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Evidence of isolation by time in freshwater migratory fish Prochilodus costatus (Characiformes, Prochilodontidae)

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Abstract

The coexistence of individuals in the same river and their ability to make long-distance migrations suggest that they constitute a single panmictic population; however, several studies have indicated population genetic structuring in freshwater migratory fish species. Historical, ecological, and anthropogenic effects have been proposed to promote the genetic differentiation among freshwater fish populations. Isolation by time and spatial differentiation have been considered to explain such finding in different fish groups. Here, we tested both hypotheses with Prochilodus costatus, a freshwater fish that migrates long distances to reproduce, using microsatellites to assess the genetic variation. We verified population structure by using diverse statistical methods: Wright’s fixation index (F ST), factorial correspondence analysis, and relatedness and assignment methods. All methods confirmed the lack of spatial structuring, refuting a homing behaviour hypothesis; however, the first three methods indicated temporal structuring within a reproductive season. Failure to detect genetic structuring using the assignment method was the result of gene flow. Whereas the gene flow can be present between differentiated populations, we conclude that isolation by time occurs in P. costatus.

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References

  • Aljanabi, S. M. & I. Martinez, 1997. Universal and rapid salt-extraction of high quality genomic DNA for PCR-based techniques. Nucleic Acids Research 25(22): 4692–4693.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Ayres, M., M. Ayres Jr, D. Ayres & A. Santos, 2003. BioEstat. Version 3.0, Sociedade Civil Mamirauá. MCT–CNPQ, Belém, Pará.

    Google Scholar 

  • Barbosa, A. C. D. R., T. C. Corrêa, F. Galzerani, P. M. Galetti Jr & T. Hatanaka, 2006. Thirteen polymorphic microsatellite loci in the Neotropical fish Prochilodus argenteus (Characiformes, Prochilodontidae). Molecular Ecology Notes 6(3): 936–938.

    Article  CAS  Google Scholar 

  • Barbosa, A., F. Galzerani, T. C. Corrêa, P. M. Galetti Jr & T. Hatanaka, 2008. Description of novel microsatellite loci in the Neotropical fish Prochilodus argenteus and cross-amplification in P. costatus and P. lineatus. Genetics and Molecular Biology 31(1): 357–360.

    Article  CAS  Google Scholar 

  • Barroca, T., G. Santos, N. Duarte & E. Kalapothakis, 2012. 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 11(4): 4456–4467.

    Article  CAS  PubMed  Google Scholar 

  • Batista, J. & J. 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(4): 723–740.

    PubMed  Google Scholar 

  • Belkhir, K., P. Borsa, L. Chikhi, N. Raufaste & F. Bonhomme, 2004. GENETIX, Software Under Windows for the Genetic of Populations, 4.05th ed. Laboratory Genome, Populations, Interactions CNRS UMR 5000, University of Montpellier II, Montpellier.

    Google Scholar 

  • Carvalho-Costa, L. F., T. Hatanaka & P. M. Galetti, 2006. Isolation and characterization of polymorphic microsatellite markers in the migratory freshwater fish Prochilodus costatus. Molecular Ecology Notes 6(3): 818–819.

    Article  CAS  Google Scholar 

  • Carvalho-Costa, L. F., T. Hatanaka & P. M. Galetti Jr, 2008. Evidence of lack of population substructuring in the Brazilian freshwater fish Prochilodus costatus. Genetics and Molecular Biology 31(1): 377–380.

    Article  CAS  Google Scholar 

  • Castro, R. M. C. & R. P. Vari, 2004. Detritivores of the South American fish family Prochilodontidae (Teleostei: Ostariophysi: Characiformes): a phylogenetic and revisionary study. Smithsonian Contributions to Zoology 622: 1–189.

    Article  Google Scholar 

  • Chapuis, M. P. & A. Estoup, 2007. Microsatellite null alleles and estimation of population differentiation. Molecular Biology and Evolution 24(3): 621–631.

    Article  CAS  PubMed  Google Scholar 

  • Davidsen, J. G., A. H. Rikardsen, E. B. Thorstad, E. Halttunen, H. Mitamura, K. Præbel, J. Skarðhamar, T. F. Næsje & M. Trudel, 2013. Homing behaviour of Atlantic salmon (Salmo salar) during final phase of marine migration and river entry. Canadian Journal of Fisheries and Aquatic Sciences 70(5): 794–802.

    Article  Google Scholar 

  • Flecker, A. S., 1996. Ecosystem engineering by a dominant detritivore in a diverse tropical stream. Ecology 77(6): 1845–1854.

    Article  Google Scholar 

  • Gagliardo, A., C. Filannino, P. Ioalè, T. Pecchia, M. Wikelski & G. Vallortigara, 2011. Olfactory lateralization in homing pigeons: a GPS study on birds released with unilateral olfactory inputs. The Journal of Experimental Biology 214(4): 593–598.

