Phylogeography and karyotypic evolution of some <i>Deuterodon</i> species from southeastern Brazil (Characiformes, Characidae, Stethaprioninae)

Rodrigues-Oliveira, Igor Henrique; Penteado, Pierre Rafael; Pasa, Rubens; Menegídio, Fabiano Bezerra; Kavalco, Karine Frehner

doi:10.1590/1678-4685-GMB-2023-0044

Igor Henrique Rodrigues-Oliveira

conceived and the study

conducted the experiments

analyzed the data

wrote the manuscript

read and approved the final version

Universidade Federal de Viçosa, Laboratório de Genética Ecológica e Evolutiva, Rio Paranaíba, MG, Brazil.

Universidade Federal de Minas Gerais, Instituto de Ciências Biológicas, Belo Horizonte, MG, Brazil.

https://orcid.org/0000-0003-1998-7768

Pierre Rafael Penteado

conceived and the study

conducted the experiments

analyzed the data

wrote the manuscript

read and approved the final version

Universidade Federal de Viçosa, Laboratório de Genética Ecológica e Evolutiva, Rio Paranaíba, MG, Brazil.

Rubens Pasa

conceived and the study

read and approved the final version

Universidade Federal de Viçosa, Laboratório de Genética Ecológica e Evolutiva, Rio Paranaíba, MG, Brazil.

Universidade Federal de Viçosa, Laboratório de Bioinformática e Genômica, Rio Paranaíba, MG, Brazil.

https://orcid.org/0000-0002-3513-4071

Fabiano Bezerra Menegídio

conceived and the study

read and approved the final version

Universidade de Mogi das Cruzes, Centro de Pesquisas Tecnológicas, Mogi das Cruzes, SP, Brazil.

Universidade de Mogi das Cruzes, Centro Integrado de Biotecnologia, Mogi das Cruzes, SP, Brazil.

Karine Frehner Kavalco

conceived and the study

conducted the experiments

analyzed the data

read and approved the final version

Universidade Federal de Viçosa, Laboratório de Genética Ecológica e Evolutiva, Rio Paranaíba, MG, Brazil.

Universidade Federal de Viçosa, Laboratório de Bioinformática e Genômica, Rio Paranaíba, MG, Brazil.

https://orcid.org/0000-0002-4955-2792

Associate Editor:

Marcelo Guerra

Send correspondence to Karine Frehner Kavalco. Universidade Federal de Viçosa, Edifício LAE, sala 102, Rodovia MG 230, km 7, Campus Rio Paranaíba, 38810-000, Rio Paranaíba, MG, Brazil. E-mail: kavalco@ufv.br

Conflicts of Interest

The authors declare that there are no conflicts of interest related to this study

Authors Contributions

IHRO, PRP, RP, FBM and KFK conceived and the study; IHRO, PRP and KFK conducted the experiments; IHRO, PRP and KFK analyzed the data; IHRO and PRP wrote the manuscript, all authors read and approved the final version.

Figures (5)
Tables (2)

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Figure 1 -
Map demonstrating the Deuterodon populations used in the phylogeny. Diamonds indicate populations of D. ribeirae, triangles indicate populations of D. giton (asterisk symbolizing sympatry with D. intermedius) and circles indicate populations of D. hastatus (letters representing the different cytotypes). In red the Ribeira de Iguape river basin, in blue the Paraíba do Sul river basin, in green the Doce river basin and in orange the coastal drainages of the state of Rio de Janeiro.

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Figure 2 -
Karyotype of D. hastatus from the Ariró river, Angra dos Reis-RJ. Scale bar: 5 µm.

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Figure 3 -
Karyotype of D. hastatus after FISH with 18S rDNA (A) and 5S rDNA (B) probes. Scale bar: 5 μm.

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Figure 4 -
Phylogenetic tree of five populations of D. hastatus, two of D. ribeirae, two of D. giton and one of D. intermedius plus 70 sequences from 24 species outside the genus Deuterodon. Bootstrap values are demonstrated on internal nodes. The best evolutionary model, used in the analysis, was the TIM3+F+I+G4 according to ModelFinder.

