Environmental Biology of Fishes

, Volume 100, Issue 9, pp 1047–1067 | Cite as

Species complex delimitation and patterns of population structure at different geographic scales in Neotropical silver catfish (Rhamdia: Heptapteridae)

  • Néstor Ríos
  • Carmen Bouza
  • Verónica Gutiérrez
  • Graciela García
Article

Abstract

The Neotropical catfish genus Rhamdia inhabits rivers and lakes from Mexico to Argentina. Previous studies have found that the taxonomy of this genus, as well as that of R. quelen, remains controversial. The present study aims to contribute to the understanding of Rhamdia systematics by delimiting putative species, and to elucidate the pattern of genetic differentiation of Rhamdia at different geographic levels within the cis-andean region. Species boundaries were defined by Generalized Mixed Yule Coalescent and Automatic Barcode Gap Discovery methods, and by phylogenetic analyses of cytochrome b (cyt b) sequences. Moreover, we performed phylogeographic analyses based on cyt b sequences and microsatellite markers. Patterns of differentiation were analyzed at three nested geographic levels: in the main cis-andean basins (macrogeographic scale); in the second major Neotropical basin system (mesogeographic scale), which encompasses La Plata basin, Patos-Merin basin, and the coastal lagoons draining to SW Atlantic Ocean; and finally, in the three most important coastal lagoons for artisanal fisheries in Uruguay (microgeographic scale). Sixteen species were found within Rhamdia, divided into two clades (cis- and trans-andean clades), each composed of eight putative species. Cis-andean Rhamdia species have probably diverged due to vicariance events occurring between and within basins since late Miocene-Pleistocene. Microgeographic scale analysis based on cyt b and microsatellite data revealed a high genetic structuring among the studied coastal lagoons. Mitochondrial and microsatellite markers enabled to identify three different populations, corresponding to the three coastal lagoons analyzed, which would have diverged recently and could be considered as different Management Units.

Keywords

Phylogeography Rhamdia quelen Conservation units Microsatellite loci Mitochondrial marker 

