Advertisement

Hydrobiologia

, Volume 819, Issue 1, pp 243–257 | Cite as

Species assignment and population genetic studies of Gran Paraná pejerrey (Odontesthes sp., Atheriniformes, Atherinopsidae) from La Plata Basin in South America

  • Gabriela Vanina Villanova
  • Manuel Vera
  • Florencia Brancolini
  • Juan Díaz
  • Paulino Martinez
  • Silvia Eda Arranz
Primary Research Paper

Abstract

Pejerrey is the common name given to Odontesthes species from South America. Every year, individuals of pejerrey called “Gran (Big) Paraná” appear during the low-temperature season at rivers in the southern section of the La Plata Basin. Gran Paraná fishes are highly appreciated for fishing, and present some biological features different from other well-characterized Odontesthes fish, such as bigger size and migratory behavior. Regulations for the management of pejerrey fisheries within La Plata Basin have not been implemented yet. The aims of the present work were to characterize the Gran Paraná pejerrey species by molecular methods and carry out the first population genetic study of Gran Parana pejerrey from the La Plata Basin. All Gran Paraná specimens were classified as O. bonariensis, based on both morphology and microsatellite loci. Genetic differentiation was observed between Gran Paraná pejerrey and O. bonariensis pejerrey sampled at Chascomús lagoon. In addition, temporal genetic differentiation was observed, suggesting the presence of different cohorts migrating along the basin. The knowledge of population dynamics and differentiation will contribute to figure out fisheries models and to design protective areas for this species under commercial exploitation.

Keywords

Molecular markers River Estuary Genetics Sustainability Fish Odontesthes bonariensis 

Notes

Acknowledgements

We would like to thank Alexis Grimberg, Julián Aguilar, and Diego Añaño and team for fishing assistance, Darío Colautti for the kind donation of samples, Victoria Posner for reading the manuscript, and anonymous reviewers that helped to improve our work. This work was supported by the National Agency for the Promotion of Science and Technology from Argentina (ANPCyT) and the Government of Santa Fe province [Grant Numbers: PID 020-2013 and PICT 0510-2011]; FB is a Ph. D student, JD is a postdoctoral fellow, and GVV is member of the researcher carrier from the National Council of Research from Argentina.

Compliance with ethical standards

Conflict of interest

The authors have no conflict of interest to declare.

Supplementary material

10750_2018_3643_MOESM1_ESM.eps (20.9 mb)
Figure S1. Genetic analyses using CR mtDNA marker. (A) Maximum-Likelihood tree. The evolutionary history was inferred by using the Maximum-Likelihood method based on the Tamura 3-parameter model (Tamura, 1992) (α = 0.1343; ts/tv: 4.87). The bootstrap consensus tree inferred from 1000 replicates is taken to represent the evolutionary history of the taxa analyzed. The percentage of replicate trees in which the associated taxa clustered together in the bootstrap test (1000 replicates) is shown next to the branches. (B) Median Joining Network. Numbers correspond to CRs haplotypes numbers. The size of circles is proportional to the number of individuals that share a particular haplotype. Median vectors are indicated as red spots. Each color represents a sample site or species previously described, and it is indicated at the color reference box. Branches length is proportional to the number of differences between haplotypes. (EPS 21443 kb)
10750_2018_3643_MOESM2_ESM.eps (7.5 mb)
Figure S2. Factorial correspondence analysis (FCA) plot. Genetic relationships between pejerrey individuals collected from PR, UR, iRLP, cRLP and CHL, at different years are shown in a 3D FCA plot. (EPS 7695 kb)
10750_2018_3643_MOESM3_ESM.docx (36 kb)
Supplementary Table 1 (DOCX 36 kb)
10750_2018_3643_MOESM4_ESM.docx (24 kb)
Supplementary Table 2 (DOCX 23 kb)
10750_2018_3643_MOESM5_ESM.docx (16 kb)
Supplementary Table 3 (DOCX 16 kb)
10750_2018_3643_MOESM6_ESM.docx (14 kb)
Supplementary Table 4 (DOCX 13 kb)
10750_2018_3643_MOESM7_ESM.docx (12 kb)
Supplementary Table 5 (DOCX 12 kb)

