Occurrence of euchromatic B chromosomes in natural populations of <i>Moenkhausia bonita</i> and <i>M. forestii</i> (Pisces: Characidae)

Ranucci, Leandro; Fernandes, Carlos A.; Borin-Carvalho, Luciana A.; Martins-Santos, Isabel C.; Portela-Castro, Ana L. B. de

doi:10.1590/1982-0224-2021-0056

Leandro Ranucci

Departamento de Biotecnologia, Genética e Biologia Celular, Centro de Ciências Biológicas, Universidade Estadual de Maringá (UEM), Av. Colombo, 5790, 87020-900 Maringá, PR, Brazil. (LR) leandroranucci@gmail.com (corresponding author), (CAF) fxande@gmail.com; (LABC) labcarvalho@uem.br, (ICMS) icmdsantos@hotmail.com, (ALBPC) albpcastro@uem.br.

http://orcid.org/0000-0001-5169-6667

Carlos A. Fernandes

Departamento de Biotecnologia, Genética e Biologia Celular, Centro de Ciências Biológicas, Universidade Estadual de Maringá (UEM), Av. Colombo, 5790, 87020-900 Maringá, PR, Brazil. (LR) leandroranucci@gmail.com (corresponding author), (CAF) fxande@gmail.com; (LABC) labcarvalho@uem.br, (ICMS) icmdsantos@hotmail.com, (ALBPC) albpcastro@uem.br.

Núcleo de Pesquisas em Limnologia, Ictiologia e Aquicultura (NUPELIA), Universidade Estadual de Maringá (UEM), Av. Colombo, 5790, 87020-900, Maringá, PR, Brazil.

http://orcid.org/0000-0002-9905-1507

Luciana A. Borin-Carvalho

Departamento de Biotecnologia, Genética e Biologia Celular, Centro de Ciências Biológicas, Universidade Estadual de Maringá (UEM), Av. Colombo, 5790, 87020-900 Maringá, PR, Brazil. (LR) leandroranucci@gmail.com (corresponding author), (CAF) fxande@gmail.com; (LABC) labcarvalho@uem.br, (ICMS) icmdsantos@hotmail.com, (ALBPC) albpcastro@uem.br.

http://orcid.org/0000-0003-1990-4803

Isabel C. Martins-Santos

Departamento de Biotecnologia, Genética e Biologia Celular, Centro de Ciências Biológicas, Universidade Estadual de Maringá (UEM), Av. Colombo, 5790, 87020-900 Maringá, PR, Brazil. (LR) leandroranucci@gmail.com (corresponding author), (CAF) fxande@gmail.com; (LABC) labcarvalho@uem.br, (ICMS) icmdsantos@hotmail.com, (ALBPC) albpcastro@uem.br.

http://orcid.org/0000-0003-4814-5607

Ana L. B. de Portela-Castro

Departamento de Biotecnologia, Genética e Biologia Celular, Centro de Ciências Biológicas, Universidade Estadual de Maringá (UEM), Av. Colombo, 5790, 87020-900 Maringá, PR, Brazil. (LR) leandroranucci@gmail.com (corresponding author), (CAF) fxande@gmail.com; (LABC) labcarvalho@uem.br, (ICMS) icmdsantos@hotmail.com, (ALBPC) albpcastro@uem.br.

Núcleo de Pesquisas em Limnologia, Ictiologia e Aquicultura (NUPELIA), Universidade Estadual de Maringá (UEM), Av. Colombo, 5790, 87020-900, Maringá, PR, Brazil.

http://orcid.org/0000-0002-0881-0345

Edited by

Claudio Oliveira

Correspondence

Leandro Ranucci leandroranucci@gmail.com

AUTHORS’ CONTRIBUTION

Leandro Ranucci: Conceptualization, Data curation, Formal analysis, Investigation, Methodology, Project administration, Resources, Software, Visualization, Writing-original draft, Writing-review and editing. Carlos Alexandre Fernandes: Conceptualization, Data curation, Supervision, Writing-review and editing. Luciana Andréia Borin-Carvalho: Methodology, Project administration, Supervision, Visualization, Writing-review and editing. Isabel Cristina Martins-Santos: Conceptualization, Formal analysis, Methodology, Project administration, Supervision, Validation, Visualization. Ana Luiza de Brito Portela-Castro: Conceptualization, Data curation, Investigation, Methodology, Project administration, Resources, Supervision, Validation, Writing-original draft, Writing-review and editing.

