Environmental Biology of Fishes

, Volume 100, Issue 1, pp 1–16 | Cite as

Population genetic structure of the Amazonian black flannelmouth characin (Characiformes, Prochilodontidae: Prochilodus nigricans Spix & Agassiz, 1829): contemporary and historical gene flow of a migratory and abundant fishery species

  • Valéria Nogueira Machado
  • Stuart C. Willis
  • Aylton S. Teixeira
  • Tomas Hrbek
  • Izeni Pires Farias


In the present study, sequences of the mtDNA control region (834 bp) were analyzed from 337 specimens of Prochilodus nigricans from sites along the main channel of the Amazonas River and three major tributaries, Madeira, Purus, and Juruá. The results of the analysis of molecular variance revealed that a large part of the genetic variation occurred within the populations analyzed (~85 %). Analysis with SAMOVA and Barriers suggested that the upper Madeira River and Purus Rivers had diverged genetically from the other samples, indicating restricted gene flow among these areas, while sites within the remaining range exhibited relatively little population structure. The high degree of structuring observed in the Madeira River basin population may be attributed to the presence of rapids along its upper course, while the genetic divergence found in the upper Purus River suggests historical connection between the upper Purus and upper Madeira Rivers followed by slow genetic drift due to large effective population sizes. However, given the life history and hypothesized evolutionary strategy of this species, we urge caution in interpreting that this targeted species is not at risk of overexploitation due to contemporary abundance. In order to preserve genetic diversity, we recommend enforcement of management regimes for regional stocks.


Curimatã Control region Amazon basin 



This research was supported by the MCT/CNPq/PPG7 557090/2005-9, CNPq/CT-Amazonia 554057/2006-9 and CNPq/ CT-Amazonia 575603/2008-9. Brazilian permits for field collection and molecular analyses were given by IBAMA/SISBIO 11325-1. TH and IPF were supported by a Bolsa de Pesquisa scholarship from CNPq during the study and VM by a CNPq fellowship. This study is part of VM’s Master’s thesis in the Fisheries Sciences in the Tropics graduate program of UFAM.

Supplementary material

10641_2016_547_Fig4_ESM.gif (669 kb)
Supplemental Figure 1.

Haplotype network of Prochilodus nigricans haplotypes estimated using Network. Circle sizes correspond to the number of observations, and missing haplotypes remain unfilled. Shading refers to the locality in which a haplotype was observed. (GIF 668 kb)

10641_2016_547_MOESM1_ESM.tif (1.8 mb)
High resolution image (TIFF 1824 kb)