References

  1. Akaike H (1974) A new look at the statiscal model identification. IEEE Trans Autom Contr 19:716–723CrossRefGoogle Scholar
  2. Albert JS, Reis RE (2011) Historical biogeography of Neotropical freshwater fishes. University of California Press, BerkeleyCrossRefGoogle Scholar
  3. Bandelt HJ, Forster P, Röhl A (1999) Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol 16:37–48CrossRefPubMedGoogle Scholar
  4. Bockmann FA, Guazzelli GM (2003) Heptapteridae (Heptapterids). In: Reis RE, Kullander SO, Ferraris CJ Jr (eds) Checklist of the freshwater fishes of south and central America. EDIPUCRS, Porto Alegre, pp 406–431Google Scholar
  5. Bonilla S, Conde D, Aubriot L, Rodríguez-Gallego L, Piccini C, Meerhoff E, Rodríguez-Graña L, Calliari D, Gómez P, Machado I, Britos A (2006) Structured process of biological communities in coastal lagoons of Uruguay. In: Menafra R, Rodríguez-Gallego L, Scarabino F, Conde D (eds) Bases para la Conservación y el Manejo de la Costa Uruguaya. Vida Silvestre Uruguay, Montevideo, pp 611–630Google Scholar
  6. Bouckaert R, Heled J, Kühnert D, Vaughan TG, Wu CH, Xie D, Suchard MA, Rambaut A, Drummond AJ (2014) BEAST 2: a software platform for Bayesian evolutionary analysis. PLoS Comput Biol 10:e1003537CrossRefPubMedPubMedCentralGoogle Scholar
  7. Cardoso YP, Montoya-Burgos JI (2009) Unexpected diversity in the catfish Pseudancistrus brevispinis reveals dispersal routes in a Neotropical center of endemism: the Guyanas region. Mol Ecol 4:947–964CrossRefGoogle Scholar
  8. Cavallotto JL, Violante RA, Colombo F (2005) Evolución y cambios ambientales de la llanura costera de la cabecera del río de la Plata. Rev Asoc Geol Argent 60:353–367Google Scholar
  9. Chistiakov DA, Hellemans B, Volckaert FAM (2006) Microsatellites and their genomic distribution, evolution, function and applications: a review with special reference to fish genetics. Aquaculture 255:1–29CrossRefGoogle Scholar
  10. Concheiro Pérez GA, Říčan O, Ortí G, Bermingham E, Doadrio I, Zardoya R (2007) Phylogeny and biogeography of 91 species of heroine cichlids (Teleostei: Cichlidae) based on sequences of the cytochrome b gene. Mol Phylogenet Evol 43:91–110CrossRefGoogle Scholar
  11. Darriba D, Taboada GL, Doallo R, Posada D (2012) jModelTest 2: more models, new heuristics and parallel computing. Nat Methods 9:772–772CrossRefPubMedPubMedCentralGoogle Scholar
  12. de Pinna MCC (1998) Phylogenetic relationships of neotropical Siluriformes (Teleostei: Ostariophysi): historical overview and synthesis of hypotheses. In: Malabarba LR, Reis RE, Vari RP, Lucena ZM, Lucena CAS (eds) Phylogeny and classification of Neotropical fishes. Edipucrs, Porto Alegre, pp 279–330Google Scholar
  13. Drummond AJ, Rambaut A (2007) BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol Biol 7:214CrossRefPubMedPubMedCentralGoogle Scholar
  14. Earl DA, vonHoldt BM (2012) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genet Resour 4:359–361Google Scholar
  15. Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14:2611–2620CrossRefPubMedGoogle Scholar
  16. Excoffier L, Lischer HEL (2010) Arlequin suite ver. 3.5: a new series of programs to perform population genetics analyses under Linux and windows. Mol Ecol Resour 10:564–567CrossRefPubMedGoogle Scholar
  17. Ezard T, Fujisawa T, Barraclough TG (2009) Splits: SPecies' LImits by threshold statistics R package version 10-14/r31. https://r-forge.r-project.org/projects/splits/. Accessed Jan 2017
  18. Fu YX (1997) Statistical test of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147:915–925PubMedPubMedCentralGoogle Scholar
  19. Garavello JC, Shibatta OA (2016) Reappraisal of Rhamdia branneri Haseman, 1911 and R. voulezi Haseman, 1911 (Siluriformes: Heptapteridae) from the rio Iguaçu with notes on their morphometry and karyotype. Neotrop Ichthyol 14:e140111CrossRefGoogle Scholar
  20. 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. Accessed Sept 2016
  21. Guindon S, Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52:696–704CrossRefPubMedGoogle Scholar
  22. Hardman M (2005) The phylogenetic relationships among non-diplomystid cat W shes as inferred from mitochondrial cytochrome b sequences; the search for the ictalurid sister taxon ( Otophysi : Siluriformes). Mol Phylogenet Evol 37:700–720CrossRefPubMedGoogle Scholar
