Abstract
Potamotrygonidae is a representative family of South American freshwater elasmobranchs. Cytogenetic studies were performed in a Potamotrygon species from the middle Negro River, Amazonas, Brazil, here named as Potamotrygon sp. C. Mitotic and meiotic chromosomes were analyzed using conventional staining techniques, C-banding, and detection of the nucleolus organizing regions (NOR) with Silver nitrate (Ag-NOR). The diploid number was distinct between sexes, with males having 2n = 67 chromosomes, karyotype formula 19m + 8sm + 10st + 30a, and fundamental number (FN) = 104, and females having 2n = 68 chromosomes, karyotype formula 20m + 8sm + 10st + 30a, and FN = 106. A large chromosome, corresponding to pair number two in the female karyotype, was missing in the male complement. Male meiotic cells had 33 bivalents plus a large univalent chromosome in metaphase I, and n = 33 and n = 34 chromosomes in metaphase II. These characteristics are consistent with a sex chromosome system of the XX/XO type. Several Ag-NOR sites were identified in both male and female karyotypes. Positive C-banding was located only in the centromeric regions of the chromosomes. This sex chromosome system, which rarely occurs in fish, is now being described for the first time among the freshwater rays of the Amazon basin.
Similar content being viewed by others
References
Almeida-Toledo LF, Foresti F (2001) Morphologically differentiated sex chromosomes in Neotropical freshwater fish. Genetica 111:91–100
Almeida-Toledo LF, Foresti F, Daniel MFZ, Toledo-Filho SA (2000a) Sex chromosome evolution in fish: the formation of the neo-Y chromosome in Eigenmannia (Gymnotiformes). Chromosoma 109:197–200
Almeida-Toledo LF, Foresti F, Daniel MFZ, Lopes CE, Toledo-Filho SA (2000b) Sex chromosome evolution in fish. II. Second occurrence of an X1X2Y sex chromosome system in Gymnotiformes. Chromosome Res 8:335–340
Alves AL, Oliveira C, Nirchio M, Granado A, Foresti F (2006) Karyotypic relationships among the tribes of Hypostominae (Siluriformes: Loricariidae) with description of XO sex chromosome system in a Neotropical fish species. Genetica 128:1–9
Andreata AA, Almeida-Toledo LF, Oliveira C, Toledo Filho SA (1993) Chromosome studies in Hypoptopomatinae (Pisces, Siluriformes, Loricariidae). Cytogenet Cell Genet 63:215–220
Arai R (2011) Fish karyotypes: a check list. Springer, University of Tokyo, Japan
Araújo MLG (1998) Biologia reprodutiva e pesca de Potamotrygon sp. (Chondrichthyes-Potamotrygonidae) no médio Rio Negro, Amazonas. Master’s Thesis
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 89:15–19
Asahida T, Ida H (1995) Karyotype and cellular DNA content of a guitarfish, Rhinobatos schlegelii. La Kromosomo 2(79–80):2725–2730
Bertollo LAC, Mestriner CA (1998) The X1X2Y sex chromosome system in the fish Hoplias malabaricus. II. Meiotic analyses. Chromosome Res 6:141–147
Bertollo LAC, Takahashi CS, Moreira-Filho O (1978) Cytotaxonomic considerations on Hoplias lacerdae (Pisces, Erytrinidae). Braz J Genet 7:103–120
Bertollo LAC, Fontes MS, Fenocchio AS, Cano J (1997) The X1X2Y sex system in the fish Hoplias malabaricus. I. G-, C- and chromosome replication banding. Chromosome Res 5:493–499
Bertollo LAC, Born GG, Dergan JA, Fenocchio AS, Moreira-Filho O (2000) A biodiversity approach in the neotropical Erytrinidae fish, Hoplias malabaricus. Karyotypic survey, geographic distribution of cytotypes and cytotaxonomic considerations. Chromosome Res 8:603–613
Born GG, Bertollo LAC (2000) An XX/XY sex chromosome system in a fish species, Hoplias malabaricus, with a polymorphic NOR-bearing X chromosome. Chromosome Res 8:11–118
Carvalho MR, Lovejoy NR (2011) Morphology and phylogenetic relationships of a remarkable new genus and two new species of Neotropical freshwater stingrays from the Amazon basin (Chondrichthyes: Potamotrygonidae). Zootaxa 2776:13–48
Carvalho MR, Lovejoy NR, Rosa RS (2003) Family Potamotrygonidae (river stingrays). In: Reis RE, Kullander SO, Ferraris CJ Jr (eds) Check list of the freshwater fishes of South and Central America. EDIPUCRS, Porto Alegre, pp 22–28
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 55:139–150