  1. Amado MV, Hrbek T, Farias IP (2011) A molecular perspective on systematics, taxonomy and classification Amazonian discus fishes of the genus Symphysodon. Int J Evol Biol 2011:360654CrossRefPubMedPubMedCentralGoogle Scholar
  2. Araújo-Lima CARM, Ruffino, ML (2004) Migratory fishes of the Brazilian Amazon. In: Carolsfield J, Harvey B, Ross C, Baer, A (eds) Migratory Fishes of South America. Biology, Fisheries, and Conservation Status. Co-published by World Fisheries Trust/ World Bank/International Development Research Center, pp 233–302Google Scholar
  3. Barbarino Duque A, Taphorn DC, Winemiller KO (1998) Ecology of the coporo, Prochilodus mariae (Characiformes, Prochilodontidae), and status of annual migrations in western Venezuela. Environ Biol Fish 53:33–46CrossRefGoogle Scholar
  4. Barthem RB, Fabré NN (2003) Biologia e diversidade dos recursos pesqueiros da Amazônia. In: Ruffino ML (ed) A Pesca e os Recursos Pesqueiros na Amazônia Brasileira. ProVarzea, Manaus, pp. 11–55Google Scholar
  5. Barthem RB, Goulding M (2007) An unexpected ecosystem: the Amazon as revealed by fisheries. Amazon Conservation Association and Missouri Botanical Garden Press, Saint Louis, MissouriGoogle Scholar
  6. Batista JS, Alves-Gomes JA (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. Genet Mol Res 5:723–740PubMedGoogle Scholar
  7. Batista VS, Petrere M Jr (2003) Characterization of the commercial fish production landed at Manaus, Amazonas state, Brazil. Acta Amaz 33:53–66CrossRefGoogle Scholar
  8. Bayley PB, Petrere Jr M (1989) Amazon fisheries: assessment methods, current status and management options. In: Dodge DP (ed) Proceedings of the International Large River Symposium. Proceedings of the International Large River Symposium. Can Spec Publ Fish Aquat Sci, 106, pp 385–398Google Scholar
  9. Beerli P (2006) Comparison of Bayesian and maximum-likelihood inference of population genetic parameters. Bioinformatics 22:341–345CrossRefPubMedGoogle Scholar
  10. Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Ser B Stat Methodol 57:289–300Google Scholar
  11. Bouckaert R, Heled J, Kühnert D, Vaughan T, Wu C-H, Xie D, Suchard MA, Rambaut A, Drummond AJ (2014) BEAST 2: a software platform for Bayesian evolutionary analysis. PLoS Comput Biol 10:e1003537CrossRefPubMedPubMedCentralGoogle Scholar
  12. Burt A, Kramer DL, Nakatsuru K, Spry C (1988) The tempo of reproduction in Hyphessobrycon pulchripinnis (Characidae), with a discussion on the biology of ‘multiple spawning’in fishes. Environ Biol Fish 22:15–27CrossRefGoogle Scholar
  13. Carvajal-Vallejos FM, Duponchelle F, Desmarais E, Cerqueira F, Querouil S, Nuñez J, García-Dávila C, Renno J-F (2014) Genetic structure in the Amazonian catfish Brachyplatystoma rousseauxii: influence of life history strategies. Genetica 142:323–336CrossRefPubMedGoogle Scholar
  14. Castro RMC (1993) Prochilodus britskii, a new species of prochilodontid fish (Ostariophysi: Characiformes), from the Rio Apiaca, Rio Tapajos system, Mato Grosso, Brazil. Proc Biol Soc Wash 106:57–62Google Scholar
  15. Colatreli OP, Meliciano NV, Toffoli D, Farias IP, Hrbek T (2012) Deep phylogenetic divergence and lack of taxonomic concordance in species of Astronotus (Cichlidae). Int J Evol Biol 2012:915265CrossRefPubMedPubMedCentralGoogle Scholar
  16. Collins SM, Bickford N, McIntyre PB, Coulon A, Ulseth AJ, Taphorn DC, Flecker AS (2013) Population structure of a Neotropical migratory fish: contrasting perspectives from genetics and otolith microchemistry. Trans Am Fish Soc 142:1192–1201CrossRefGoogle Scholar