  23. Hasegawa M, Kishino H, Yano T (1985) Dating of the human-ape splitting by a molecular clock of mitochondrial DNA. J Mol Evol 22:160–174CrossRefPubMedGoogle Scholar
  24. Hernandez CL, Ortega-Lara A, Sánchez-Garcés GC, Alford MH (2015) Genetic and morphometric evidence for the recognition of several recently synonymized species of trans-andean Rhamdia (Pisces: Siluriformes: Heptapteridae). Copeia 103:563–579CrossRefGoogle Scholar
  25. Hubert N, Duponchelle F, Nuñez J, Garcia-Davila C, Paugy D, Renno J-F (2007) Phylogeography of the piranha genera Serrasalmus and Pygocentrus: implications for the diversification of the Neotropical ichthyofaunal. Mol Ecol 16:2115–2136CrossRefPubMedGoogle Scholar
  26. Hurd LE, Sousa RGC, Siqueira-Souza FK, Cooper GJ, Kahn JK, Freitas CEC (2016) Amazon floodplain fish communities: habitat connectivity and conservation in a rapidly deteriorating environment. Biol Conserv 195:118–127CrossRefGoogle Scholar
  27. Kekkonen M, Mutanen M, Kaila L, Nieminem M, Hebert PDN (2015) Delineating species with DNA barcodes: a case of taxon dependent method performance in moths. PLoS One 10:e0122481CrossRefPubMedPubMedCentralGoogle Scholar
  28. Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874CrossRefPubMedGoogle Scholar
  29. Lanave C, Preparata C, Saccone C, Serio G (1984) A new method for calculating evolutionary substitution rates. J Mol Evol 20:86–93CrossRefPubMedGoogle Scholar
  30. Librado P, Rozas J (2009) DnaSP v5, a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452CrossRefPubMedGoogle Scholar
  31. Loureiro M, Zarucki M, González I, Vidal N, Fabiano G. 2013. Peces continentales. In: Soutullo A, Clavijo C, Martínez-Lanfranco JA (eds) Especies prioritarias para la conservación en Uruguay. Vertebrados, moluscos continentales y plantas vasculares. SNAP/DINAMA/MVOTMA y DICYT/MEC, Montevideo, pp 91–112Google Scholar
  32. Lundberg JG, Marshall LG, Guerrero J, Horton B, Malabarba MCSL, Wesselingh F (1998) The stage for Neotropical fish diversification: a history of tropical South American rivers. In: Malabarba LR, Reis RE, Vari RP, Lucena ZMS, Lucena CAS (eds) Phylogeny and classification of Neotropical fishes. EDIPUCRS, Porto Alegre, pp 13–48Google Scholar
  33. Ma C, Cheng Q, Zhang Q, Zhuang P, Zhao Y (2010) Genetic variation of Coilia ectenes (Clupeiformes: Engraulidae) revealed by the complete cytochrome b sequences of mitochondrial DNA. J Exp Mar Bio Ecol 385:14–19CrossRefGoogle Scholar
  34. Martinez JF, Lui RL, Blanco DR, Traldi JB, Silva LF, Venere PC, Souza IL, Moreira-Filho O (2011) Comparative cytogenetics of three populations from the Rhamdia quelen species complex (Siluriformes, Heptapteridae) in two Brazilian hydrographic basins. Caryologia 64:121–128CrossRefGoogle Scholar
  35. Medrano JF, Aasen E, Sharrow L (1990) DNA extraction from nucleated red blood cells. BioTechniques 8:43PubMedGoogle Scholar
  36. Minin V, Abdo Z, Joyce P, Sullivan J (2003) Performance-based selection of likelihood models for phylogeny estimation. Syst Biol 52:674–683CrossRefPubMedGoogle Scholar
  37. Moeser AA, Bermingham E (2005) Isolation and characterization of eight microsatellite loci for the Neotropical freshwater catfish Pimelodella chagresi (Teleostei: Pimelodidae). Mol Ecol Notes 5:363–365CrossRefGoogle Scholar
  38. Moritz C (1994) Defining ‘evolutionarily significant units’ for conservation. Trends Ecol Evol 9:373–375CrossRefPubMedGoogle Scholar
  39. Nylander JAA (2004) MrModeltest v2. Program distributed by the author. Evolutionary Biology Centre, Uppsala University, UppsalaGoogle Scholar
  40. Palumbi S, Martin A, Romano S, McMillan WO, Stice L, Grabowski G (1991) The simple fool’s guide to PCR. Department of Zoology and Kewalo Marine Laboratory, Univ. Hawaii, HonoluluGoogle Scholar
  41. Paradis E, Claude J, Strimmer K (2004) APE: analyses of phylogenetics and evolution in R language. Bioinformatics 20:289–290CrossRefPubMedGoogle Scholar
  42. Perdices A, Bermingham E, Montilla A, Doadrio I (2002) Evolutionary history of the genus Rhamdia (Teleostei: Pimelodidae) in Central America. Mol Phylogenet Evol 25:172–189CrossRefPubMedGoogle Scholar
  43. Pereira LHG, Foresti F, Oliveira C (2009) Genetic structure of the migratory catfish Pseudoplatystoma corruscans (Siluriformes: Pimelodidae) suggests homing behaviour. Ecol Freshw Fish 18:215–255CrossRefGoogle Scholar