Centofante L, Bertollo LAC, Buckup PA, Moreira-Filho O (2003) Chromosomal divergence and maintenance of sympatric Characidium fish species (Crenuchidae, Characidiinae). Hereditas 138:213–218
Centofante L, Bertollo LAC, Moreira-Filho O (2006) Cytogenetic characterization and description of XX/XY1Y2 sex chromosome system in catfish Harttia carvalhoi (Siluriformes, Loricariidae). Cytogenet Genome Res 112:320–324
Chen TR (1968) Karyological evidence of female heterogamety in the mosquitofish Gambusia affinis (Baird and Girard). Copeia 1968(1):70–75
Chen TR (1969) Karyological heterogamety of deep-sea fishes. Postilla 130:1–29
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
Cioffi MB, Martins C, Vicari MR, Rebordinos L, Bertollo LAC (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
Cioffi MB, Sánchez A, Marchal JA, Kosyakova N, Liehr T, Trifonov V, Bertollo LAC (2011a) Cross-species chromosome painting tracks the independent origin of multiple sex chromosomes in two cofamiliar Erythrinidae fishes. BMC Evol Biol (Online) 11:1–10
Cioffi MB, Sánchez A, Marchal JA, Kosyakova N, Liehr T, Trifonov V, Bertollo LAC (2011b) Whole chromosome painting reveals independent origin of sex chromosomes in closely related forms of a fish species. Genetica 139:1065–1072
Cruz VP, Shimabukuro-Dias CK, Oliveira C, Foresti F (2011) Karyotype description and evidence of multiple sex chromosome system X1X1X2X2/X1X2Y in Potamotrygon aff. motoro and P. falkneri (Chondrichthyes: Potamotrygonidae) in upper Paraná River basin, Brazil. Neotropical Ichthyol 9(1):201–208
da Rosa R, Bellafronte E, Moreira-Filho O, Margarido VP (2006) Constitutive heterochromatin, 5S and 18S rDNA genes in Apareiodon sp. (Characiformes, Parodontidae) with a ZZ/ZW sex chromosome system. Genetica 128:159–166
de Oliveira RR, Feldberg E, dos Anjos MB, Zuanon J (2008) Occurrence of multiple sex chromosomes (XX/XY1Y2 and Z1Z1Z2Z2/Z1Z2W1W2) in catfishes of the genus Ancistrus (Siluriformes: Loricariidae) from the Amazon basin. Genetica 134:243–249
de Oliveira RR, Feldberg E, dos Anjos MB, Zuanon J (2009) Mechanisms of chromosomal evolution and its possible relation to natural history characteristics in Ancistrus catfishes (Siluriformes: Loricariidae). J Fish Biol 75:2209–2225
Devlin RH, Nagahama Y (2002) Sex determination and sex differentiation in fish: an overview of genetic, physiological, and environmental influences. Aquaculture 208:191–364
Diniz D, Laudicina A, Bertollo LAC (2009) Chromosomal location of 18S and 5S rDNA sites in Triportheus fish species (Characiformes, Characidae). Genet Mol Biol 32:37–41
Donahue WH (1974) A karyotypic study of three species of Rajiformes (Chondrichthyes, Pisces). Can J Genet Cytol 16:203–211
Feldberg E, Bertollo LAC, Almeida-Toledo LF, Foresti F, Moreira-Filho O, Santos AF (1987) Biological aspects of Amazonian fish. IX. Cytogenetic studies in two species of the genus Semaprochilodus (Pisces, Prochilodontidae). Genome 29:1–4
Galetti PM Jr, Lima NR, Venere PC (1995) A monophyletic ZW Sex chromosome system in Leporinus (Anostomidae, Characiformes). Cytologia 60:375–382
Gross MC, Feldberg E, Cella DM, Schneider MC, Schneider CH, Porto JIR, Martins C (2009) Intriguing evidence of translocations in discus fish (Symphysodon, Cichlidae) and a report of the largest meiotic chromosomal chain observed in vertebrates. Heredity 102:435–441
Harvey SC, Masabanda J, Carrasco LAP, Bromage NR, Penman DJ, Griffin DK (2002) Molecular-cytogenetic analysis reveals sequence differences between the sex chromosomes of Oreochromis niloticus: evidence for an early stage of sex-chromosome differentiation. Cytogenet Genome Res 79:76–80
Henning F, Moysés CB, Calcagnotto D, Meyer A, Almeida-Toledo LF (2011) Independent fusions and recent origins of sex chromosomes in the evolution and diversification of glass knife fishes (Eigenmannia). Heredity 106:391–400
Hobza R, Lengerova M, Svoboda J, Kubekova H, Kejnovsky E, Vyskot B (2006) An accumulation of tandem DNA repeats on the Y chromosome in Silene latifolia during early stages of sex chromosome evolution. Chromosoma 115:376–382
Howell WM, Black DA (1979) Location of the nucleolus organizer regions on the sex chromosomes of the banded killifish, Fundulus diaphanus. Copeia 3:544–546
