Chromosomal characterization of two species of the genus Steatogenys (Gymnotiformes: Rhamphichthyoidea: Steatogenini) from Amazon basin: sex chromosomes and correlations with Gymnotiformes phylogeny, Rev. Fish Biol. Fisher., 2011, vol. 21, pp. 613−621. https://doi.org/10.1007/s11160?010?9196?0

    Article  Google Scholar 

  8. Cardoso, A.L., Pieczarka, J.C., and Nagamachi, C.Y., X1X1X2X2/X1X2Y sex chromosome system in the Neotropical Gymnotiformes electric fish of the genus Brachyhypopomus, Genet. Mol. Biol., 2015, vol. 38, no. 2, pp. 213−219. https://doi.org/10.1590/S1415?4757382220140189

    Article  PubMed  PubMed Central  Google Scholar 

  9. Cardoso, A.L., Pieczarka, J.C., Crampton, W.G.R., et al., Karyotypic diversity and evolution in a sympatric assemblage of neotropical electric knifefish, Front. Genet., 2018, vol. 9, no. 81, pp. 1−12. https://doi.org/10.3389/fgene.2018.00081

    Article  CAS  Google Scholar 

  10. Carvalho, R.A. and Dias A.L., Interindividual size heteromorphism of NOR and chromosomal location of 5S rRNA genes in Iheringichthys labrosus, Braz. Arch. Biol. Technol., 2007, vol. 50, no. 1, pp.141−146. https://doi.org/10.1590/S1516?89132007000100017

    Article  Google Scholar 

  11. Costa, W.J.E.M. and Campos-da-Paz, R., Description d’une nouvelle espèce de poisson électrique du genre néotropical Hypopomus (Siluriformes: Gymnotoidei: Hypopomidae) du Sud-Est du Brésil, Revue Franç. d’Aquariol, Herpétol., 1992, vol. 18, no. 4, pp. 117−120.

    Google Scholar 

  12. Crampton, W.G.R., Gymnotiform fish: an important component of Amazonian floodplain fish communities, J. Fish. Biol., 1996, vol. 48, pp. 298−301.

    Google Scholar 

  13. Crampton, W.G.R., Chapman, J.L., and Bell, J., Interspecific variation in gill size is correlated to ambient dissolved oxygen in the Amazonian electric fish Brachyhypopomus (Gymnotiformes: Hypopomidae), Environ. Biol. Fish., 2007, vol. 83, no. 2, pp. 223−235. https://doi.org/10.1007/s10641?007?9325?3

    Article  Google Scholar 

  14. Crampton, W.G.R., Santana, C.D., Waddell, J.C., et al., Phylogenetic systematics, biogeography, and ecology of the electric fish genus Brachyhypopomus (Ostariophysi: Gymnotiformes), PLoSOne, 2016, vol. 11, Article 10, pp. 1−66. https://doi.org/10.1371/journal.pone.0161680

  15. Crampton, W.G.R., Santana, C.D., Waddell, J.C., et al., A taxonomic revision of the Neotropical electric fish genus Brachyhypopomus (Ostariophysi: Gymnotiformes: Hypopomidae), with descriptions of 15 new species, Neotrop. Ichthyol., 2017, vol. 14, no. 4, pp. 1−152. https://doi.org/10.1590/1982?0224?20150146

    Article  Google Scholar 

  16. Fernández-Yépez, A., Analisis ictiológico del complejo hidrográfico (04) Río Yaracuy Caracas, Dirección de Obras Hidraulicas: Ministerio de Obras Públicas, República de Venezuela, 1972, pp. 1−25.

  17. Fernandes, C.A., Paiz, L.M., Baumgartner, L., et al., Comparative cytogenetics of the black ghost knifefish (Gymnotiformes: Apteronotidae): evidence of chromosomal fusion and pericentric inversions in karyotypes of two Apteronotus species, Zebrafish, 2017, vol. 14, no. 5, pp. 471−476. https://doi.org/10.1089/zeb.2017.1432

    Article  CAS  PubMed  Google Scholar 

  18. Ferreira, D.C., Porto-Foresti, F., Oliveira, C., et al., Transposable elements as a potential source for understanding the fish genome, Mob. Genet. Elements, 2011, vol. 1, no. 2, pp. 112−117. https://doi.org/10.4161/mge.1.2.16731

    Article  PubMed  PubMed Central  Google Scholar 

  19. Ferreira, M., Garcia, C., Matoso, D.A., et al., The Bunocephalus coracoideus species complex (Siluriformes, Aspredinidae). Signs of a speciation process through chromosomal, genetic and ecological diversity, Front. Genet., 2017, vol. 8, Article 120, pp. 1−12. https://doi.org/10.3389/fgene.2017.00120

  20. Fonteles, S.B., Lopes, A.C.E., Akama, A., et al., Cytogenetic characterization of the strongly electric Amazonian eel, Electrophorus electricus (Teleostei, Gymnotiformes), from the Brazilian rivers Amazon and Araguaia, Gen. Mol. Biol., 2008, vol. 31, pp. 227−230. https://doi.org/10.1590/S1415?47572008000200010

    Article  CAS  Google Scholar 

  21. Fricke, R. and Eschmeyer, W.N., Guide to fish collections, http://researcharchive.calacademy.org/research/ichthyology/catalog/collections.asp, Cited March, 2022.