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Figure 5 -
On the left, calibrated Bayesian tree, based on the ATP synthase subunit 6 gene, demonstrating the evolutionary relationships between the species of Deuterodon analyzed plus outgroups. Timescale indicated on the x-axis in millions of years. Numbers on inner nodes represent divergence estimates and blue bars represent 95% highest posterior density interval. On the right, haplotype network of the four Deuterodon species analyzed, length of branches proportional to the number of mutations, number of sequences per haplotype demonstrated within each haplotype.

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Table 1 -
Cytogenetic characteristics of nine Deuterodon species.

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Table 2 -
Bottom triangle: genetic distances between analytical populations. Upper triangle: standard deviations.

Species	Sample procedence	2n	Karyotypic formulae	FN	C-banding	Ag-NORs	GC-rich sites	18S	5S	As-51	References
D. giton ^a	Jacuí stream/SP - Paraíba do Sul river basin	50	6M+8SM+8ST+28A	72	Pericentromeric and interstitial. Many chromosomes.	6	absent	10	10	absent	Kavalco and Moreira-Filho (2003Kavalco KF and Moreira- Filho O (2003) Cytogenetical analyses in four species of the genus Astyanax (Pisces, Characidae) from Paraíba do Sul river basin. Caryologia 56:453-461.) Kavalco et al. (2004Kavalco KF, Pazza R, Bertollo LAC and Moreira-FilhoO (2004) Gene mapping of 5S rDNA sites in eight fish species from the Paraíba do Sul river basin, Brazil. Cytogenet Genome Res 106:107-110.) Kavalco et al. (2007Kavalco KF, Pazza R, Bertollo LAC and Moreira-FilhoO (2007) Satellite DNA sites in four species of the genus Astyanax (Teleostei, Characiformes). Genet Mol Biol 30:529-535.)
D. giton ^a	Latão Creek/MG Doce river basin	50	6M+8SM+24ST+12A	88	Multiple markes many chromosomes.	2	2	10	2	-	Aguiar et al. (2011Aguiar HJACD (2011) First report on spontaneous hybridization between Astyanax giton Baird & Girard 1854 and Oligosarcus argenteus Günther 1864 (Pisces: Characidae): Ecological and phylogenetic inferences. M. Sc. Thesis, Universidade Federal de Viçosa, Viçosa, 134 p.)
D. intermedius ^a	Jacuí stream/SP - Paraíba do Sul river basin	50	6M+8SM+4ST+32A	68	Pericentromeric and interstitial. Many chromosomes.	6	absent	12	10	absent	Kavalco and Moreira-Filho (2003Kavalco KF and Moreira- Filho O (2003) Cytogenetical analyses in four species of the genus Astyanax (Pisces, Characidae) from Paraíba do Sul river basin. Caryologia 56:453-461.) Kavalco et al. (2004Kavalco KF, Pazza R, Bertollo LAC and Moreira-FilhoO (2004) Gene mapping of 5S rDNA sites in eight fish species from the Paraíba do Sul river basin, Brazil. Cytogenet Genome Res 106:107-110.) Kavalco et al. (2007Kavalco KF, Pazza R, Bertollo LAC and Moreira-FilhoO (2007) Satellite DNA sites in four species of the genus Astyanax (Teleostei, Characiformes). Genet Mol Biol 30:529-535.)
D. hastatus ^a	Ypiranga Community/RJ Guapimirim-Macacu river basin	50	4M+8SM+10ST+28A (Cytotype A)	72	Pericentromeric and interstitial. Many chromosomes.	3	-	6	-	absent	Kavalco et al. (2009Kavalco KF , Brandão KdO, Pazza R and Almeida-Toledo LF (2009) Astyanax hastatus Myers, 1928 (Teleostei, Characidae): A new species complex within the genus Astyanax? Genet Mol Biol 32:477-483.)
	Santana de Japuíba County/RJ Guapimirim-Macacu river basin	50	8M+10SM+14ST+18A (Cytotype B)	82	Pericentromeric and interstitial. Many chromosomes.	3	-	8	-	absent	Kavalco et al. (2009Kavalco KF , Brandão KdO, Pazza R and Almeida-Toledo LF (2009) Astyanax hastatus Myers, 1928 (Teleostei, Characidae): A new species complex within the genus Astyanax? Genet Mol Biol 32:477-483.)
	Macacu River Guapimirim-Macacu river basin	50	6M+8SM+4ST+32A (Cytotype C)	68	Pericentromeric and interstitial. Many chromosomes.	2	-	6	-	absent	Kavalco et al. (2009Kavalco KF , Brandão KdO, Pazza R and Almeida-Toledo LF (2009) Astyanax hastatus Myers, 1928 (Teleostei, Characidae): A new species complex within the genus Astyanax? Genet Mol Biol 32:477-483.)