COMPETING INTERESTS

The authors declare no competing interests.

ETHICAL STATEMENTS

This study was carried out in strict accordance with the recommendations of the Guide for the Care and Use of Laboratory Animals, approved by the Committee on Ethics of Animal Experiments of the Universidade Estadual de Maringá (License number: protocol 4607140416 - CEUA/UEM). Animals were captured with the permission of the Instituto Chico Mendes de Conservação da Biodiversidade (ICMBio; license number 58187-2).

Figures (2)
Tables (2)

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FIGURE 1
| Karyotypes A and D Moenkhausia bonita from the Índios River, B and E M. bonita from the Paraná River, C and F M. forestii from the Paraná River. Karyotypes A, B, and C stained with Giemsa, D, E, and F C-banded. In evidence the AgNOR-bearing chromosomes (box) and B chromosomes. Scales bar = 10 µm.

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FIGURE 2
| Karyotypes A. Moenkhausia bonita from the Índios River, B. M. bonita from the Paraná River, and C. M. forestii from the Paraná River after double-FISH with 18S rDNA (green) and 5S rDNA (red) probes. In evidence B chromosomes (B, C). Scales bar = 10 µm.

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TABLE 1
| Review of cytogenetic data in Moenkhausia. Abbreviations: m = metacentric; sb = submetacentric; st = subtelocentric; a = acrocentric; FN = fundamental number; cyt = cytotype; B = B chromosome; 5S = 5S rDNA, 18S = 18S rDNA; NOR = AgNOR; Ref = reference; BC = C band; H = heterochromatin; E = euchromatin; P = partially heterochromoatic; * = technique not performed. AM = Amazonas; MG = Minas Gerais; SP = São Paulo; MT = Mato Grosso; MS = Mato Grosso do Sul; PR = Paraná. 1- Portela-Castro et al. (1988Portela ALB, Galetti PM Júnior, Bertollo LAC. Considerations on the chromosome evolution of Tetragonopterinae (Pisces, Characidae). Rev Bras Gen. 1988; 11:307-16.); 2- Dantas et al. (2007Dantas ESO, Vicari MR, Souza IL, Moreira-Filho O, Bertollo LAC, Artoni RF. Cytotaxonomy and karyotype evolution in Moenkhausia Eigenmann, 1903 (Teleostei, Characidae). The Nucleus. 2007; 50(3):505-38.); 3- Foresti et al. (1989Foresti F, Almeida-Toledo LF, Toledo-Filho AS. Supernumerary chromosome, C-banding pattern characterization and multiple nucleolus organizer regions in Moenkhausia sanctafilomenae (Pisces, Characidae). Genetica. 1989; 79:107-14. https://doi.org/10.1007/BF00057927
https://doi.org/10.1007/BF00057927... ); 4- Alberdi, Fenocchio (1997Alberdi AJ, Fenocchio A. Karyotypes of five Tetragonopterinae species (Pisces, Characidae) from Argentina. Cytologia. 1997; 62(2):171-76. http://doi.org/10.1508/cytologia.62.171
http://doi.org/10.1508/cytologia.62.171... ); 5- Arefjev (1990Arefjev VA. Problems of karyotypic in the family Characidae (Pisces, Characiformes) with the description of somatic karyotypes for six species of tetras. Caryologia. 1990; 43(3-4):305-19. https://doi.org/10.1080/00087114.1990.10797009
