Genetic diversity of migratory fish populations of the Rio Grande Reservoir (São Paulo, Brazil)
DOI:
https://doi.org/10.5433/1679-0359.2019v40n1p503Keywords:
Brycon orbignyanus, Conservation, Genetic variability, Microsatellites, Piaractus mesopotamicus, Prochilodus lineatus.Abstract
In recent years, anthropogenic factors such as pollution, overfishing, and construction of hydroelectric plants have significantly impacted natural fish populations. Research focusing on genetically evaluation of these impacts is necessary to objectively target conservation programs. The aim of this study was to evaluate the genetic diversity of Curimba (Prochilodus lineatus), Pacu (Piaractus mesopotamicus), and Piracanjuba (Brycon orbignyanus) populations from the Água Vermelha Reservoir, Rio Grande-SP. Microsatellite loci were amplified, producing 56, 24, and 26 alleles for the populations of the three species, respectively. The number of alleles per locus ranged from three to ten for P. lineatus, two to five for P. mesopotamicus, and two to four for B. orbignyanus. The observed heterozygosity (Ho) was higher in the P. lineatus population (0.547), relative to the P. mesopotamicus and B. orbignyanus populations (0.473 and 0.527, respectively). The mean values of Ho were lower than the average expected heterozygosity (He) in the three species, being corroborated by the positive inbreeding coefficient (Fis). Deviations from the Hardy-Weinberg equilibrium (HWE) were found in five, three, and two loci for P. lineatus, P. mesopotamicus, and B. orbignyanus, respectively. Wilcoxon tests revealed recent bottlenecks in the three species, evidenced by a significant excess of heterozygotes (p < 0.05) detected only in the Infinite Allele Model (IAM). In conclusion, adequate genetic variability was observed in the three populations with the presence of heterozygous deficits.Downloads
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References
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ASHIKAGA, F. Y.; ORSI, M. L.; OLIVEIRA, C.; SENHORINI, J. A.; FORESTI, F. The endangered species Brycon orbignyanus: genetic analysis and definition of priority areas for conservation. Environmental Biology of Fishes, Dordrecht, v. 98, n. 7, p. 1845-1855, 2015.
BARBOSA, A. C.; CORREA, T. C.; GALZERANI, F.; GALETTI, P. M.; HATANAKA, T. Thirteen polymorphic microsatellite loci in the Neotropical fish Prochilodus argenteus (Characiformes, Prochilodontidae). Molecular Ecology Resources, Oxford, v. 6, n. 3, p. 936-938, 2006.
BARBOSA, A. C.; GALZERANI, F.; CORRÊA, T. C.; GALETTI JUNIOR, P. M.; HATANAKA, T. Description of novel microsatellite loci in the Neotropical fish Prochilodus argenteus and cross-amplification in P. costatus and P. lineatus. Genetics and Molecular Biology, Ribeirão Preto, v. 31, n. 1, p. 357-360, 2008.
BARROCA, T. M.; SANTOS, G. B.; DUARTE, N. V. R.; KALAPOTHAKIS, E. Evaluation of genetic diversity and population structure in a commercially important freshwater fish Prochilodus costatus (Characiformes, Prochilodontidae) using complex hypervariable repeats. Genetics and Molecular Research, Ribeirão Preto, v. 11, n. 4, p. 4456-4467, 2012.
BARROSO, R. M.; HILSDORF, A. W. S.; MOREIRA, H. L. M.; MELLO, A. M.; GUIMARÃES, S. E. F.; CABELLO, P. H.; TRAUB-CSEKO, Y. M. Identification and characterization of microsatellites loci in Brycon opalinus (Cuvier, 1819) (Characiforme, Characidae, Bryconiae). Molecular Ecology Notes, Oxford, v. 3, n. 1, p. 297-298, 2003.