  17. Darriba D, Taboada GL, Doallo R, Posada D (2012) jModelTest 2: more models, new heuristics and parallel computing. Nat Methods 9:772–772CrossRefPubMedPubMedCentralGoogle Scholar
  18. Donaldson KA, Wilson RR Jr (1999) Amphi-Panamic germinates of Snook (Percoidei: Centropomidae) provide a calibration of the divergence rate in the mitochondrial DNA control region of fishes. Mol Phylogenet Evol 13:208–213CrossRefPubMedGoogle Scholar
  19. Doyle JJ, Doyle JL (1987) A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phys Bull 19:11–15Google Scholar
  20. Drummond AJ, Rambaut A (2007) BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol Biol 7:214CrossRefPubMedPubMedCentralGoogle Scholar
  21. Dunn OJ (1961) Multiple comparisons among means. J Am Stat Assoc 56:52–64CrossRefGoogle Scholar
  22. Dupanloup I, Schneider S, Excoffier L (2002) A simulated annealing approach to define the genetic structure of populations. Mol Ecol 11:2571–2581CrossRefPubMedGoogle Scholar
  23. Edwards SV, Beerli P (2000) Perspective: gene divergence, population divergence, and the variance in coalescence time in phylogeographic studies. Evolution 54:1839–1854PubMedGoogle Scholar
  24. Espurt N, Baby P, Brusset S, Roddaz M, Hermoza W, Barbarand J (2010) The Nazca Ridge and uplift of the Fitzcarrald Arch: implications for regional geology in northern South America. In: Hoorn C, Wesselingh FP (eds) Amazonia: Landscape and Species Evolution: A Look into the Past. Wiley-Blackwell; pp 89–100Google Scholar
  25. 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
  26. Excoffier L, Smouse PE, Quattro JM (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131:479–491PubMedPubMedCentralGoogle Scholar
  27. Farias IP, Hrbek T (2008) Patterns of diversification in the discus fishes (Symphysodon spp. Cichlidae) of the Amazon basin. Mol Phylogenet Evol 49:32–43CrossRefPubMedGoogle Scholar
  28. Farias IP, Torrico JP, García-Dávila C, Santos MCF, Hrbek T, Renno J-F (2010) Are rapids a barrier for floodplain fishes of the Amazon basin? A demographic study of the keystone floodplain species Colossoma macropomum (Teleostei: Characiformes). Mol Phylogenet Evol 56:1129–1135CrossRefPubMedGoogle Scholar
  29. Felsenstein J (1981) Evolutionary trees from DNA sequences: a maximum likelihood approach. J Mol Evol 17:368–376CrossRefPubMedGoogle Scholar
  30. Flecker AS (1996) Ecosystem engineering by a dominant detritivore in a diverse tropical stream. Ecology 77:1845–1854CrossRefGoogle Scholar
  31. Flowers JM, Schroeter SC, Burton RS (2002) The recruitment sweepstakes has many winners: genetic evidence from the sea urchin Strongylocentrotus purpuratus. Evolution 56:1445–1453CrossRefPubMedGoogle Scholar
  32. Frederico RG, Farias IP, Araújo MLG, Charvet-Almeida P, Alves-Gomes JA (2012) Phylogeography and conservation genetics of the Amazonian freshwater stingray Paratrygon aiereba Müller & Henle, 1841 (Chondrichthyes: Potamotrygonidae). Neotrop Ichthyol 10:71–80CrossRefGoogle Scholar
  33. Fu Y-X (1997) Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147:915–925PubMedPubMedCentralGoogle Scholar
  34. Funk WC, McKay JK, Hohenlohe PA, Allendorf FW (2012) Harnessing genomics for delineating conservation units. Trends Ecol Evol 27:489–496CrossRefPubMedPubMedCentralGoogle Scholar
  35. Geisler R, Annibal S (1987) Ecology of the cardinal tetra, Paracheirodon axelrodi (Pisces, Characoidea), in the River Basin of the Rio Negro, Brazil, as well as breeding related factors. Trop. Fish Hobbyist 35:66–87Google Scholar