	Town of Chachoeiras de Macacu/RJ Guapimirim-Macacu river basin	50	6M+8SM+4ST+32A (Cytotype C)	68	Pericentromeric and interstitial. Many chromosomes.	2	-	6	-	absent	Kavalco et al. (2009Kavalco KF , Brandão KdO, Pazza R and Almeida-Toledo LF (2009) Astyanax hastatus Myers, 1928 (Teleostei, Characidae): A new species complex within the genus Astyanax? Genet Mol Biol 32:477-483.)
	Angra dos Reis/RJ Ariró river basin	50	6M+8SM+8ST+28A (Cytotype D)	72	-	-	-	6	7	-	present work
D. ribeirae ^a	Poço Grande Community, Iporanga City/SP Ribeira de Iguape river basin	50	4M+10SM+6ST+30A	70	Pericentromeric. Some chromosomes.	2	-	4	6	absent	Kavalco et al. (2010Kavalco KF , Pazza R and de Almeida-Toledo LF (2010) Molecular cytogenetics of Astyanax ribeirae (Teleostei, Characidae), an endemic characin of the Atlantic rainforest. Nucleus (India) 53:51-54.)
	Town of Registro/SP Ribeira de Iguape river basin	50	4M+10SM+6ST+30A	70	Pericentromeric. Some chromosomes.	2	-	4	6	absent	Kavalco et al. (2010Kavalco KF , Pazza R and de Almeida-Toledo LF (2010) Molecular cytogenetics of Astyanax ribeirae (Teleostei, Characidae), an endemic characin of the Atlantic rainforest. Nucleus (India) 53:51-54.)
	Town of Sete Barras/SP Ribeira de Iguape river basin	50	4M+10SM+6ST+30A	70	Pericentromeric. Some chromosomes.	-	6	4	6	absent	Kavalco et al. (2010Kavalco KF , Pazza R and de Almeida-Toledo LF (2010) Molecular cytogenetics of Astyanax ribeirae (Teleostei, Characidae), an endemic characin of the Atlantic rainforest. Nucleus (India) 53:51-54.)
D. taeniatus ^a	Hydroelectric Risoleta Neves Reservoir/MG Doce river basin	50	14M+12SM+16ST+8A	92	Centromeric and pericentromeric. Most SM and ST.	4-8	-	10	8	-	Da Cunha et al. (2016Cunha MS, Reis VJC and Dergam JA (2016) Closely related syntopic cytotypes of Astyanax taeniatus (Jenyns, 1842) from the upper Piranga River, upper Doce Basin in southeastern Brazil. Zebrafish 13:112-117.)
D. taeniatus ^a		50	10M+14SM+18ST+8A	92	Centromeric and pericentromeric. Most SM and ST.	4-8	-	8	8	-	Da Cunha et al. (2016Cunha MS, Reis VJC and Dergam JA (2016) Closely related syntopic cytotypes of Astyanax taeniatus (Jenyns, 1842) from the upper Piranga River, upper Doce Basin in southeastern Brazil. Zebrafish 13:112-117.)
D. pedri	Sant’Anna dos Ferros/MG Santo Antônio river basin	50	12M+12SM+20ST+6A	94	Centromeric many chromosomes. Instersticial some chromosomes.	2-4	-	10	2	-	Coutinho-Sanches and Dergam (2015Coutinho-Sanches N and Dergam JA (2015) Cytogenetic and molecular data suggest Deuterodon pedri Eigenmann, 1907 (Teleostei: Characidae) is a member of an ancient coastal group. Zebrafish 12:357-365.)
D. iguape ^b	Ipiranga River/SP Ribeira do Iguape river basin	50	14M/SM+36ST/A	-	-	-	-	-	-	-	Portela et al. (1988)
D. stigmaturus	Maquiné River/RS Tramandaí river basin	50	8M+6SM+2ST+34A	66	Pericentromeric. All chromossomes.	4-7	Many A short arms.	8	-	-	Mendes et al. (2011)
D. janeiroensis ^a	Açungui River/PR Ribeira do Igapé river basin	50	6M+14SM+14SM+16A	84	Centromeric and telomeric. Most chromosomes	3-7	16	22	2	14	Carvalho et al. (2002Carvalho ML, Oliveira C and Foresti F (2002) Cytogenetic analysis of five species of the subfamily Tetragonopterinae (Teleostei, Characiformes, Characidae). Caryologia 55:181-188.) Vicari et al. (2008Vicari MR, Artoni RF, MoreiraFilhoO and Bertollo LAC (2008a) Colocalization of repetitive DNAs and silencing of major rRNA genes. A case report of the fish Astyanax janeiroensis. Cytogenet Genome Res 122:67-72.)
D. janeiroensis ^a	Sacovão River/PR Ribeira do Igapé river basin	50	6M+14SM+14SM+16A	84	Centromeric and telomeric. Most chromosomes	3-7	16	22	2	14	Vicari et al. (2008Vicari MR , Noleto RB, Artoni RF , Moreira-FilhoO and Bertollo LAC (2008b) Comparative cytogenetics among species of the Astyanax scabripinnis complex: Evolutionary and biogeographical inferences. Genet Mol Biol 31:173-179.)