BASSAM, B. J.; CAETANO-ANOLLÉS, G.; GRESSHOFF, P. M. Fast and sensitive silver staining of DNA in polyacrylamide gels. Analytical Biochemistry, Bethesda, v. 196, n. 2, p. 80-83, 1991.
CALCAGNOTTO, D.; DESALLE, R. Population genetic structuring in pacu (Piaractus mesopotamicus) across the parana-paraguay basin: evidence from microsatellites. Neotropical Ichthyology, Maringá, v. 7, n. 4, p. 607-616, 2009.
CALCAGNOTTO, D.; RUSSELLO, M.; DESALLE, R. Isolation and characterization of microsatellite loci in Piaractus mesopotamicus and their applicability in other Serrasalminae fish. Molecular Ecology Notes, Oxford, v. 1, n. 4, p. 245-247, 2001.
CARVALHO-COSTA, L. F.; HATANAKA, T.; GALETTI JUNIOR, P. M. Evidence of lack of population substructuring in the Brazilian freshwater fish Prochilodus costatus. Genetics and Molecular Biology, Ribeirão Preto, v. 31, n. 1, p. 377-380, 2008.
CASTRO, P. L.; RIBEIRO, R. P.; SANTOS, S. C. A.; GOES, E. S. D. R.; SOUZA, F. P.; POVEDA-PARRA, A. R.; VARGAS, L.; URREA-ROJAS, A. M.; LOPERA-BARRERO, N. M. Cross-amplification of heterologous microsatellite markers in Piracanjuba. Ciência Rural, Santa Maria, v. 47, n. 12, p. 1-6, 2017.
CORNUET, J. M.; LUIKART, G. Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics, Rockville, v. 144, n. 4, p. 2001-2014, 1996.
FERREIRA, D. G.; SOUZA-SHIBATTA, L.; SHIBATTA, O. A.; SOFIA, S. H.; CARLSSON, J.; DIAS, J. H. P.; MAKRAKIS, S.; MAKRAKIS, M. C. Genetic structure and diversity of migratory freshwater fish in a fragmented Neotropical river system. Reviews in Fish Biology and Fisheries, London, v. 27, n. 1, p. 209-231, 2017.
GOUDET, J. FSTAT: a program to estimate and test gene diversities and fixation indices (version 2.9.3.2). Lausanne: University of Lausanne, Department of Ecology & Evolution, 2002. Disponível em: <http://www2.unil.ch/popgen/softwares/fstat.htm>. Acesso em: 26 jan. 2018.
INSTITUTO BRASILEIRO DE GEOGRAFIA E ESTATÍSTICA - IBGE. Produção da pecuária municipal 2015. Rio de Janeiro: IBGE, 2015. 49 p.
LAROCHE, J.; DURAND, J. D. Genetic structure of fragmented populations of a threatened endemic percid of the Rhône river: Zingel asper. Heredity, London, v. 92, n. 4, p. 329-334, 2004.
LOPERA-BARRERO, N. M.; POVH, J. A.; RIBEIRO, R. P.; GOMES, P. C.; JACOMETO, C. B.; LOPES, T. S. Comparación de protocolos de extracción de ADN con muestras de aleta y larva de peces: extracción modificada con cloruro de sodio. Ciencia e Investigación Agraria, Santiago, v. 35, n. 1, p. 76-86, 2008.
LOPERA-BARRERO, N. M.; SANTOS, S. C. A.; GOES, E. S. R.; CASTRO, P. L.; SOUZA, F. P.; POVEDA-PARRA, A. R.; CASSETA, J.; PONTILLO, B. G.; RIBEIRO, R. P. Monitoring and conservation genetics of Prochilodus lineatus wild populations of Pardo, Mogi Guaçu and Tiete rivers, São Paulo. Arquivo Brasileiro de Medicina Veterinária e Zootecnia, Belo Horizonte, v. 68, n. 6, p. 1621-1628, 2016.