  36. Genner MJ, Seehausen O, Lunt DH, Joyce DA, Shaw PW, Carvalho GR, Turner GF (2007) Age of cichlids: new dates for ancient lake fish radiations. Mol Biol Evol 24:1269–1282CrossRefPubMedGoogle Scholar
  37. Ghalambor CK, McKay JK, Carroll SP, Reznick DN (2007) Adaptive versus non-adaptive phenotypic plasticity and the potential for contemporary adaptation in new environments. Funct Ecol 21:394–407CrossRefGoogle Scholar
  38. Goulding M (1979) Ecologia de Pesca do Rio Madeira. INPA, ManausGoogle Scholar
  39. Goulding M (1981) Man and fisheries on an Amazon frontier. Dr. W. Junk Publishers, The HagueCrossRefGoogle Scholar
  40. Gradado-Lorencio C, Araújo-Lima CARM, Lobón-Cerviá J (2005) Abundance: distribution relationships in fish assembly of the Amazonas floodplain lakes. Ecography 28:515–520CrossRefGoogle Scholar
  41. Gravena W, Farias IP, da Silva MNF, da Silva VMF, Hrbek T (2014) Looking to the past and the future: were the Madeira River rapids a geographic barrier to the boto (Cetacea: Iniidae)? Conserv Genet 15:619–629Google Scholar
  42. Gravena W, da Silva VMF, da Silva MNF, Farias IP, Hrbek T (2015) Living between rapids: genetic structure and hybridization in botos (Cetacea: Iniidae: Inia spp.) of the Madeira River, Brazil. Biol J Linn Soc 114:764–777CrossRefGoogle Scholar
  43. Hall T (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98Google Scholar
  44. Hedrick PW (2006) Genetic polymorphism in heterogeneous environments: the age of genomics. Annu Rev Ecol Syst 37:67–93CrossRefGoogle Scholar
  45. Hellberg ME, Burton RS, Neigel JE, Palumbi SR (2002) Genetic assessment of connectivity among marine populations. Bull Mar Sci 70:273–290Google Scholar
  46. Heller R, Chikhi L, Siegismund HR (2013) The confounding effect of population structure on Bayesian skyline plot inferences of demographic history. PLoS One 8:e62992CrossRefPubMedPubMedCentralGoogle Scholar
  47. Ho SYW, Phillips MJ, Cooper A, Drummond AJ (2005) Time dependency of molecular rate estimates and systematic overestimation of recent divergence times. Mol Biol Evol 22:1561–1568CrossRefPubMedGoogle Scholar
  48. Hoorn C, Wesselingh FP, ter Steege H, Bermudez MA, Mora A, Sevink J, Sanmartín I, Sanchez-Meseguer A, Anderson CL, Figueiredo JP, Jaramillo C, Riff D, Negri FR, Hooghiemstra H, Lundberg J, Stadler T, Särkinen T, Antonelli A (2010) Amazonia through time: Andean uplift, climate change, landscape evolution, and biodiversity. Science 330:927–931CrossRefPubMedGoogle Scholar
  49. Hrbek T, Farias IP, Crossa M, Sampaio I, Porto JIR, Meyer A (2005) Population genetic analysis of Arapaima gigas, one of the largest freshwater fishes of the Amazon basin: implications for its conservation. Anim Conserv 8:297–308CrossRefGoogle Scholar
  50. Hrbek T, Crossa M, Farias IP (2007) Conservation strategies for Arapaima gigas (Schinz, 1822) and the Amazonian várzea ecosystem. Braz J Biol 67:909–917CrossRefPubMedGoogle Scholar
  51. Hrbek T, Vasconcelos WR, Rebêlo GH, Farias IP (2008) Phylogenetic relationships of south American alligatorids and the caiman of Madeira River. J Exp Zool Part A Ecol Genet Physiol 309A:588–599CrossRefGoogle Scholar
  52. Jennings S, Kaiser MJ (1998) The effects of fishing on marine ecosystems. Adv Mar Biol 34:201–352CrossRefGoogle Scholar
  53. Junk WJ, Bayley PB, Sparks R (1989) The flood pulse concept in river-floodplain systems. Can Spec Publ Fish Aquat Sci 106:110–127Google Scholar