  22. Giora, J. and Malabarba, L.R., Brachyhypopomus gauderio, new species, a new example of underestimated species diversity of electric fishes in the southern South America (Gymnotiformes: Hypopomidae), Zootaxa, 2009, vol. 2093, no. 1, pp. 60−68. https://doi.org/10.11646/zootaxa.2093.1.4

    Article  Google Scholar 

  23. Giora, J., Malabarba, L.R., and Crampton W., Brachyhypopomus draco, a new sexually dimorphic species of neotropical electric fish from southern South America (Gymnotiformes: Hypopomidae), Neotrop. Ichthyol., 2008, vol. 6, pp. 159−168. https://doi.org/10.1590/S1679?62252008000200002

    Article  Google Scholar 

  24. Giora, J., Tarasconi. H.M., and Fialho, C.B., Reproduction and feeding habits of the highly seasonal Brachyhypopomus bombilla (Gymnotiformes: Hypopomidae) from southern Brazil, with evidence for a dormancy period, Environ. Biol. Fish., 2012, vol. 94, pp. 649−662. https://doi.org/10.1007/s10641?011?9971?3

    Article  Google Scholar 

  25. Giuliano-Caetano, L., Polimorfismo Cromossômico Robertsoniano em populações de Rineloricaria latirostris (Pisces, Loricariidae), PhD Thesis, São Carlos: Department of Genetics and Evolution, Universidade Federal de Department of Genetics and Evolution, Universidade Federal de São Carlos, 1998.

  26. Glick, L. and Mayrose, I., ChromEvol: assessing the pattern of chromosome number evolution and the inference of polyploidy, Mol. Biol. Evol., 2014, vol. 31, pp. 1914−1922. https://doi.org/10.1093/molbev/msu122

    Article  CAS  PubMed  Google Scholar 

  27. Griffiths, S.P., The use clove oil as an anaesthetic and method for sampling intertidal rockpool fishes, J. Fish Biol., 2000, vol. 57, pp. 1453−1464. https://doi.org/10.1111/j.1095?8649.2000.tb02224.x

    Article  Google Scholar 

  28. Hatanaka, T. and Galetti P.M., Jr., Mapping 18S and 5S ribosomal RNA genes in the fish Prochilodus argenteus Agassiz, 1929 (Characiformes, Prochilodontidae), Genetica, 2004, vol. 122, pp. 239−244. https://doi.org/10.1007/s10709?004?2039?y

    Article  CAS  PubMed  Google Scholar 

  29. Henning, F., Moysés, C.B., Calcagnotto, D., et al., Independent fusions and recents origins of sex chromosome in the evolution and diversification of glass knifefishes (Eigenmannia), Heredity, 2010, vol. 106, pp. 391−400. https://doi.org/10.1038/hdy.2010.82

    Article  PubMed  PubMed Central  Google Scholar 

  30. Hopkins, C.D., Hypopomus pinnicaudatus (Hypopomidae), a new species of gymnotiform fish from French Guiana, Copeia, 1991, vol. 1991, no.1, pp. 151−161.

    Article  Google Scholar 

  31. Kitano, J. and Peichel, C.L., Turnover of sex chromosomes and speciation in fishes, Environ. Biol. Fishes, 2012, vol. 94, pp. 549−558. https://doi.org/10.1007/s10641?011?9853?8

    Article  PubMed  Google Scholar 

  32. Kligerman, A.D. and Bloom, S.E., Rapid chromosome preparations from solid tissues of fishes, J. Fish. Res. Board Can., 1977, vol. 34, no. 2, pp. 266−269. https://doi.org/10.1139/f77?039

    Article  Google Scholar 

  33. Kumar, S., Stecher, G., and Tamura, K., MEGA: Molecular Evolutionary Genetics Analysis Version 7.0 for bigger datasets, Mol. Biol. Evol., 2016, vol. 33, no. 7, pp. 1870−1874. https://doi.org/10.1093/molbev/msw054

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Levan, A., Fredga, K., and Sandberg, A.A., Nomenclature for centromeric position on chromosomes, Hereditas, 1964, vol. 52, pp. 201−220. https://doi.org/10.1111/j.1601?5223.1964.tb01953.x