LOPERA-BARRERO, N. M.; SANTOS, S. C. A.; RODRIGUEZ-RODRIGUEZ, M. P.; FORNARI, D. C.; ZANCHETA, C.; POVEDA-PARRA, A. R.; OLIVEIRA, C. A. L.; RIBEIRO, R. P. Genetic diversity of wild populations and broodstocks of curimba for restocking programs in the Tietê, Grande, Pardo and Mogi-Guaçu rivers (Brazil). Boletim do Instituto de Pesca, São Paulo, v. 41, n. 2, p. 287-304, 2015.
POVH, J. A.; RIBEIRO, R. P.; SIROL, R. N.; STREIT JUNIOR, D. P.; MOREIRA, H. L. M.; SIEWERDT, F.; LOPERA-BARRERO, N. M.; MANGOLIN, C. A.; VARGAS, L. Microsatellite analysis of the parental contribution of Piaractus mesopotamicus to the production of offspring in the semi-natural system of reproduction. Brazilian Archives of Biology and Technology, Curitiba, v. 53, n. 2, p. 389-396, 2010.
RAMOS, J. V. B.; SODRÉ, L. M. K.; ORSI, M. L.; ALMEIDA, F. S. Genetic diversity of the species Leporinus elongatus (Teleostei: Characiformes) in the Canoas Complex - Paranapanema River. Neotropical Ichthyology, Maringá, v. 10, n. 4, p. 821-828, 2012.
REVALDAVES, E.; RENESTO, E.; GOLD, J. R. Genetic variation of Prochilodus lineatus (Valenciennes, 1836) from Paraná, Baía, Miranda, and Corumbá rivers, Brazil. Genetics and Molecular Research, Ribeirão Preto, v. 15, n. 4, p. 1-11, 2016.
RIBEIRO, R. P.; LOPERA-BARRERO, N. M.; POVH, J. A.; RODRIGUEZ-RODRIGUEZ, M. P.; FORNARI, D. C.; BAUMGARTNER, G.; BAUMGARTNER, D.; SOUZA, F. P.; CASTRO, P. L.; POVEDA-PARRA, A. R. Genetic diversity of Salminus brasiliensis wild populations in downstream and upstream Cachoeira Branca, Verde River MS Brazil: a preliminary view. Semina: Ciências Agrárias, Londrina, v. 37, n. 1, p. 507-516, 2016.
RIBEIRO, R. P.; LOPERA-BARRERO, N. M.; SANTOS, S. C. A.; RODRIGUEZ-RODRIGUEZ, M. P.; OLIVEIRA, S. N.; ALEXANDRE FILHO, L.; VARGAS, L.; GOES, E. S. R.; CASTRO, P. L.; POVEDA-PARRA, A. R. Genetic diversity of pacu for restocking programs in the Tietê and Grande rivers, Brazil. Semina: Ciências Agrárias, Londrina, v. 36, n. 6, p. 3807-3826, 2015.
SANCHES, A.; GALETTI JUNIOR, P. M. Microsatellites loci isolated in the freshwater fish Brycon hilarii. Molecular Ecology Notes, Oxford, v. 6, n. 4, p. 1045-1046, 2006.
SOUZA, F. P.; CASTRO, P. L.; GOES, E. S. R.; RIBEIRO, R. P.; SANTOS, S. C. A.; LIMA, E. C. S.; FURLAN MURARI, P. J.; LOPERA-BARRERO, N. M. Genetic variability of Prochilodus lineatus in artificial and semi-natural reproduction. Italian Journal of Animal Science, Bologna, v. 17, n. 2, p. 321-325, 2018.
WAGNER, R. L.; MAKRAKIS, S.; CASTRO-SANTOS, T.; MAKRAKIS, M. C.; DIAS, J. H. P.; BELMONT, R. F. Passage performance of long-distance upstream migrants at a large dam on the Paraná River and the compounding effects of entry and ascent. Neotropical Ichthyology, Maringá, v. 10, n. 4, p. 785-795, 2012.