  44. Pons J, Barraclough TG, Gomez-Zurita J, Cardoso A, Duran DP, Hazell S, Kamoun S, Sumlin WD, Vogler AP (2006) Sequence-based species delimitation for the DNA taxonomy of Undescribed insects. Syst Biol 55:595–609CrossRefPubMedGoogle Scholar
  45. Pritchard JK, Stephens P, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959PubMedPubMedCentralGoogle Scholar
  46. Puillandre N, Lambert A, Brouillet S, Achaz G (2012) ABGD, automatic barcode gap discovery for primary species delimitation. Mol Ecol 21:1864–1877CrossRefPubMedGoogle Scholar
  47. Rambaut A, Drummond AJ (2007a) Tracer v1.5. Computer program and documentation distributed by the authors. http://tree.bio.ed.ac.uk/software/tracer/. Accessed Sept 2016
  48. Rambaut A, Drummond AJ (2007b) TreeAnnotator v 1.5.4. Program and documentation distributed by the author. Website http://beast.bio.ed.ac.uk/TreeAnnotator/. Accessed Sept 2016
  49. Revaldaves E, Pereira LHG, Foresti F, Oliveira C (2005) Isolation and characterization of microsatellite loci in Pseudoplatystoma corruscans (Siluriformes: Pimelodidae) and cross-species amplification. Mol Ecol Notes 5:463–465CrossRefGoogle Scholar
  50. Ribolli J, Zaniboni-Filho E (2009) Individual contributions to pooled-milt fertilizations of silver catfish Rhamdia quelen. Neotrop Ichthyol 7:629–634CrossRefGoogle Scholar
  51. Ronquist F, Teslenko M, Van Der Mark P, Ayres DL, Darling A, Höhna S, Larget B, Liu L, Suchard MA, Huelsenbeck JP (2012) Mrbayes 3.2: efficient bayesian phylogenetic inference and model choice across a large model space. Syst Biol 61:539–542CrossRefPubMedPubMedCentralGoogle Scholar
  52. Rousset F (2008) GENEPOP’007: a complete re-implementation of the GENEPOP software for windows and Linux. Mol Ecol Resour 8:103–106CrossRefPubMedGoogle Scholar
  53. Schwarz G (1978) Estimating the dimension of a model. Ann Statist 6:461–464CrossRefGoogle Scholar
  54. Silfvergrip AMC (1996) A systematic revision of the Neotropical catfish genus Rhamdia (Teleostei Pimelodidae). Thesis, Swedish Museum of Natural History, StockholmGoogle Scholar
  55. Singh M, Lakra WS, Bahuguna SN (2012) Cytochrome b gene sequence divergence of seven sisorid species of catfish genus Glyptothorax (siluriformes, sisoridae) from India. Mol Biol Rep 39:4275–4282CrossRefPubMedGoogle Scholar
  56. So N, Maes GE, Volckaert FAM (2006) High genetic diversity in cryptic populations of the migratory sutchi catfish Pangasianodon hypophthalmus in the Mekong River. Heredety 96:166–174CrossRefGoogle Scholar
  57. Sugiura N (1978) Further analysis of the data by akaike’s information criterion and the finite corrections. Commun Stat Theory Methods 7:13–26CrossRefGoogle Scholar
  58. Sullivan JP, Lundberg JG, Hardman M (2006) A phylogenetic analysis of the major groups of catfishes (Teleostei: Siluriformes) using rag1 and rag2 nuclear gene sequences. Mol Phylogenet Evol 41:636–662Google Scholar
  59. Swofford DL (2002) PAUP* phylogenetic analysis using parsimony (* and other methods). Sinauer Associates, Inc., SunderlandGoogle Scholar
  60. Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585–595PubMedPubMedCentralGoogle Scholar
  61. Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680CrossRefPubMedPubMedCentralGoogle Scholar
  62. Van Oosterhout C, Hutchinson WF, Wills DPM, Shipley P (2004) MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Mol Notes 4:535–538CrossRefGoogle Scholar
  63. Vaz BS, Cerqueira GM, Silva JC, Manzke VHB, Moreira CGA, Moreira HLM (2010) Sequence analysis of the growth hormone gene of the South American catfish Rhamdia quelen. Genet Mol Res 9:2184–2190CrossRefPubMedGoogle Scholar
  64. Zhang J, Hanner R (2012) Molecular approach to the identification of fish in the South China Sea. PLoS One 7:1–9Google Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2017

Authors and Affiliations

  • Néstor Ríos
    • 1
    • 2
  • Carmen Bouza
    • 3
  • Verónica Gutiérrez
    • 1
  • Graciela García
    • 1
  1. 1.Sección Genética Evolutiva, Facultad de CienciasUdelaRMontevideoUruguay
  2. 2.Museo Nacional de Historia NaturalMontevideoUruguay
  3. 3.Departamento de Zoología, Genética y Antropología Física, Facultad de Veterinaria, Campus de LugoUniversidade de Santiago de CompostelaLugoSpain

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