References

  1. Alarcón-Durán, I., M. A. Castillo-Rivera, G. Figueroa-Lucero, J. Arroyo-Cabrales & I. Barriga-Sosa, 2017. Morphological diversity in 6 populations of the Silverside Chirostoma humboldtianum. Revista Mexicana de Biodiversidad 88: 207–214.CrossRefGoogle Scholar
  2. Avigliano, E. & A. V. Volpedo, 2013. Actinopterygii, Atheriniformes, Atherinopsidae, Odontesthes bonariensis Valenciennes, 1835: new records for the Plata Basin. Argentina Check List 9: 640–641.CrossRefGoogle Scholar
  3. Baigún, C. R. M., A. Puig, P. M. Minotti, P. Kandus, R. D. Quintana, R. Vicari, R. Bo, N. Oldani & J. A. Nestler, 2008. Resource use in the Parana River Delta (Argentina) moving away from an ecohydrological approach? Ecohydrology and Hydrobiology 8: 245–262.CrossRefGoogle Scholar
  4. Bamber, R. N. & P. A. Henderson, 1988. Pre-adaptive plasticity in atherinids and the estuarine seat of teleost evolution. Journal of Fish Biology 33: 17–23.CrossRefGoogle Scholar
  5. Bandelt, H. J., P. Forster & A. Röhl, 1999. Median-joining networks for inferring intraspecific phylogenies. Molecular Biology and Evolution 16: 37–48.CrossRefPubMedGoogle Scholar
  6. Barrero, N. L., 2008. Caracterización genética de lotes de peces usados en programas de repoblamiento y su importancia en la conservación genética en la piscicultura. Zootecnia 26: 515–522.Google Scholar
  7. Beheregaray, L. B. & P. Sunnucks, 2001. Fine-scale genetic structure, estuarine colonization and incipient speciation in the marine silverside fish Odontesthes argentinensis. Molecular Ecology 10: 2849–2866.CrossRefPubMedGoogle Scholar
  8. Beheregaray, L. B., P. Sunnucks & D. A. Briscoe, 2002. A rapid fish radiation associated with the last sea-level changes in southern Brazil: the silverside Odontesthes perugiae complex. Proceedings of the Royal Society of London B 269: 65–73.CrossRefGoogle Scholar
  9. Belkhir, K., P. Borsa, L. Chikhi, N. Raufaste & F. Bonhomme, 1996–2004. GENETIX 4.05, logiciel sous Windows TM pour la génétique des populations. Laboratoire Génome, Populations, Interactions, CNRS UMR 5171, Université de Montpellier II, Montpellier (France).Google Scholar
  10. Bemvenuti, M. A., 2002. Silversides in South Brazil: morphological and ecological aspects. Biocell 30: 111–118.Google Scholar
  11. Bemvenuti, M. A., 2006. Silversides in South Brazil: Morphological and ecological aspects. Biocell, 30 (1): 111–118.PubMedGoogle Scholar
  12. Bloom, D. D., J. T. Weir, K. R. Piller & N. R. Lovejoy, 2013. Do freshwater fishes diversify faster than marine fishes? A test using state-dependent diversification analyses and molecular phylogenetic of new world silversides (atherinopsidae). Evolution 67: 2040–2057.CrossRefPubMedGoogle Scholar
  13. Campanella, D., L. C. Hughes, P. J. Unmack, D. D. Bloom, K. R. Piller & G. Ortí, 2015. Multi-locus fossil-calibrated phylogeny of Atheriniformes (Teleostei, Ovalentaria). Molecular Phylogenetic and Evolution 86: 8–23.CrossRefGoogle Scholar
  14. Colautti, D., C. Baigún, F. Llompart, T. Maiztegui, J. Garcia de Souza, P. Solimano, L. Balboni & G. Berasain, 2015. Fish assemblage of a Pampean shallow lake, a story of instability. Hydrobiologia 752: 175–186.CrossRefGoogle Scholar
  15. Crispo, E. & L. J. Chapman, 2010. Temporal variation in population genetic structure of a Riverine African Cichlid Fish. Journal of Heredity 101: 97–106.CrossRefPubMedGoogle Scholar