    Article  PubMed  Google Scholar 

  • Garcez, R., D. Calcagnotto, D. Almeida-Toledo & L. Foresti, 2011. Population structure of the migratory fish Prochilodus lineatus (Characiformes) from Rio Grande basin (Brazil), an area fragmented by dams. Aquatic Conservation: Marine and Freshwater Ecosystems 21(3): 268–275.

    Article  Google Scholar 

  • Gerking, S. D., 1959. The restricted movement of fish populations. Biological Reviews 34(2): 221–242.

    Article  Google Scholar 

  • Godinho, A. L. & B. Kynard, 2006. Migration and spawning of radio-tagged zulega Prochilodus argenteus in a dammed Brazilian River. Transactions of American Fisheries Society 135(3): 811–824.

    Article  Google Scholar 

  • Godinho, A., P. Pompeu & H. Godinho, 2003. A importância de ribeirões para os peixes de piracema. Águas, peixes e pescadores do São Francisco das Gerais. PUC Minas, Belo Horizonte: 361–372.

    Google Scholar 

  • Goudet, J., 2001. FSTAT, a program to estimate and test gene diversities and fixation indices (version 2.9. 3). Available from http://www.unil.ch/izea/softwares/fstat.html.

  • Hatanaka, T., F. Henrique-Silva & P. M. Galetti, 2006. Population substructuring in a migratory freshwater fish Prochilodus argenteus (Characiformes, Prochilodontidae) from the São Francisco River. Genetica 126(1): 153–159.

    Article  PubMed  Google Scholar 

  • Hendry, A. P. & T. Day, 2005. Population structure attributable to reproductive time: isolation by time and adaptation by time. Molecular Ecology 14(4): 901–916.

    Article  CAS  PubMed  Google Scholar 

  • Jones, O. R. & J. Wang, 2012. A comparison of four methods for detecting weak genetic structure from marker data. Ecology and Evolution 2(5): 1048–1055.

    Article  PubMed Central  PubMed  Google Scholar 

  • Jørgensen, H. B. H., M. M. Hansen & V. Loeschcke, 2005. Spring-spawning herring (Clupea harengus L.) in the southwestern Baltic Sea: Do they form genetically distinct spawning waves? ICES Journal of Marine Science: Journal du Conseil 62(6): 1065–1075.

    Google Scholar 

  • Jost, L., 2008. GST and its relatives do not measure differentiation. Molecular Ecology 17(18): 4015–4026.

    Article  PubMed  Google Scholar 

  • Kiss, L., A. Pintye, G. M. Kovacs, T. Jankovics, M. C. Fontaine, N. Harvey, X. Xu, P. C. Nicot, M. Bardin & J. A. Shykoff, 2011. Temporal isolation explains host-related genetic differentiation in a group of widespread mycoparasitic fungi. Molecular Ecology 20(7): 1492–1507.

    Article  PubMed  Google Scholar 

  • Maes, G. E., J. Pujolar, B. Hellemans & F. A. Volckaert, 2006. Evidence for isolation by time in the European eel (Anguilla anguilla L.). Molecular Ecology 15(8): 2095–2107.

    Article  CAS  PubMed  Google Scholar 

  • McPherson, A. A., R. L. Stephenson & C. T. Taggart, 2003. Genetically different Atlantic herring Clupea harengus spawning waves. Marine Ecology Progress Series 247: 303–309.

    Article  CAS  Google Scholar 

  • Møller, A., A. Antonov, B. Stokke, F. Fossøy, A. Moksnes, E. Røskaft & F. Takasu, 2011. Isolation by time and habitat and coexistence of distinct host races of the common cuckoo. Journal of Evolutionary Biology 24(3): 676–684.

    Article  PubMed  Google Scholar 

  • Ozerov, M. Y., A. E. Veselov, J. Lumme, C. R. Primmer & P. Moran, 2012. “Riverscape” genetics: river characteristics influence the genetic structure and diversity of anadromous and freshwater Atlantic salmon (Salmo salar) populations in northwest Russia. Canadian Journal of Fisheries and Aquatic Sciences 69(12): 1947–1958.

    Article  Google Scholar 

  • Pecchia, T., A. Gagliardo, C. Filannino, P. Ioalè & G. Vallortigara, 2013. Navigating Through an Asymmetrical Brain: Lateralisation and Homing in Pigeon Behavioral Lateralization in Vertebrates. Springer, Berlin: 107–124.

    Google Scholar 

  • 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(2): 215–225.

    Article  Google Scholar 

  • Perrier, C., R. Guyomard, J. L. Bagliniere & G. Evanno, 2011. Determinants of hierarchical genetic structure in Atlantic salmon populations: environmental factors vs. anthropogenic influences. Molecular Ecology 20(20): 4231–4245.