https://doi.org/10.1080/00087114.1990.10... ); 6- Miyazawa (1997Miyazawa CS. Citogenética de caracídeos da bacia do rio Paraguai. Análises citotaxonômicas - evolutivas e considerações biogeográficas. [PhD Thesis]. São Carlos: Universidade Federal de São Carlos; 1997.); 7- Santos (1999Santos AF. Estudos citogenéticos em peixes dos gêneros Bryconops e Moenkhausia (Teleostei, Characidae, Tetragonopterinae). [Master Dissertation]. São Carlos: Universidade Federal de São Carlos/Fundação Universidade do Amazonas; 1999.); 8- Hashimoto et al. (2012Hashimoto DT, Voltolin TA, Paes ADNVA, Foresti F, Bortolozzi J, Porto-Foresti F. Cytogenetic analysis of B chromosomes in one population of the fish Moenkhausia sanctaefilomenae (Steindachner, 1907) (Teleostei, Characiformes). Comp Cytogenet. 2012; 6(2):141-51. https://doi.org/10.3897/CompCytogen.v6i2.1769
https://doi.org/10.3897/CompCytogen.v6i2... ); 9- Portela-Castro et al. (2001Portela-Castro ALB, Júlio HF Junior, Nishiyama PB. New occurrence of microchromosomes B in Moenkhausia sanctaefilomenae (Pisces, Characidae) from the Paraná River of Brazil: analysis of the synaptonemal complex. Genetica. 2000; 110:277-83. https://doi.org/10.1023/A:1012742717240
https://doi.org/10.1023/A:1012742717240... ); 10- Scudeler et al. (2015Scudeler PES, Diniz D, Wasko AP, Oliveira C, Foresti F. Whole chromosome painting of B chromosomes of the red-eye tetra Moenkhausia sanctaefilomenae (Teleostei, Characidae). Comp Cytogenet . 2015; 9(4):661-69. https://doi.org/10.3897/CompCytogen.v9i4.5460
https://doi.org/10.3897/CompCytogen.v9i4... ); 11- Utsunomia et al. (2016Utsunomia R, Silva DMZA, Ruiz-Ruano FJ, Araya-Jaime C, Pansonato-Alves JC, Scacchetti PC, Hashimoto DT, Oliveira C, Trifonov VA, Porto-Foresti F, Camacho JPM, Foresti F. Uncovering the ancestry of B chromosomes in Moenkhausia sanctaefilomenae (Teleostei, Characidae). PLoS ONE. 2016; 11(3):e0150573. https://doi.org/10.1371/journal.pone.0150573
https://doi.org/10.1371/journal.pone.015... ); 12- Present study; 13- Portela-Castro, Júlio Junior (2002Portela-Castro ALB, Júlio HF Junior. Karyotype relationships among species of subfamily Tetragonopterinae (Pisces, Characidae): citotaxonomy and evolution aspects. Cytologia. 2002; 67(3):329-36. https://doi.org/10.1508/cytologia.67.329
https://doi.org/10.1508/cytologia.67.329... ); 14- Fernandes, Alves (2017Fernandes CA, Alves DS. Occurrence of multiple euchromatic B Microchromosomes in Moenkhausia sanctaefilomenae (Pisces, Characidae) from the upper Paraná River basin, Brazil. Cytologia. 2017; 82(5):545-50. https://doi.org/10.1508/cytologia.82.547
https://doi.org/10.1508/cytologia.82.547... ); 15- Nascimento et al. (2020Nascimento CN, Troy WP, Pansonato-Alves JC, Carvalho ML, Oliveira C, Foresti F. Molecular cytogenetic analyses reveal extensive chromosomal rearrangements and novel B chromosomes in Moenkhausia (Teleostei, Characidae). Genet Mol Biol. 2020; 43(4):1-09. http://dx.doi.org/10.1590/1678-4685-GMB-2020-0027
http://dx.doi.org/10.1590/1678-4685-GMB-... ). Column 18S corresponds to the number of chromosome pairs with 18S rDNA.

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TABLE 2
| Frequency of B chromosomes in metaphases of Moenkhausia bonita 1 from Índios River (Paraná, Brazil), M. bonita 2 and M. forestii from Paraná River (Paraná, Brazil). Simbols: ♀ female; ♂ male; V unidentified sex.