YAZBECK, G. M.; KALAPOTHAKIS, E. Isolation and characterization of microsatellite DNA in the piracema fish Prochilodus lineatus (Characiformes). Genetics and Molecular Research, Ribeirão Preto, v. 6, n. 4, p. 1026-1034, 2007.
YEH, F. C.; BOYLE, T. Y. Z.; XIYAN, J. M. POPGENE version 131: microsoft window-based freeware for population genetic analysis. Alberta: University of Alberta and Center for International Forestry Research, 1999. 29 p.
AGOSTINHO, A. A.; PELICICE, F. M.; GOMES, L. C. Dams and the fish fauna of the Neotropical region: impacts and management related to diversity and fisheries. Brazilian Journal of Biology, São Carlos, v. 68, n. 4, p. 1119-1132, 2008. Supplement.
ASHIKAGA, F. Y.; ORSI, M. L.; OLIVEIRA, C.; SENHORINI, J. A.; FORESTI, F. The endangered species Brycon orbignyanus: genetic analysis and definition of priority areas for conservation. Environmental Biology of Fishes, Dordrecht, v. 98, n. 7, p. 1845-1855, 2015.
BARBOSA, A. C.; CORREA, T. C.; GALZERANI, F.; GALETTI, P. M.; HATANAKA, T. Thirteen polymorphic microsatellite loci in the Neotropical fish Prochilodus argenteus (Characiformes, Prochilodontidae). Molecular Ecology Resources, Oxford, v. 6, n. 3, p. 936-938, 2006.
BARBOSA, A. C.; GALZERANI, F.; CORRÊA, T. C.; GALETTI JUNIOR, P. M.; HATANAKA, T. Description of novel microsatellite loci in the Neotropical fish Prochilodus argenteus and cross-amplification in P. costatus and P. lineatus. Genetics and Molecular Biology, Ribeirão Preto, v. 31, n. 1, p. 357-360, 2008.
BARROCA, T. M.; SANTOS, G. B.; DUARTE, N. V. R.; KALAPOTHAKIS, E. Evaluation of genetic diversity and population structure in a commercially important freshwater fish Prochilodus costatus (Characiformes, Prochilodontidae) using complex hypervariable repeats. Genetics and Molecular Research, Ribeirão Preto, v. 11, n. 4, p. 4456-4467, 2012.
BARROSO, R. M.; HILSDORF, A. W. S.; MOREIRA, H. L. M.; MELLO, A. M.; GUIMARÃES, S. E. F.; CABELLO, P. H.; TRAUB-CSEKO, Y. M. Identification and characterization of microsatellites loci in Brycon opalinus (Cuvier, 1819) (Characiforme, Characidae, Bryconiae). Molecular Ecology Notes, Oxford, v. 3, n. 1, p. 297-298, 2003.
BASSAM, B. J.; CAETANO-ANOLLÉS, G.; GRESSHOFF, P. M. Fast and sensitive silver staining of DNA in polyacrylamide gels. Analytical Biochemistry, Bethesda, v. 196, n. 2, p. 80-83, 1991.
CALCAGNOTTO, D.; DESALLE, R. Population genetic structuring in pacu (Piaractus mesopotamicus) across the parana-paraguay basin: evidence from microsatellites. Neotropical Ichthyology, Maringá, v. 7, n. 4, p. 607-616, 2009.
CALCAGNOTTO, D.; RUSSELLO, M.; DESALLE, R. Isolation and characterization of microsatellite loci in Piaractus mesopotamicus and their applicability in other Serrasalminae fish. Molecular Ecology Notes, Oxford, v. 1, n. 4, p. 245-247, 2001.
CARVALHO-COSTA, L. F.; HATANAKA, T.; GALETTI JUNIOR, P. M. Evidence of lack of population substructuring in the Brazilian freshwater fish Prochilodus costatus. Genetics and Molecular Biology, Ribeirão Preto, v. 31, n. 1, p. 377-380, 2008.