    Article  Google Scholar 

  35. Lorscheider, C.A., Oliveira, J.I.N., Dulz, T.A., et al., Comparative cytogenetics among three sympatric Hypostomus species (Siluriformes: Loricariidae): an evolutionary analysis in a high endemic region, Braz. Arch. Biol. Technol., 2018, vol. 61, Article e18180417, pp. 1−14. https://doi.org/10.1590/1678-4324-2018180417

  36. Loureiro, M. and Silva, A., A new species of Brachyhypopomus (Gymnotiformes, Hypopomidae) from northeast Uruguay, Copeia, 2006, no. 4, pp. 667−673. https://doi.org/10.1643/0045?8511(2006)6[665:ANSOBG]-2.0.CO;2

  37. Lui, R.L., Blanco, D.R., Moreira-Filho, O., et al., Propidium iodide for making heterochromatin more evident in the C-banding technique, Biotech. Histochem., 2012, vol. 87, no. 7, pp. 433−438. https://doi.org/10.3109/10520295.2012.696700

    Article  CAS  PubMed  Google Scholar 

  38. Mayrose, I., Barker, M., and Otto, S., Probabilistic models of chromosome number evolution and the inference of polyploidy, Syst. Biol., 2010, vol. 59, no. 2, pp. 132−144. https://doi.org/10.1093/sysbio/syp083

    Article  PubMed  Google Scholar 

  39. Mendes, V.P., Portela-Castro, A.L.B., and Julio, H.F., Jr., First record of supernumerary (B) chromosomes in electric fish (Gymnotiformes) and the karyotype structure of three species of the same order from the upper Paranáriver basin, Comp. Cytogen., 2012, vol. 6, no. 1, pp. 1−16. https://doi.org/10.3897/CompCytogen.v6i1.1752

    Article  Google Scholar 

  40. Molina, W.F., Alves, D.E.O., Araújo, W.C., et al., Performance of human immunostimulating agents in the improvement of fish cytogenetic preparations, Gen. Mol. Res., 2010, vol. 9, pp. 1807–1814. https://doi.org/10.4238/vol9?3gmr840

    Article  CAS  Google Scholar 

  41. Pinkel, D., Strume T., and Gray, J.W., Cytogenetic analysis using quantitative, high−sensitivity, fluorescence hybridization, Proc. Natl. Acad. Sci. USA, 1986, vol. 83 no. 9, pp. 2934−2938. https://doi.org/10.1073/pnas.83.9.2934

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Santana, C.D., Apteronotus caudimaculosus n. sp. (Gymnotiformes: Apteronotidae), a sexually dimorphic black ghost knifefish from the Pantanal, Western Brazil, with a note on the monophyly of A. albifrons species complex, Zootaxa, 2003, vol. 252, no. 1, pp. 1−11. https://doi.org/10.11646/zootaxa.252.1.1

    Article  Google Scholar 

  43. Schultz, L.P., Two new species of fishes (Gymnotidae, Loricariidae) from Caripito, Venezuela, Zoologica: Scientific Contributions of the New York Zoological Society, 1944, vol. 29, no. 5, pp. 39−44.

    Google Scholar 

  44. da Silva, L.L., Giuliano-Caetano, L., and Dias, A.L., Karyotypic diversity in a population of Bryconamericus aff. iheringii (Characidae), Genet. Mol. Res., 2014, vol. 13, no. 1, pp. 2069−2081. https://doi.org/10.4238/2014.March.24.11

    Article  CAS  PubMed  Google Scholar 

  45. Silva, M., Matoso, D.A., Vicari, M.R., et al., Repetitive DNA and meiotic behavior of sex chromosomes in Gymnotus pantanal (Gymnotiformes, Gmynotidae), Cytogenet. Genome Res., 2011, vol. 135, no. 2, pp. 143−149. https://doi.org/10.1159/000330777

    Article  PubMed  Google Scholar 

  46. Silva, P.C., Nagamachi, C.Y., Silva, D.S., et al., Karyotypic similarities between two species of Rhamphichthys (Rhamphichthyidae, Gymnotiformes) from the Amazon basin, Comp. Cytogen., 2013, vol. 7, no. 4, pp. 279−291. https://doi.org/10.3897/compcytogen.v7i4.4366

    Article  Google Scholar 

  47. Silva, F.H.R., Pieczarka, J.C., Cardoso, A.L., et al., Chromosomal diversity in three species of electric fish (Apteronotidae, Gymnotiformes) from Amazon Basin, Genet. Mol. Biol., 2014, vol. 37, no. 4, pp. 638−645. https://doi.org/10.1590/S1415?47572014005000018

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Silva, M.D., Matoso, D.A., Margarido, V.P., et al., Composition and nature of heterochromatin in the electrical fish (knifefishes), in Cytogenetics—Classical and Molecular Strategies for Analysing Heredity Material, Larramendy, M.L. and Soloneski, S., Eds., London: IntechOpen, 2021.