Howell WM, Black DA (1980) Controlled silver staining of nucleolus organizer regions with a protective colloidal developer: a 1-step method. Experientia 36:1014–1015
Kikuno T, Ojima Y (1987) A karyotypic studies of a guitar fish, Rhinobatos hyinnicephalus Richardson (Pisces, Rajiformes). La Kromosomo 2(47–48):1538–1544
Kirpichnikov VS (1981) Genetic basis of fish selection. Springer, Berlin
Levan A, Fregda K, Sandberg HA (1964) Nomenclature for centromeric position on chromosomes. Hereditas 52:201–220
Maddock MB, Schwartz FJ (1996) Elasmobranch cytogenetics: methods and sex chromosomes. Bull Mar Sci 58:147–155
Marchal JA, Acosta MJ, Bullejos M, Puerma E, Díaz de la Guardia R, Sánchez A (2006) Distribution of L1-retrotransposons on the giant sex chromosomes of Microtus cabrerae (Arvicolidae, Rodentia): functional and evolutionary implications. Chromosome Res 14:177–186
Matsubara K, Tarui H, Toriba M, Yamada K, Nishida-Umehara C (2006) Evidence for different origin of sex chromosomes in snakes, birds, and mammals and step-wise differentiation of snake sex chromosomes. Proc Natl Acad Sci 103:18190–18195
Oliveira C, Almeida-Toledo LF, Foresti F, Toledo-Filho SA (1988) Supernumerary chromosomes, Robertsonian rearrangement and multiple NOR in Corydoras aeneus (Pisces, Siluriformes, Callichthyidae). Caryologia 41:227–236
Oliveira C, Foresti F, Hilsdorf AWS (2009) Genetics of Neotropical fish: from chromosomes to populations. Fish Physiol Biochem 35:81–100
Ramos ICG (2009) Caracterização citogenética de Leptoglossus gonagra e Pachylis aff. pharaonis (Heteroptera, Cereidae). Master’s Thesis
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. Chromosome Res 5(4):221–227
Schmid M, Feichtinger W, Steinlein C, Rupprecht A, Haaf T, Kaiser H (2002) Chromosome banding in amphibia. XXIII. Giant W sex chromosomes and extremely small genomes in Eleutherodactylus euphronides and Eleutherodactylus shrevei (Anura, Leptodactylidae). Cytogenet Genome Res 97:81–94
Silva EB, Margarido VP (2005) An X1X1X2X2/X1X2Y multiple sex chromosome system in a new species of the genus Gymnotus (Pisces, Gymnotiformes). Environ Biol Fishes 73:293–297
Steinemann S, Steinemann M (2005) Y chromosomes: born to be destroyed. BioEssays 27:1076–1083
Sumner AT (1972) A simple technique for demonstrating centromeric heterochromatin. Exp Cell Res 75:304–306
Terencio ML, Schneider CH, Gross MC, Nogaroto V, Almeida MC, Artoni RF, Vicari MR, Feldberg E (2013) Repetitive sequences associated with differentiation of W chromosome in Semaprochilodus taeniurus. Genetica 140(10–12):505–512
Toffoli D, Hrbek T, Araújo MLG, Almeida MP, Charvet-Almeida P, Farias IP (2008) A test of the utility of DNA barcoding in the radiation of the freshwater stingray genus Potamotrygon (Potamotrygonidae, Myliobatiformes). Genet Mol Biol 31(1 suppl):324–336
Valentim FCS, Falcão JN, Porto JIR, Feldberg E (2006) Chromosomes of three freshwater stingrays (Rajiformes, Potamotrygonidae) from the Rio Negro Basin, Amazon, Brazil. Genetica 128:33–39
Vicari MR, Artoni RF, Moreira-Filho O, Bertollo LAC (2008) Diversification of a ZZ/ZW sex chromosome system in Characidium fish (Crenuchidae, Characiformes). Genetica 134:311–317
Vicente VE, Bertollo LAC, Valentini SR, Moreira-Filho O (2003) Origin and differentiation of sex chromosome system in Parodon hilarii (Pisces, Parodontidae). Satellite DNA, G and C-banding. Genetica 119:115–120
Wang X, Zhang Q, Ren J, Jiang Z, Wang C (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
Acknowledgments
This study was supported by the Instituto Nacional de Pesquisas da Amazônia (INPA), and the Fundação de Amparo à Pesquisa do Estado do Amazonas (FAPEAM—Programa Integrado de Pesquisa Científica and Tecnológica—PIPT Proc. 1749/08/T.O.N.: 299/08). FCS Valentim received a study grant from FAPEAM through the graduate program in Genetics, Conservation and Evolutionary Biology (GCBEv/INPA).
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
de Souza Valentim, F.C., Porto, J.I.R., Bertollo, L.A.C. et al. XX/XO, a rare sex chromosome system in Potamotrygon freshwater stingray from the Amazon Basin, Brazil. Genetica 141, 381–387 (2013). https://doi.org/10.1007/s10709-013-9737-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10709-013-9737-2