TABLE 1 | Review of cytogenetic data in Moenkhausia. Abbreviations: m = metacentric; sb = submetacentric; st = subtelocentric; a = acrocentric; FN = fundamental number; cyt = cytotype; B = B chromosome; 5S = 5S rDNA, 18S = 18S rDNA; NOR = AgNOR; Ref = reference; BC = C band; H = heterochromatin; E = euchromatin; P = partially heterochromoatic; * = technique not performed. AM = Amazonas; MG = Minas Gerais; SP = São Paulo; MT = Mato Grosso; MS = Mato Grosso do Sul; PR = Paraná. 1- Portela-Castro et al. (1988Portela ALB, Galetti PM Júnior, Bertollo LAC. Considerations on the chromosome evolution of Tetragonopterinae (Pisces, Characidae). Rev Bras Gen. 1988; 11:307-16.); 2- Dantas et al. (2007Dantas ESO, Vicari MR, Souza IL, Moreira-Filho O, Bertollo LAC, Artoni RF. Cytotaxonomy and karyotype evolution in Moenkhausia Eigenmann, 1903 (Teleostei, Characidae). The Nucleus. 2007; 50(3):505-38.); 3- Foresti et al. (1989Foresti F, Almeida-Toledo LF, Toledo-Filho AS. Supernumerary chromosome, C-banding pattern characterization and multiple nucleolus organizer regions in Moenkhausia sanctafilomenae (Pisces, Characidae). Genetica. 1989; 79:107-14. https://doi.org/10.1007/BF00057927
https://doi.org/10.1007/BF00057927... ); 4- Alberdi, Fenocchio (1997Alberdi AJ, Fenocchio A. Karyotypes of five Tetragonopterinae species (Pisces, Characidae) from Argentina. Cytologia. 1997; 62(2):171-76. http://doi.org/10.1508/cytologia.62.171
http://doi.org/10.1508/cytologia.62.171... ); 5- Arefjev (1990Arefjev VA. Problems of karyotypic in the family Characidae (Pisces, Characiformes) with the description of somatic karyotypes for six species of tetras. Caryologia. 1990; 43(3-4):305-19. https://doi.org/10.1080/00087114.1990.10797009
https://doi.org/10.1080/00087114.1990.10... ); 6- Miyazawa (1997Miyazawa CS. Citogenética de caracídeos da bacia do rio Paraguai. Análises citotaxonômicas - evolutivas e considerações biogeográficas. [PhD Thesis]. São Carlos: Universidade Federal de São Carlos; 1997.); 7- Santos (1999Santos AF. Estudos citogenéticos em peixes dos gêneros Bryconops e Moenkhausia (Teleostei, Characidae, Tetragonopterinae). [Master Dissertation]. São Carlos: Universidade Federal de São Carlos/Fundação Universidade do Amazonas; 1999.); 8- Hashimoto et al. (2012Hashimoto DT, Voltolin TA, Paes ADNVA, Foresti F, Bortolozzi J, Porto-Foresti F. Cytogenetic analysis of B chromosomes in one population of the fish Moenkhausia sanctaefilomenae (Steindachner, 1907) (Teleostei, Characiformes). Comp Cytogenet. 2012; 6(2):141-51. https://doi.org/10.3897/CompCytogen.v6i2.1769
https://doi.org/10.3897/CompCytogen.v6i2... ); 9- **Portela-Castro et al. (2001Portela-Castro ALB, Júlio HF Junior, Nishiyama PB. New occurrence of microchromosomes B in Moenkhausia sanctaefilomenae (Pisces, Characidae) from the Paraná River of Brazil: analysis of the synaptonemal complex. Genetica. 2000; 110:277-83. https://doi.org/10.1023/A:1012742717240
https://doi.org/10.1023/A:1012742717240... ); 10- Scudeler et al. (2015Scudeler PES, Diniz D, Wasko AP, Oliveira C, Foresti F. Whole chromosome painting of B chromosomes of the red-eye tetra Moenkhausia sanctaefilomenae (Teleostei, Characidae). Comp Cytogenet . 2015; 9(4):661-69. https://doi.org/10.3897/CompCytogen.v9i4.5460
https://doi.org/10.3897/CompCytogen.v9i4... ); 11- Utsunomia et al. (2016Utsunomia R, Silva DMZA, Ruiz-Ruano FJ, Araya-Jaime C, Pansonato-Alves JC, Scacchetti PC, Hashimoto DT, Oliveira C, Trifonov VA, Porto-Foresti F, Camacho JPM, Foresti F. Uncovering the ancestry of B chromosomes in Moenkhausia sanctaefilomenae (Teleostei, Characidae). PLoS ONE. 2016; 11(3):e0150573. https://doi.org/10.1371/journal.pone.0150573
https://doi.org/10.1371/journal.pone.015... ); 12- Present study; 13- Portela-Castro, Júlio Junior (2002Portela-Castro ALB, Júlio HF Junior. Karyotype relationships among species of subfamily Tetragonopterinae (Pisces, Characidae): citotaxonomy and evolution aspects. Cytologia. 2002; 67(3):329-36. https://doi.org/10.1508/cytologia.67.329
https://doi.org/10.1508/cytologia.67.329... ); 14- Fernandes, Alves (2017Fernandes CA, Alves DS. Occurrence of multiple euchromatic B Microchromosomes in Moenkhausia sanctaefilomenae (Pisces, Characidae) from the upper Paraná River basin, Brazil. Cytologia. 2017; 82(5):545-50. https://doi.org/10.1508/cytologia.82.547
https://doi.org/10.1508/cytologia.82.547... ); 15- Nascimento et al. (2020**Nascimento CN, Troy WP, Pansonato-Alves JC, Carvalho ML, Oliveira C, Foresti F. Molecular cytogenetic analyses reveal extensive chromosomal rearrangements and novel B chromosomes in Moenkhausia (Teleostei, Characidae). Genet Mol Biol. 2020; 43(4):1-09. http://dx.doi.org/10.1590/1678-4685-GMB-2020-0027
http://dx.doi.org/10.1590/1678-4685-GMB-... ). Column 18S corresponds to the number of chromosome pairs with 18S rDNA.