  16. Cuello, M. V., A. Solari & M. L. García, 2010. Pisces, Atheriniformes, Atherinopsidae, Odontesthes perugiae Evermann and Kendall, 1906: distribution extension, new records and geographic distribution map for the species. Check List 6: 309–310.CrossRefGoogle Scholar
  17. DeWoody, J. A. & J. C. Avise, 2000. Microsatellite variation in marine, freshwater and anadromous fishes compared with other animals. Journal of Fish Biology 56: 461–473.CrossRefGoogle Scholar
  18. Diaz, J., G. V. Villanova, F. Brancolini, F. Del Pazo, V. M. Posner, A. Grimberg & S. E. Arranz, 2016. First DNA barcode reference library for the identification of South American freshwater fish from the lower Paraná River. PLoS ONE 11: e0157419.  https://doi.org/10.1371/journal.pone.0157419.CrossRefPubMedPubMedCentralGoogle Scholar
  19. Dunn, O. J., 1961. Multiple comparisons among means. Journal of the American Statistical Association 56: 52–64.CrossRefGoogle Scholar
  20. Dyer, B. S., 1993. A phylogenetic study of atheriniform fishes with a systematic revision of the South American silversides (Atherinomorpha, Atherinopsinae, Sorgentinini). PhD Thesis, University of Michigan.Google Scholar
  21. Dyer, B. S., 2006. Systematic revision of the South American silversides (Teleostei, Atheriniformes). Biocell 30: 69–88.PubMedGoogle Scholar
  22. Elisio, M., T. Chalde & L. A. Miranda, 2014. Seasonal changes and endocrine regulation of pejerrey (Odontesthes bonariensis) oogenesis in the wild. Comparative Biochemistry and Physiology Part A 175: 102–109.CrossRefGoogle Scholar
  23. Elisio, M., T. Chalde & L. A. Miranda, 2015. Seasonal changes and endocrine regulation of pejerrey (Odontesthes bonariensis) spermatogenesis in the wild. General and Comparative Endocrinology 221: 236–243.CrossRefPubMedGoogle Scholar
  24. Excoffier, L., G. Laval & S. Schneider, 2005. Arlequin ver. 3.0: an integrated software package for population genetics data analysis. Evolutionary Bioinformatics Online 1: 47–50.Google Scholar
  25. FISHBASE, (ver. 06/2016). http://www.fishbase.org
  26. Frankham, R., J. D. Ballou & D. A. Briscoe, 2002. Introduction to Conservation Genetics. Cambridge University Press, Cambridge.CrossRefGoogle Scholar
  27. Fu, Y. X. & W. H. Li, 1993. Statistical tests of neutrality of mutations. Genetics 133: 693–709.PubMedPubMedCentralGoogle Scholar
  28. García, G., N. Ríos, V. Gutiérrez, J. G. Varela, C. Bouza Fernández, B. Gómez Pardo & P. Martinez, 2014. Promiscuous speciation with gene flow in silverside fish genus Odontesthes (Atheriniformes, Atherinopsidae) from South Western Atlantic Ocean Basins. PLoS ONE. 9: e104659.  https://doi.org/10.1371/journal.pone.0104659.CrossRefPubMedPubMedCentralGoogle Scholar
  29. Gómez, S. E. & R. A. Ferriz, 2001. Algunos aspectos de la ecofisiología del pejerrey. In Grosman, F. (ed.), Fundamentos biológicos, económicos y sociales para una correcta gestión del recurso pejerrey. Buenos Aires, Argentina, Editorial Astyanax: 15–20.Google Scholar
  30. González-Castro, M., J. J. Rosso, E. Mabragaña & J. M. Díaz de Astarloa, 2016. Surfing among species, populations and morphotypes: inferring boundaries between two species of new world silversides (Atherinopsidae). Comptes Rendus Biologies 339(1): 10–23.CrossRefPubMedGoogle Scholar
