Hydrobiologia

, Volume 815, Issue 1, pp 65–72 | Cite as

Genetic evidences of non-reproductive shoaling in the freshwater fish Salminus brasiliensis

  • Josiane Ribolli
  • Evoy Zaniboni-Filho
  • Patricia D. Freitas
  • Pedro M. GalettiJr.
Primary Research Paper

Abstract

Recent studies have identified patterns of genetic organization during schooling in the reproductive period of several Neotropical freshwater migratory fish. However, population segregation during non-reproductive periods is still unknown for most species. In this study, we investigated the genetic structure of populations of Salminus brasiliensis, a high-value large migratory freshwater fish, sampled during the non-reproductive season. We analysed 89 adults from Uruguay River Basin (Brazil) collected during the two consecutive non-reproductive periods, and assessed the genetic diversity levels using eleven microsatellite loci. Our results showed that populations are genetically structured, suggesting these fish can remain grouped likely due to a cooperative behaviour, not related to reproduction, in a typical shoaling behaviour. Besides, we found high genetic diversity for S. brasiliensis from the Turvo State Park area, highlighting the importance of this conservation unit as a relevant area for maintaining the genetic variability of S. brasiliensis in the Uruguay River.

Keywords

Freshwater fish Conservation genetics Genetic structure Microsatellites Migratory fish 

Notes

Acknowledgements

JR acknowledges the financial support provided by Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) and Programa de Doutorado Sanduíche no Exterior (PDSE) (process1592/81-2). PMGJ thanks Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP, Grant 2010/52315-7), Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq, 308385/2014-4) and Sistema Nacional de Pesquisa em Biodiversidade (SISBIOTA-Brazil, MCTI/CNPq 563299/2010-0). EZF thanks Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq, Grant 302860/2014-2). We are grateful to Laboratório de Biologia e Cultivo de Peixes de Água Doce (LAPAD) of Universidade Federal de Santa Catarina (UFSC), Pedro Iaczinki and local fishermen for help with fish collections. The authors thank the two anonymous reviewers for valuable contributions improving the manuscript. Research was conducted under Animal Care Protocol PP00788.

Supplementary material

10750_2018_3550_MOESM1_ESM.pdf (160 kb)
Table S1 (PDF 159 kb)
10750_2018_3550_MOESM2_ESM.tif (17.6 mb)
Fig. S2 Plots displays mean log-likelihood values (LnP (D)) and Evanno´s Delta K generated in STRUCTURE HARVESTER based in 89 Salminus brasiliensis from Uruguay River Basin. STRUCTURE analysis was performed with six independent runs for K = 1-10 were performed at 500,000 Markov Chain Monte Carlo (MCMC) repetitions after a burn-in period of 300,000 iterations. Delta K results indicated that samples comprise two populations (K = 2) (TIFF 17982 kb)
10750_2018_3550_MOESM3_ESM.tif (120 kb)
Fig. S3 Discriminant Analysis of Principal Components (DAPC). (a) Density of individual scores on the first discriminant function, with groups represented in red (Pop-2011) and blue (Pop-2011). (b) Membership probabilities (in bar plots), represent individuals in different clusters. (TIFF 119 kb)
10750_2018_3550_MOESM4_ESM.docx (21 kb)
Table S4 (DOCX 21 kb)