CASTRO, P. L.; RIBEIRO, R. P.; SANTOS, S. C. A.; GOES, E. S. D. R.; SOUZA, F. P.; POVEDA-PARRA, A. R.; VARGAS, L.; URREA-ROJAS, A. M.; LOPERA-BARRERO, N. M. Cross-amplification of heterologous microsatellite markers in Piracanjuba. Ciência Rural, Santa Maria, v. 47, n. 12, p. 1-6, 2017.
CORNUET, J. M.; LUIKART, G. Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics, Rockville, v. 144, n. 4, p. 2001-2014, 1996.
FERREIRA, D. G.; SOUZA-SHIBATTA, L.; SHIBATTA, O. A.; SOFIA, S. H.; CARLSSON, J.; DIAS, J. H. P.; MAKRAKIS, S.; MAKRAKIS, M. C. Genetic structure and diversity of migratory freshwater fish in a fragmented Neotropical river system. Reviews in Fish Biology and Fisheries, London, v. 27, n. 1, p. 209-231, 2017.
GOUDET, J. FSTAT: a program to estimate and test gene diversities and fixation indices (version 2.9.3.2). Lausanne: University of Lausanne, Department of Ecology & Evolution, 2002. Disponível em: <http://www2.unil.ch/popgen/softwares/fstat.htm>. Acesso em: 26 jan. 2018.
INSTITUTO BRASILEIRO DE GEOGRAFIA E ESTATÍSTICA - IBGE. Produção da pecuária municipal 2015. Rio de Janeiro: IBGE, 2015. 49 p.
LAROCHE, J.; DURAND, J. D. Genetic structure of fragmented populations of a threatened endemic percid of the Rhône river: Zingel asper. Heredity, London, v. 92, n. 4, p. 329-334, 2004.
LOPERA-BARRERO, N. M.; POVH, J. A.; RIBEIRO, R. P.; GOMES, P. C.; JACOMETO, C. B.; LOPES, T. S. Comparación de protocolos de extracción de ADN con muestras de aleta y larva de peces: extracción modificada con cloruro de sodio. Ciencia e Investigación Agraria, Santiago, v. 35, n. 1, p. 76-86, 2008.
LOPERA-BARRERO, N. M.; SANTOS, S. C. A.; GOES, E. S. R.; CASTRO, P. L.; SOUZA, F. P.; POVEDA-PARRA, A. R.; CASSETA, J.; PONTILLO, B. G.; RIBEIRO, R. P. Monitoring and conservation genetics of Prochilodus lineatus wild populations of Pardo, Mogi Guaçu and Tiete rivers, São Paulo. Arquivo Brasileiro de Medicina Veterinária e Zootecnia, Belo Horizonte, v. 68, n. 6, p. 1621-1628, 2016.
LOPERA-BARRERO, N. M.; SANTOS, S. C. A.; RODRIGUEZ-RODRIGUEZ, M. P.; FORNARI, D. C.; ZANCHETA, C.; POVEDA-PARRA, A. R.; OLIVEIRA, C. A. L.; RIBEIRO, R. P. Genetic diversity of wild populations and broodstocks of curimba for restocking programs in the Tietê, Grande, Pardo and Mogi-Guaçu rivers (Brazil). Boletim do Instituto de Pesca, São Paulo, v. 41, n. 2, p. 287-304, 2015.
POVH, J. A.; RIBEIRO, R. P.; SIROL, R. N.; STREIT JUNIOR, D. P.; MOREIRA, H. L. M.; SIEWERDT, F.; LOPERA-BARRERO, N. M.; MANGOLIN, C. A.; VARGAS, L. Microsatellite analysis of the parental contribution of Piaractus mesopotamicus to the production of offspring in the semi-natural system of reproduction. Brazilian Archives of Biology and Technology, Curitiba, v. 53, n. 2, p. 389-396, 2010.