Species	Collection site	2n	Karyotype formula	FN	AgNOR/Par	18S/Pair	5S/Pair	B/BC	Ref.
M. intermedia	Lake of Mato, Mogi Guaçu River, SP	50	50m/sm	100	6(m/sm)	*	*	0-1; *	1
M. intermedia	Paraná River, Paraná River basin, PR	50	16m+34sm	100	*	*	*	0	13
M. intermedia	Mogi Guaçu, SP	50	16m+34sm	100	2(m)	2(m)	*	0	2
M. sanctaefilomenae	Batalha River, Tietê River basin, SP	50	6m+16sm+28st	100	6(m); B	*	*	2-3; H-E.	8
M. sanctaefilomenae	Capivara River Tietê River basin, SP	50	48m/sm+2st/a	98	19(sm/m)	*	*	0-8; H-E.	3
M. sanctaefilomenae	Aquapey River (Argentina)	50	48m/sm+2st	100	*	*	*	0-3; *	4
M. sanctaefilomenae	Paraná River, Paraná River basin, PR	50	12m+36sm+2st	100	*	*	*	0-2; P.	9
M. sanctaefilomenae	Capivara stream tributary, Tietê River basin, SP	50	12m+36sm+2st	100	sm	3 pairs (m), 2 pairs (sm), 2 -B	*	0-6; H-E.	2
M. sanctaefilomenae	Araquá stream, tributaries of Tietê River, SP	50	6m+44sm	100	*	7,12,15,17(sm); 1-B	*	0-4; *	10
M. sanctaefilomenae	Olaria stream, tributaries of Tietê River, SP	50	6m+44sm	100	*	4,7,10,15(sm); 1-B	*	0-4; *	10
M. sanctaefilomenae	Mané Teixeira stream, tributaries of Tietê River, SP	50	6m+44sm	100	*	7,10,14,15,17(sm)	*	0-2*	10
M. sanctaefilomenae	Guaçu stream, Paraná River basin, MS	50	8m+36sm+6st	100	24(st)	*	*	0-8; P.	14
M. sanctaefilomenae	Batalha River, Tietê River basin, SP	50	6m+16sm+28st	100	6(m); B.	6(m); 1-B	1,2(m); 5,7(sm)	0-6; H-E.	11
M. sanctaefilomenae	Novo River, Paranapanema River basin, SP	50	6m+16sm+28st	100	6(m).	6(m)	1,2(m); 5,6,7 (sm); 17,18(st)	0	11
M. costae	São Francisco River, MG	50	50m/sm	100	6(m/sm)	*	*	0	1
M. pittieri	not registered	49	4m+39sm/st+6a	92	*	*	*	0	5
M. pittieri	not registered	50	4m+40sm/st+6a	94	*	*	*	0	5
M. dichroura	Cuiabá River, MT	50	32m+14sm+4st	100	*	*	*	0	6
M. gracilima (cyt a)	Amazonas River, AM	50	14m+26sm+6st+4a	96	*	*	*	0	7
M. gracilima (cyt b)	Amazonas River, AM	48	4m+24sm+12st+8a	88	*	*	*	0	7
Moenkhausia sp.	Taquaral stream, Barra do Garças region, MT	50	16m+34sm	100	sm	sm	*	0	2
M. bonita	Índios River, Paraná River basin, PR	50	14m+24sm+8st+4a	96	3(m)	3(m).	8,14(sm); 20,22(st)	0-1; E.	12
M. bonita	Paraná River, Paraná River basin, PR	50	14m+24sm+8st+4a	96	3(m)	3(m)	9(sm); 23 (st)	0-2; E.	12
M. forestii	Paraná River, Paraná River basin, PR	50	10m+28sm+10st+2a	98	3(m)	3(m)	1(m)	0-2; E.	12
M. forestii	Sapo stream, Tangará da Serra, MT	50	10m+32sm+8st	100	22(st)	22(st)	1,2(m);6,8,10 (sm)	0-3; H-E-P	15
M. oligolepis	Corredeira stream, Denise, MT	50	12m+32sm+6st	100	23(st)	23(st)	17 chromosomes	0-4; H-E-P	15
M. oligolepis	Sangue River, Campo Novo do Parecis, MT	50	12m+32sm+6st	100	22(sm)	22(sm)	4 chromosomes	0-3, H-E-P	15
M. oligolepis	Nameless stream, Xapuri, AC	50	10m+26sm+14st	100	17(sm)	7 chromosomes	21 chromosomes	0-2; P	15
M. cosmops	Verde River, Campo Novo do Parecis, MT	50	14m+30sm+6st	100	19(sm)	19(sm)	1,2(m)	0	15
M. nigromaginata	Verde River, Campo Novo do Parecis, MT	50	14m+32sm+4a	96	16(sm)	16(sm)	19(sm);24,25(a)	0	15
M. nigromarginata	Membeca River, Campo Novo do Parecis, MT	50	14m+32sm+4a	96	16(sm)	16(sm)	24,25(a)	0	15
Moenkhausia sp.	Membeca River, Campo Novo do Parecis, MT	50	10m+32sm+8st	100	22(sm)	22sm	1(m);6(sm)	0	15