  31. Goudet, J., 2001. FSTAT, a program to estimate and test gene diversities and fixation indices version 2.9.3. http://www.unil.ch/izea/softwares/fstat.html, updated from Goudet (1995) FSTAT (vers. 1.2): a computer program to calculate F-statistics. Journal of Heredity 86:485–186
  32. Guo, S. & E. A. Thompson, 1992. Performing the exact test of Hardy-Weinberg proportion for multiple alleles. Biometrics 48: 361–372.CrossRefPubMedGoogle Scholar
  33. Hall, A. T., 1999. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series 41: 95–98.Google Scholar
  34. Hasegawa, M., H. Kishino & T. Yano, 1985. Dating of human-ape splitting by a molecular clock of mitochondrial DNA. Journal of Molecular Evolution 22: 160–174.CrossRefPubMedGoogle Scholar
  35. Hendry, A. P. & T. Day, 2005. Population structure attributable to reproductive time: isolation by time and adaptation by time. Molecular Ecology 14: 901–916.CrossRefPubMedGoogle Scholar
  36. Heras, S. & M. I. Roldan, 2011. Phylogenetic inference in Odontesthes and Atherina (Teleostei:Atheriniformes) with insights into ecological adaptation. Comptes Rendus Biologies 334(4): 273–281.CrossRefPubMedGoogle Scholar
  37. Higgins, D., J. Thompson, T. Gibson, J. D. Thompson, D. G. Higgins & T. J. Gibson, 1994. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Research 22: 4673–4680.CrossRefPubMedPubMedCentralGoogle Scholar
  38. Hughes, L. C., G. M. Somoza, B. N. Nguyen, J. P. Bernot, M. González-Castro, J. M. Díaz de Astarloa & G. Ortí, 2017. Transcriptomic differentiation underlying marine-to-freshwater transitions in the South American silversides Odontesthes argentinensis and O. bonariensis (Atheriniformes). Ecology and Evolution 7: 5258–5268.CrossRefPubMedPubMedCentralGoogle Scholar
  39. Ivanova, N. V., T. S. Zemlak, R. H. Hanner & P. D. N. Hebert, 2007. Universal primer cocktails for fish DNA barcoding. Molecular Ecology Notes 7: 544–548.CrossRefGoogle Scholar
  40. Iwaszkiw, J. M., & F. F. Lacoste, 2011. La pesca artesanal en la Cuenca del Plata (Argentina) y sus implicancias en la conservación de la biodiversidad en la Cuenca del Plata. Revista del Museo Argentino de Ciencias Naturales n.s. 2113: 21–25.Google Scholar
  41. Jaureguizar, A., R. Menni, R. Guerrero & C. Lasta, 2004. Environmental factors structuring fish communities of the Río de la Plata estuary. Fisheries Research 66: 195–211.CrossRefGoogle Scholar
  42. Kalinowski, S. T., M. L. Taper & T. C. Marshall, 2007. Revising how the computer program CERVUS accommodates genotyping error increases success in paternity assignment. Molecular Ecology 16: 1099–1106.CrossRefPubMedGoogle Scholar
  43. Kandus, P., 2006. Patrones de paisaje y biodiversidad del Bajo Delta del Río Paraná. Mapa de ambientes. Landscape patterns and biodiversity of the Lower Delta of the Paraná River. Landcover map/Patricia Kandus; Rubén D. Quintana; Roberto F. Bó - 1a ed. - Buenos Aires: Pablo Casamajor,Google Scholar
  44. Langella, O., 1999. Populations 1.2.30: Population genetic software (individuals or populations distances, phylogenetic trees). France. http://bioinformatics.org/~tryphon/populations/
  45. Librado, P. & J. Rozas, 2009. DnaSP v. 5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25: 1451–1452.CrossRefPubMedGoogle Scholar