  54. Junk WJ, Soares MGM, Saint-Paul U (1997) The fish. In: Junk WJ (ed) The Central Amazon: ecology of a pulsing system. Springer, Berlin Heidelberg, pp. 385–408CrossRefGoogle Scholar
  55. Kimura M (1969) The number of heterozygous nucleotides sites maintained in a finite population due to the steady flux of mutations. Genetics 61:893–903PubMedPubMedCentralGoogle Scholar
  56. Levine H (1953) Genetic equilibrium when more than one ecological niche is available. Am Nat 87:331–333CrossRefGoogle Scholar
  57. Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452CrossRefPubMedGoogle Scholar
  58. Lima ÁC, Araújo-Lima CARM (2004) The distributions of larval and juvenile fishes in Amazonian rivers of different nutrient status. Freshw Biol 49:787–800CrossRefGoogle Scholar
  59. Lovejoy NR, Collette BB (2001) Phylogenetic relationships of new world needlefishes (Teleostei: Belonidae) and the biogeography of transitions between marine and freshwater habitats. Copeia 2001:324–338CrossRefGoogle Scholar
  60. Manni F, Guerard E, Heyer E (2004) Geographic patterns of (genetic, morphologic, linguistic) variation: how barriers can be detected by using Monmonier’s algorithm. Hum Biol 76:173–190CrossRefPubMedGoogle Scholar
  61. Needleman SB, Wunsch CD (1970) A general method applicable to the search for similarities in the amino acid sequence of two proteins. J Mol Biol 48:443–453CrossRefPubMedGoogle Scholar
  62. Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New YorkGoogle Scholar
  63. Nei M, Li W-H (1979) Mathematical model for studying genetic variation in terms of restriction endonoclueases. Proc Natl Acad Sci U S A 76:5269–5273CrossRefPubMedPubMedCentralGoogle Scholar
  64. Ochoa LE, Pereira LHG, Costa-Silva GJ, Roxo FF, Batista JS, Formiga K, Foresti F, Oliveira C (2015) Genetic structure and historical diversification of catfish Brachyplatystoma platynemum (Siluriformes: Pimelodidae) in the Amazon basin with implications for its conservation. Ecol Evol 5:2005–2020Google Scholar
  65. Pearse DE, Arndt AD, Valenzuela N, Miller BA, Cantarelli VH, Sites JW (2006) Estimating population structure under nonequilibrium conditions in a conservation context: continent-wide population genetics of the giant Amazon River turtle, Podocnemis expansa (Chelonia; Podocnemididae). Mol Ecol 15:985–1006CrossRefPubMedGoogle Scholar
  66. Petrere M Jr, Barthem RB, Agudelo Cordoba E, Corrales B (2004) Review of the large catfish fisheries in the upper Amazon and the stock depletion of piraíba (Brachyplatystoma filamentosum Lichtenstein). Rev Fish Biol Fish 14:403–414CrossRefGoogle Scholar
  67. Pinsky ML, Palumbi SR (2014) Meta-analysis reveals lower genetic diversity in overfished populations. Mol Ecol 23:29–39CrossRefPubMedGoogle Scholar
  68. Queiroz HL, Sobanski MB, Magurran AE (2010) Reproductive strategies of red-bellied piranha (Pygocentrus nattereri Kner, 1858) in the white waters of the Mamirauá flooded forest, central Brazilian Amazon. Environ Biol Fish 89:11–19CrossRefGoogle Scholar
  69. Rambaut A, Drummond AJ, Suchard M (2013) Tracer v1.6, Available from
  70. Reis RE, Kullander SO, Ferraris Jr CJ (2003) Check List of the Freshwater Fishes of South and Central America, pp 734Google Scholar
  71. Romiguier J, Gayral P, Ballenghien M, Bernard A, Cahais V, Chenuil A, Chiari Y, Dernat R, Duret L, Faivre N, Loire E, Lourenco JM, Nabholz B, Roux C, Tsagkogeorga G, Weber AAT, Weinert LA, Belkhir K, Bierne N, Glémin S, Galtier N (2014) Comparative population genomics in animals uncovers the determinants of genetic diversity. Nature 515:261–263CrossRefPubMedGoogle Scholar