    Google Scholar 

  49. Sullivan, J.P., Zuanon J., and Cox Fernandes, C., Two new species and new subgenus of toothed Brachyhypopomus electric knifefishes (Gymnotiformes, Hypopomidae) from the central Amazon and considerations pertaining to the evolution of a monophasic electric organ discharge, Zookeys, 2013, vol. 327, pp. 1−34. https://doi.org/10.3897/zookeys.327.5427

    Article  Google Scholar 

  50. Sumner, A.M.T., A simple technique for demonstrating centromeric heterochromatin, Exp. Cell. Res., 1972, vol. 75, pp. 304−306. https://doi.org/10.1016/0014?4827(72)90558?7

    Article  CAS  PubMed  Google Scholar 

  51. Takagui, F.H., Venturelli, N.B., Dias, A.L., et al., The importance of pericentric inversions in the karyotypic diversification of the species Loricariichthys anus and Loricariichthys platymetopon, Zebrafish, 2014, vol. 11, no. 4, pp. 300−305. https://doi.org/10.1089/zeb.2014.0985

    Article  PubMed  Google Scholar 

  52. Takagui, F.H., Dias, A.L., Birindelli, J.L.O., et al., First report of B chromosomes in three neotropical thorny catfishes (Siluriformes, Doradidae), Comp. Cytogen., 2017a, vol. 11, no. 1, pp. 55−64. https://doi.org/10.3897/CompCytogen.v11i1.10496

    Article  Google Scholar 

  53. Takagui, F.H., Moura, L.F., Ferreira, D.C., et al., Karyotype diversity in Doradidae (Siluriformes, Doradoidae) and presence of the heteromorphic ZZ/ZW sex chromosome system in the family, Zebrafish, 2017b, vol. 14, no. 3, pp. 236−243. https://doi.org/10.1089/zeb.2016.1368

    Article  CAS  PubMed  Google Scholar 

  54. Takagui, F.H., Rosa, R., Shibatta, O.A., et al., Chromosomal similarity between two species of Apteronotus albifrons complex (Apteronotidae−Gymnotiformes) implications in citotaxonomy and karyotypic evolution, Caryologia, 2017c, vol. 70, no. 2, pp. 147−150. https://doi.org/10.1080/00087114.2017.1306385

    Article  Google Scholar 

  55. Triques, M.L. and Khamis, D.K., Brachyhypopomus jureiae, a new species of freshwater Neotropical electric fish (Teleostei: Gymnotiformes: Hypopomidae) from a coastal stream of Southeastern Brazil, Lundiana, 2003, vol. 4, pp. 61−64.

    Google Scholar 

  56. Volff, J.N., Genome evolution and biodiversity in teleost fish, Heredity, 2005, vol. 94, pp. 280−294. https://doi.org/10.1038/sj.hdy.6800635

    Article  CAS  PubMed  Google Scholar 

Download references

ACKNOWLEDGMENTS

We also thanks the State University of Londrina (Center of Biological Sciences—General Biology Department) for providing its laboratory structure for the experiments. ICMBio (Instituto Chico Mendes de Conservação da Biodiversidade) for allowing the collection of the biological material. And Dr. Luiz R. Malabarba (UFRS—Federal University of Rio Grande do Sul) for identifying the specimens.

Funding

This research was supported by a grant from Coordenação de Aperfeiçoamento de Pessoal de Nível Superior—Brazil (CAPES)—Finance code 001.

Author information

Authors and Affiliations

  1. Laboratório de Citogenética Animal, Departamento de Biologia Geral, Universidade Estadual de Londrina, Londrina, Brazil

    F. H. Takagui, J. F. Dionisio & L. Giuliano-Caetano

  2. Laboratório Genômica Integrativa, Departamento de Biologia Estrutural e Funcional, Instituto de Biociências de Botucatu, Universidade Estadual Paulista—UNESP, Botucatu, Brazil

    A. L. Cardoso

  3. Museu de Zoologia, Departamento de Biologia Animal e Vegetal, Universidade Estadual de Londrina, Londrina, Brazil

    O. A. Shibatta

Authors
  1. F. H. Takagui
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. A. L. Cardoso
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. J. F. Dionisio
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. O. A. Shibatta
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. L. Giuliano-Caetano
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to F. H. Takagui.

Ethics declarations

Conflict of interests. The authors declare that they have no conflicts of interest.

Statement on the welfare of animals. All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Takagui, F.H., Cardoso, A.L., Dionisio, J.F. et al. Cytogenetic Analysis of Two Species of Brachyhypopomus (Hypopomidae): New Inferences about Karyotypic Diversification of Grass Knifefish. J. Ichthyol. 62, 828–839 (2022). https://doi.org/10.1134/S0032945222050198

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S0032945222050198

Keywords:

Search

Navigation