References

  1. Aljanabi, S. M. & I. Martinez, 1997. Universal and rapid salt-extraction of high quality genomic DNA for PCR-based techniques. Nucleic acids research 25: 4692–4693.CrossRefPubMedPubMedCentralGoogle Scholar
  2. Batista, J. S. & J. A. Alves-Gomes, 2006. Phylogeography of Brachyplatystoma rousseauxii (Siluriformes–Pimelodidae) in the Amazon Basin offers preliminary evidence for the first case of “homing” for an Amazonian migratory catfish. Genetics and Molecular Research 5: 723–740.PubMedGoogle Scholar
  3. Braga-Silva, A. & P. M. Galetti, 2016. Evidence of isolation by time in freshwater migratory fish Prochilodus costatus (Characiformes, Prochilodontidae). Hydrobiologia 765: 159–167.CrossRefGoogle Scholar
  4. Carolsfeld, Y. & B. Harvey, 2003. Introduction: fishes of the floods. In Carolsfeld, J., B. Harvey, A. Baer & C. Ross (eds), Migratory fishes of South America: biology, fisheries and conservation status. International Development Research Centre and the World Bank, Victoria.Google Scholar
  5. Danzmann, R. G., M. M. Ferguson & D. L. G. Noakes, 1993. The genetic basis of fish behaviour. In Pitcher, T. J. (ed.), Behaviour of Teleost Fishes. Chapman & Hall, London.Google Scholar
  6. Delcourt, J. & P. Poncin, 2012. Shoals and schools: back to the heuristic definitions and quantitative references. Reviews in Fish Biology and Fisheries 22(3): 595–619.CrossRefGoogle Scholar
  7. Earl, D. & B. VonHoldt, 2012. STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conservation Genetics Resources 4: 359–361.CrossRefGoogle Scholar
  8. Evanno, G., S. Regnaut & J. Goudet, 2005. Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Molecular Ecology 14: 2611–2620.CrossRefPubMedGoogle Scholar
  9. Excoffier, L. & H. E. L. Lischer, 2010. Arlequin suite v. 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Molecular Ecology Resources 10: 564–567.CrossRefPubMedGoogle Scholar
  10. Falush, D. D., M. M. Stephens & J. K. Pritchard, 2003. Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics 164: 1567–1587.PubMedPubMedCentralGoogle Scholar
  11. Godoy, M. P., 1975. Peixes do Brasil, subordem Characoidei: bacia do rio Mogí Guassú. Editora Franciscana, Pirassununga.Google Scholar
  12. Goudet, J., 2001. FSTAT, a program to estimate and test gene diversities and fixation indices (v. 2.9. 3).Google Scholar
  13. Goulding, M., 1980. The Fishes and the Forest: Explorations in Amazonian Natural History. University of California Press, Berkeley.Google Scholar
  14. Hatanaka, T. & P. M. Galetti Jr., 2003. RAPD markers indicate the occurrence of structured populations in a migratory freshwater fish species. Genetics and Molecular Biology 26: 19–25.CrossRefGoogle Scholar
  15. Jombart, T., 2008. adegenet: a R package for the multivariate analysis of genetic markers. Bioinformatics 24(11): 1403–1405.CrossRefPubMedGoogle Scholar
  16. Jombart, T., S. Devillard, A. B. Dufour & D. Pontier, 2008. Revealing cryptic spatial patterns in genetic variability by a new multivariate method. Heredity 101(1): 92–103.CrossRefPubMedGoogle Scholar
  17. Jost, L., 2008. GST and its relatives do not measure differentiation. Molelucar Ecology 17: 4015–4026.CrossRefGoogle Scholar
  18. Jueterbock, A., P. Kraemer, G. Gerlach, J. Deppermann & M. A. Jueterbock, 2012. Package “DEMEtics”. Molecular Ecology 19: 3845–3852.Google Scholar
  19. Leberg, P. L., 2002. Estimating allelic richness: effects of sample size and bottlenecks. Molecular Ecology 11: 2445–2449.CrossRefPubMedGoogle Scholar
  20. Lowe-McConnell, R. H., 1967. Ecological Studies in Tropical Fish Communities. Cambridge University Press, Cambridge.Google Scholar
  21. Lucas, M. C. & E. Baras, 2001. Migration of Freshwater Fishes. Blackwell Science, Oxford.CrossRefGoogle Scholar
  22. Myers, G. S., 1949. Usage of anadromous, catadromous and allied terms for migratory fishes. Copeia 1949: 89–97.CrossRefGoogle Scholar
  23. 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
  24. Pereira, L. H. G., F. Foresti & C. Oliveira, 2009. Genetic structure of the migratory catfish Pseudoplatystoma corruscans (Siluriformes: Pimelodidae) suggests homing behaviour. Ecology of Freshwater Fish 18: 215–225.CrossRefGoogle Scholar
  25. Pitcher, T. J., 1983. Heuristic definitions of fish shoaling behaviour. Animal Behavior 31: 611–613.CrossRefGoogle Scholar
  26. Pitcher, T. J., 1986. Functions of shoaling behaviour in teleosts. In Pitcher, T. J. (ed.), The Behaviour of Teleost Fishes. Springer, Boston.CrossRefGoogle Scholar