  46. Liotta, J., 2005. Distribución Geográfica de los Peces de Aguas Continentales de la República Argentina. 701 Eds, ProBiota Serie Documentos 3, Buenos Aires, Argentina.Google Scholar
  47. Mabragaña, E., J. M. Diaz de Astarloa, R. Hanner, J. Zhang & M. González-Castro, 2011. DNA barcoding identifies argentine fishes from marine and brackish waters. PLoS ONE 6(12): E28655.CrossRefPubMedPubMedCentralGoogle Scholar
  48. Mancini, M. & F. Grosman, 2001. Efecto de la pesca deportiva sobre una población de pejerrey Odontesthes bonariensis. In Grosman, F. (ed.), Fundamentos biológicos, económicos y sociales para una correcta gestión del recurso pejerrey. Editorial Astyanax, Buenos Aires.Google Scholar
  49. Mancini, M., Grosman, F., Dyer, B., García, G., Del Ponti, O., Sanzano, P. & V. Salinas, 2016. Taxonomía y distribución de los pejerreyes. Un panorama complejo y desafiante. In: Pejerreyes del sur de América: aportes al estado de conocimiento con especial referencia a Odontesthes bonariensis. Editorial Unirío. Universidad Nacional de Río Cuarto, Río Cuarto, Argentina.Google Scholar
  50. Mirande, J. M. & S. Koerber, 2015. Checklist of the freshwater fishes of Argentina (CLOFFAR). Ichthyological Contributions of Peces Criollos 36: 1–68.Google Scholar
  51. Nei, M. & S. Kumar, 2000. Molecular evolution and phylogenetics. Oxford University Press, New York.Google Scholar
  52. Nei, M., F. Tajima & Y. Tateno, 1983. Accuracy of estimated phylogenetic trees from molecular data. II. Gene frequency data. Journal of Molecular Evolution 19: 153–170.CrossRefPubMedGoogle Scholar
  53. Neiff, J. J., &, A. I. Malvarez, 2004. Grandes humedales fluviales. In Malvarez A. I. & R. F. Bó (eds), Documentos del curso-taller Bases ecológicas para la clasificación e inventario de humedales en Argentina. FCEN (UBA)—RAMSAR—USFWS—USDS, Buenos Aires, Argentina: 77–85.Google Scholar
  54. Peakall, R. & P. E. Smouse, 2006. GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Molecular Ecology Notes 6: 288–295.CrossRefGoogle Scholar
  55. Rice, W. R., 1989. Analyzing tables of statistical tests. Evolution 43 (1):223–225.CrossRefPubMedGoogle Scholar
  56. Rosso, J. J., 2008. Relación entre la abundancia y estructura de la comunidad de peces y el régimen hidrológico en lagunas de la alta cuenca del río Salado. Unpublished Ph.D. Dissertation, Universidad de Buenos Aires, Buenos Aires.Google Scholar
  57. Rosso, J. J. & R. Quirós, 2009. Interactive effects of abiotic, hydrological and anthropogenic factors on fish abundance and distribution in natural run-of-the-river shallow lakes. River Research and Applications 25: 713–733.CrossRefGoogle Scholar
  58. Rousset, F., 2008. Genepop’007: a complete reimplementation of the Genepop software for Windows and Linux. Molecular Ecology Resources 8: 103–106.CrossRefPubMedGoogle Scholar
  59. Schneider, H., 2003. Métodos de análise filogenética—Um guia prático. Holos and SBG, Ribeirão Preto.Google Scholar
  60. Sivasundar, A., E. Bermingham & G. Ortí, 2001. Population structure and biogeography of migratory freshwater fishes (Prochilodus: Characiformes) in major South American rivers. Molecular ecology 10: 407–417.CrossRefPubMedGoogle Scholar
  61. Strüssmann, C. A., T. Akaba, K. Ijima, K. Yamaguchi, G. Yoshizaki & F. Takashima, 1997. Spontaneous hybridization in the laboratory and genetic markers for the identification of hybrids between two atherinid species, Odontesthes bonariensis (Cuvier et Valenciennes) and Patagonina hatcheri Eigenmann. Aquaculture Research 28: 291–300.CrossRefGoogle Scholar