*Individuals M. bonita* 1**	Number of B chromosomes			Total metaphases	*Individuals M. bonita* 2**	Number of B chromosomes			Total metaphases	Individuals M. forestii	Number of B chromosomes			Total metaphases
Sex	0	1	2		Sex	0	1	2		Sex	0	1	2	Total metaphases
1 ♂	1	1	0	2	1 ♂	6	0	0	6	1 V	1	3	0	4
2 V	5	2	0	7	2 ♀	3	2	0	5	2 ♀	4	6	0	10
3 ♂	0	1	0	1	3 ♀	174	4	0	178	3 V	2	4	0	6
4 V	8	4	0	12	4 ♂	42	81	7	130	4 ♀	11	3	0	14
5 V	5	14	7	26	5 ♀	7	31	5	43	5 V	5	5	0	10
6 ♂	6	13	0	19	6 ♀	2	20	2	24	6 ♀	46	4	0	50
7 V	4	11	1	16	7 ♀	0	5	9	14	7 V	8	21	2	31
8 ♀	10	26	0	36	8 ♂	2	5	0	7	8 V	46	10	1	57
9 V	1	1	0	2	9 ♂	1	3	6	10	9 V	3	0	0	3
10 V	0	1	0	1	10 ♀	0	2	0	2	10 V	1	2	0	3
11 V	3	0	0	3	11 ♀	8	5	0	13	11 V	12	18	1	31
12 V	0	1	0	1
Total	43	75	8	126	Total	245	158	29	432	Total	139	76	4	219
%	34.13	59.52	6.35		%	56.71	36.58	6.71		%	63.47	34.70	1.83

[1] Edited by

Claudio Oliveira

Brasil

Brasil

Occurrence of euchromatic B chromosomes in natural populations of Moenkhausia bonita and M. forestii (Pisces: Characidae)

ABSTRACT