  27. Pitcher, T. J. & J. K. Parrish, 1993. Functions of shoaling behaviour in teleosts. In Pitcher, T. J. (ed.), Behaviour of Teleost Fishes. Chapman & Hall, London.CrossRefGoogle Scholar
  28. Pritchard, J. K., M. Stephens & P. Donnelly, 2000. Inference of population structure using multilocus genotype data. Genetics 155: 945–959.PubMedPubMedCentralGoogle Scholar
  29. R Development Core Team, R., 2017. R: A Language and Environment for Statistical Computing. Vienna, R Foundation for Statistical Computing.Google Scholar
  30. Raymond, M. & F. Rousset, 1995. GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. Journal of heredity 86: 248–249.CrossRefGoogle Scholar
  31. Reynalte-Tataje, D. A., A. P. Nuñer, M. C. Nunes, V. Garcia, C. A. Lopes & E. Zaniboni-Filho, 2012. Spawning of migratory fish species between two reservoirs of the upper Uruguay River, Brazil. Neotropical Ichthyology 10(4): 829–835.CrossRefGoogle Scholar
  32. Ribeiro, M. B. L. B., 1983. As migrações dos jaraquis (Pisces, Prochilodontidae) no rio Negro, Amazonas, Brasil. Masters Dissertation, INPA/FUA. Manaus, 192 p.Google Scholar
  33. Ribolli, J., D. J. Hoeinghaus, J. A. Johnson, E. Zaniboni-Filho, P. D. de Freitas & P. M. Galetti, 2017. Isolation-by-time population structure in potamodromous Dourado Salminus brasiliensis in southern Brazil. Conservation Genetics 18: 67–76.CrossRefGoogle Scholar
  34. Rice, W. R., 1989. Analyzing tables of statistical tests. Evolution 43: 223–225.CrossRefPubMedGoogle Scholar
  35. Rueda, E. C., P. Carriquiriborde, A. M. Monzón, G. M. Somoza & G. Ortí, 2013. Seasonal variation in genetic population structure of sábalo (Prochilodus lineatus) in the Lower Uruguay River. Genetica 141: 401–407.CrossRefPubMedGoogle Scholar
  36. Ruschel, A. R., R. O. Nodari & B. M. Moerschbacher, 2007. Woody plant species richness in the Turvo State park, a large remnant of deciduous Atlantic forest, Brazil. Biodiversity Conservation 16: 1699–1714.CrossRefGoogle Scholar
  37. Sanches, A. & P. M. Galetti Jr., 2007. Genetic evidence of population structuring in the neotropical freshwater fish Brycon hilarii (Valenciennes, 1850). Brazilian Journal of Biology 67: 889–895.CrossRefGoogle Scholar
  38. Schork, G., S. Hermes-Silva, L. F. Beux, E. Zaniboni-Filho & A. P. O. Nuñer, 2012. Diagnóstico da pesca artesanal na usina hidrelétrica de machadinho, alto Rio Uruguai – Brasil. Boletim do Instituto de Pesca 38: 97–108.Google Scholar
  39. Schork, G., S. Hermes-Silva & E. Zaniboni-Filho, 2013. Analysis of fishing activity in the Itá reservoir, Upper Uruguay River, in the period 2004-2009. Brazilian Journal of Biology 73: 559–571.CrossRefGoogle Scholar
  40. Schuelke, M., 2000. An economic method for the fluorescent labeling of PCR fragments. Nature Biotechnology 18(2): 233–234.CrossRefPubMedGoogle Scholar
  41. Slatkin, M., 1995. A measure of population subdivision based on microsatellite allele frequencies. Genetics 139: 457–462.PubMedPubMedCentralGoogle Scholar
  42. 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
  43. Weir, B. S. & C. C. Cockerham, 1984. Estimating F-statistics for the analysis of population structure. Evolution 38: 1358–1370.PubMedGoogle Scholar
  44. Zaniboni-Filho, E., 1985. Biologia da reprodução do matrinxã, Bricon cephalus (Günther, 1869) (Teleostei: Characidae). Masters dissertation, INPA/FUA. Manaus, Brazil, 134 p.Google Scholar
  45. Zaniboni-Filho, E. & U. H. Schulz, 2003. Migratory fishes of the Uruguay River. In Carolsfeld, J., B. Harvey, A. Baer & C. Ross (eds), Migratory Fishes of South America: Biology, Fisheries and Conservation Status. International Development Research Centre and the World Bank, Victoria.Google Scholar
  46. Ziober, S. R., D. A. Reynalte-Tataje & E. Zaniboni-Filho, 2015. The importance of a conservation unit in a subtropical basin for fish spawning and growth. Environmental Biology of Fishes 98: 725–737.CrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  • Josiane Ribolli
    • 1
    • 2
    • 3
  • Evoy Zaniboni-Filho
    • 2
  • Patricia D. Freitas
    • 3
  • Pedro M. GalettiJr.
    • 3
  1. 1.Programa de Pós-Graduação em Ecologia e Recursos NaturaisUniversidade Federal de São CarlosSão CarlosBrazil
  2. 2.Laboratório de Biologia e Cultivo de Peixes de Água Doce, Departamento de AquiculturaUniversidade Federal de Santa CatarinaFlorianópolisBrazil
  3. 3.Laboratório de Biodiversidade Molecular e Conservação, Departamento de Genética e EvoluçãoUniversidade Federal de São CarlosSão CarlosBrazil

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