  62. Tajima, F., 1989. Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123: 585–595.PubMedPubMedCentralGoogle Scholar
  63. Tamura, K., 1992. Estimation of the number of nucleotide substitutions when there are strong transition-transversion and G + C content biases. Molecular Biology and Evolution 9: 678–687.PubMedGoogle Scholar
  64. Tamura, K., D. Peterson, N. Peterson, G. Stecher, M. Nei & S. Kumar, 2011. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution 28: 2731–2739.CrossRefPubMedPubMedCentralGoogle Scholar
  65. Tejedor, D., 2001. El pejerrey como recurso genético. In Grosman, F. (ed.), Fundamentos biológicos, económicos y sociales para una correcta gestión del recurso pejerrey. Editorial Astyanax, Azul.Google Scholar
  66. Tsuzuki, M. Y., H. Aikawa & C. A. Strüssmann, 2000. Comparative survival and growth of embryos\larvae\and juveniles of pejerrey Odontesthes bonariensis and O. hatchery at different salinities. Journal of Applied Ichthyology 16: 126–130.CrossRefGoogle Scholar
  67. Van Oosterhout, C., W. F. Hutchinson, D. P. M. Wills & P. Shipley, 2004. MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Molecular Ecology Notes 4: 535–538.CrossRefGoogle Scholar
  68. Villanova, G. V., M. Vera, J. Díaz, P. Martinez, N. B. Calcaterra & S. E. Arranz, 2013. Microsatellite marker characterization for the pejerrey, Odontesthes bonariensis, using 454-Roche pyrosequencing technology. Molecular Ecology Resources 13: 546–549.CrossRefPubMedGoogle Scholar
  69. Walsh, P. S., D. A. Metzger & R. Higuchi, 1991. Chelex 100 as a medium for simple extraction of DNA for PCR-based typing from forensic material. Biotechniques 10: 506–513.PubMedGoogle Scholar
  70. Ward, R. D., 2009. DNA barcode divergence among species and genera of birds and fishes. Molecular Ecology Resources 9: 1077–1085.CrossRefPubMedGoogle Scholar
  71. Wingert, J. M., J. Ferrer & L. R. Malabarba, 2017. Review of the Odontesthes perugiae species group from Río de La Plata drainage, with the description of a new species (Atherinomorpha: Atherinopsidae). Zootaxa 4250(6): 501–528.CrossRefPubMedGoogle Scholar
  72. Wright, S., 1951. The genetical structure of populations. Annals of Eugenics 15: 323–354.CrossRefPubMedGoogle Scholar
  73. Xia, X., C. Li & Q. Yang, 2003. Routine analysis of molecular data with software DAMBE. In Yang, Q. (ed.), Fundamental Concepts and Methodology in Molecular Paleontology. Science Publishers, China: 149–167.Google Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  • Gabriela Vanina Villanova
    • 1
  • Manuel Vera
    • 2
  • Florencia Brancolini
    • 3
  • Juan Díaz
    • 1
  • Paulino Martinez
    • 2
  • Silvia Eda Arranz
    • 1
  1. 1.Laboratorio de Biotecnología AcuáticaFacultad de Ciencias Bioquímicas y Farmacéuticas – Universidad Nacional de Rosario- Centro Científico, Tecnológico y Educativo Acuario del Río ParanáRosarioArgentina
  2. 2.Department of Zoology, Genetics and Physical Anthropology, Faculty of VeterinaryUniversity of Santiago de CompostelaLugoSpain
  3. 3.Instituto de Investigación e Ingeniería AmbientalUniversidad Nacional de San Martín, CONICETSan MartinArgentina

Personalised recommendations