	1.	2.	3.	4.	5.	6.	7.	8.	9.	10.
1. D. giton - Paraíba do Sul river (Cunha, SP)		0.00584	0.01007	0.01137	0.01135	0.00588	0.01133	0.00364	0.01089	0.01214
2. D. giton - Doce river (Latão Creek, MG)	0.02511		0.01071	0.01091	0.01088	0.00611	0.01084	0.00514	0.01035	0.01195
3. D. hastatus - Ariró river (Angra dos Reis, RJ)	0.08014	0.06560		0.00766	0.00750	0.01135	0.00756	0.01075	0.00750	0.00916
4. D. hastatus - Guapimirim river (Cachoeiras de Macacu, RJ)	0.07721	0.06215	0.03773		0.00125	0.01259	0.00111	0.01187	0.00290	0.00786
5. D. hastatus - Guapimirim river (rio Macacu, RJ)	0.07684	0.06177	0.03584	0.00218		0.01251	0.00111	0.01185	0.00257	0.00802
6. D. hastatus - Guapimirim river (Santana de Japuiba, RJ)	0.02109	0.02298	0.07916	0.07382	0.07345		0.01246	0.00503	0.01196	0.01241
7. D. hastatus - Guapimirim river (Ypiranga, RJ)	0.07596	0.06089	0.03672	0.00201	0.00113	0.07257		0.01176	0.00273	0.00780
8. D. intermedius - Paraíba do Sul river (Cunha, SP)	0.01381	0.01820	0.07627	0.07282	0.07244	0.01281	0.07156		0.01137	0.01205
9. D. ribeirae - Ribeira de Iguape river (Iporanga, SP)	0.07345	0.05838	0.03547	0.00603	0.00414	0.07006	0.00502	0.06905		0.00799
10. D. ribeirae - Ribeira de Iguape river (Registro, SP)	0.08475	0.06968	0.04488	0.04746	0.04557	0.07947	0.04645	0.08035	0.04143

[1] Associate Editor:

Marcelo Guerra

Brasil

Brasil

Phylogeography and karyotypic evolution of some Deuterodon species from southeastern Brazil (Characiformes, Characidae, Stethaprioninae)

Abstract