    Article  PubMed  Google Scholar 

  • Pritchard, J. K., M. Stephens & P. Donnelly, 2000. Inference of population structure using multilocus genotype data. Genetics 155(2): 945–959.

    PubMed Central  CAS  PubMed  Google Scholar 

  • Raymond, M. & F. Rousset, 1995. Genepop (Version-1.2) – population-genetics software for exact tests and ecumenicism. Journal of Heredity 86(3): 248–249.

    Google Scholar 

  • Ritland, K., 1996. Estimators for pairwise relatedness and individual inbreeding coefficients. Genetical Research 67(2): 175–186.

    Article  Google Scholar 

  • 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: 401–417.

    Article  PubMed  Google Scholar 

  • Saied, A., F. Maffucci, S. Hochscheid, S. Dryag, B. Swayeb, M. Borra, A. Ouerghi, G. Procaccini & F. Bentivegna, 2012. Loggerhead turtles nesting in Libya: an important management unit for the Mediterranean stock. Marine Ecology Progress Series 450: 207–218.

    Article  Google Scholar 

  • Sanches, A., P. M. Galetti Jr, F. Galzerani, J. Derazo, B. Cutilak-Bianchi & T. Hatanaka, 2012. Genetic population structure of two migratory freshwater fish species (Brycon orthotaenia and Prochilodus argenteus) from the São Francisco River in Brazil and its significance for conservation. Latin American Journal of Aquatic Research 40(1): 177.

    Article  Google Scholar 

  • Sato, Y. & H. P. Godinho, 2004. Migratory fishes of the São Francisco River. In Carolsfeld, J., B. Harvey, C. Ross & A. Baer (eds), Migratory Fishes of South America: Biology, Fisheries and Conservation Status. IDRC, Victoria: 195–232.

    Google Scholar 

  • Schuelke, M., 2000. An economic method for the fluorescent labeling of PCR fragments. Nature Biotechnology 18(2): 233–234.

    Article  CAS  PubMed  Google Scholar 

  • Shamblin, B. M., K. A. Bjorndal, A. B. Bolten & C. J. Nairn, 2012. Natal homing by an adult male green turtle at Tortuguero, Costa Rica. Marine Turtle Newsletter 134: 21–22.

    Google Scholar 

  • 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(3): 535–538.

    Article  Google Scholar 

  • Verspoor, E., 1997. Genetic diversity among Atlantic salmon (Salmo salar L.) populations. ICES Journal of Marine Science: Journal du Conseil 54(6): 965–973.

    Google Scholar 

  • Wang, J., 2011. COANCESTRY: a program for simulating, estimating and analysing relatedness and inbreeding coefficients. Molecular Ecology Resources 11(1): 141–145.

    Article  PubMed  Google Scholar 

  • Wasko, A. P. & P. M. Galetti Jr, 2002. RAPD analysis in the Neotropical fish Brycon lundii: genetic diversity and its implications for the conservation of the species. Hydrobiologia 474(1–3): 131–137.

    Article  Google Scholar 

  • Weir, B. & C. C. Cockerham, 1984. Estimating F-statistics for the analysis of population structure. Evolution 38: 1358–1370.

    Article  Google Scholar 

  • Wright, S., 1978. Evolution and the Genetics of Populations. Variability Within and Among Natural Populations, Vol. 4. University of Chicago Press, Chicago.

    Google Scholar 

  • Yazbeck, G. & E. Kalapothakis, 2007. Isolation and characterization of microsatellite DNA in the piracema fish Prochilodus lineatus (Characiformes). Genetics and Molecular Research 6(4): 1026–1034.

    CAS  PubMed  Google Scholar 

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Acknowledgments

The authors are very thankful to the Brazilian agencies Fundação de Amparo à Pesquisa do Estado de São Paulo—FAPESP (2009/13164-6)—and Conselho Nacional de Desenvolvimento Científico e Tecnológico (304440/2009-4) for financial support. Instituto Chico Mendes de Conservação da Biodiversidade and Ministério do Meio Ambiente are also acknowledged for providing fish collection authorization.

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  1. Laboratório de Biodiversidade Molecular e Conservação, Departamento de Genética e Evolução, Universidade Federal de São Carlos, Rodovia Washington Luís, Km 235, São Carlos, SP, CEP: 13565-905, Brazil

    Alline Braga-Silva & Pedro Manoel Galetti Jr.

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  1. Alline Braga-Silva
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  2. Pedro Manoel Galetti Jr.
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Correspondence to Alline Braga-Silva.

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Braga-Silva, A., Galetti, P.M. Evidence of isolation by time in freshwater migratory fish Prochilodus costatus (Characiformes, Prochilodontidae). Hydrobiologia 765, 159–167 (2016). https://doi.org/10.1007/s10750-015-2409-8

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