RAMOS, J. V. B.; SODRÉ, L. M. K.; ORSI, M. L.; ALMEIDA, F. S. Genetic diversity of the species Leporinus elongatus (Teleostei: Characiformes) in the Canoas Complex - Paranapanema River. Neotropical Ichthyology, Maringá, v. 10, n. 4, p. 821-828, 2012.
REVALDAVES, E.; RENESTO, E.; GOLD, J. R. Genetic variation of Prochilodus lineatus (Valenciennes, 1836) from Paraná, Baía, Miranda, and Corumbá rivers, Brazil. Genetics and Molecular Research, Ribeirão Preto, v. 15, n. 4, p. 1-11, 2016.
RIBEIRO, R. P.; LOPERA-BARRERO, N. M.; POVH, J. A.; RODRIGUEZ-RODRIGUEZ, M. P.; FORNARI, D. C.; BAUMGARTNER, G.; BAUMGARTNER, D.; SOUZA, F. P.; CASTRO, P. L.; POVEDA-PARRA, A. R. Genetic diversity of Salminus brasiliensis wild populations in downstream and upstream Cachoeira Branca, Verde River MS Brazil: a preliminary view. Semina: Ciências Agrárias, Londrina, v. 37, n. 1, p. 507-516, 2016.
RIBEIRO, R. P.; LOPERA-BARRERO, N. M.; SANTOS, S. C. A.; RODRIGUEZ-RODRIGUEZ, M. P.; OLIVEIRA, S. N.; ALEXANDRE FILHO, L.; VARGAS, L.; GOES, E. S. R.; CASTRO, P. L.; POVEDA-PARRA, A. R. Genetic diversity of pacu for restocking programs in the Tietê and Grande rivers, Brazil. Semina: Ciências Agrárias, Londrina, v. 36, n. 6, p. 3807-3826, 2015.
SANCHES, A.; GALETTI JUNIOR, P. M. Microsatellites loci isolated in the freshwater fish Brycon hilarii. Molecular Ecology Notes, Oxford, v. 6, n. 4, p. 1045-1046, 2006.
SOUZA, F. P.; CASTRO, P. L.; GOES, E. S. R.; RIBEIRO, R. P.; SANTOS, S. C. A.; LIMA, E. C. S.; FURLAN MURARI, P. J.; LOPERA-BARRERO, N. M. Genetic variability of Prochilodus lineatus in artificial and semi-natural reproduction. Italian Journal of Animal Science, Bologna, v. 17, n. 2, p. 321-325, 2018.
WAGNER, R. L.; MAKRAKIS, S.; CASTRO-SANTOS, T.; MAKRAKIS, M. C.; DIAS, J. H. P.; BELMONT, R. F. Passage performance of long-distance upstream migrants at a large dam on the Paraná River and the compounding effects of entry and ascent. Neotropical Ichthyology, Maringá, v. 10, n. 4, p. 785-795, 2012.
YAZBECK, G. M.; KALAPOTHAKIS, E. Isolation and characterization of microsatellite DNA in the piracema fish Prochilodus lineatus (Characiformes). Genetics and Molecular Research, Ribeirão Preto, v. 6, n. 4, p. 1026-1034, 2007.
YEH, F. C.; BOYLE, T. Y. Z.; XIYAN, J. M. POPGENE version 131: microsoft window-based freeware for population genetic analysis. Alberta: University of Alberta and Center for International Forestry Research, 1999. 29 p.
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2019-02-15
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Lopera-Barrero, N. M., Souza, F. P. de, Lima, E. C. S. de, Urrea-Rojas, A. M., Castro, P. L. de, Goes, E. S. dos R., … Ribeiro, R. P. (2019). Genetic diversity of migratory fish populations of the Rio Grande Reservoir (São Paulo, Brazil). Semina: Ciências Agrárias, 40(1), 503–510. https://doi.org/10.5433/1679-0359.2019v40n1p503
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