  72. Ruffino ML (2004) A Pesca e os Recursos Pesqueiros na Amazônia Brasileira. IBAMA-PROVÁRZEA, Manaus, p. 272Google Scholar
  73. Ruffino ML, Soares EC, Silva CO, Barthem RB, Batista VS, Estupian G, Pinto W (2006) Estatística Pesqueira do Amazonas e Pará: 2003. IBAMA-PROVÁRZEA, v. 1, Manaus, AM, BrazilGoogle Scholar
  74. Santos MCF, Ruffino ML, Farias IP (2007) High levels of genetic variability and panmixia of the tambaqui Colossoma macropomum (Cuvier, 1818) in the main channel of the Amazon River. J Fish Biol 71A:33–44CrossRefGoogle Scholar
  75. Sato A, Takezaki N, Tichy H, Figueroa F, Mayer WE, Klein J (2003) Origin and speciation of haplochromine fishes in east African crater lakes investigated by the analysis of their mtDNA, Mhc genes, and SINEs. Mol Biol Evol 20:1448–1462CrossRefPubMedGoogle Scholar
  76. Simões PI, Lima AP, Farias IP (2012) Restricted natural hybridization between two species of litter frogs on a threatened landscape in southwestern Brazilian Amazonia. Conserv Genet 13:1145–1159CrossRefGoogle Scholar
  77. Soares MGM, Costa LC, Siqueira-Souza FK, Anjos HDB, Yamamoto CK, Freitas CEC (2007) Peixes de Lagos do Médio rio Solimões. EDUA, ManausGoogle Scholar
  78. Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585–595PubMedPubMedCentralGoogle Scholar
  79. Taylor BW, Flecker AS, Hall RO Jr (2006) Loss of a harvested fish species disrupts carbon flow in a diverse tropical river. Science 313:833–836CrossRefPubMedGoogle Scholar
  80. Thompson JD, Higgins DG, Gibson TJ (1996) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680CrossRefGoogle Scholar
  81. Torrente-Vilara G, Zuanon J, Leprieur F, Oberdorff T, Tedesco PA (2011) Effects of natural rapids and waterfalls on fish assemblage structure in the Madeira River (Amazon Basin). Ecol Freshw Fish 20:588–597CrossRefGoogle Scholar
  82. Turner TF, McPhee MV, Campbell P, Winemiller KO (2004) Phylogeography and intraspecific genetic variation of prochilodontid fishes endemic to rivers of northern South America. J Fish Biol 64:186–201CrossRefGoogle Scholar
  83. Vonhof HB, Kaandorp RJG (2010) Climate variation in Amazonia during the Neogene and the quaternary. In: Hoorn C, Wesselingh FP (eds) Amazonia: landscape and species evolution: a look into the past. Blackwell Publishing Ltd, Oxford, pp. 201–210Google Scholar
  84. Willis SC, Macrander J, Farias IP, Ortí G (2012) Simultaneous delimitation of species and quantification of interspecific hybridization in Amazonian peacock cichlids (genus Cichla) using multi-locus data. BMC Evol Biol 12:96CrossRefPubMedPubMedCentralGoogle Scholar
  85. Willis SC, Winemiller KO, Montaña CG, Macrander J, Reiss P, Farias IP, Ortí G (2015) Population genetics of the speckled peacock bass (Cichla temensis), South America’s most important inland sport fishery. Conserv Genet. doi: 10.1007/s10592-015-0744-y Google Scholar
  86. Winemiller KO (2005) Life history strategies, population regulation, and implications for fisheries management. Can J Fish Aquat Sci 62:872–885CrossRefGoogle Scholar
  87. Winemiller KO, Jepsen DB (1998) Effects of seasonality and fish movement on tropical river food webs. J Fish Biol 53:267–296CrossRefGoogle Scholar
  88. Wright S (1943) Isolation by distance. Genetics 28:114–138PubMedPubMedCentralGoogle Scholar
  89. Wright S (1969) Evolution and the genetics of populations. Volume 2. The theory of Gene frequencies. University of Chicago Press, ChicagoGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2016

Authors and Affiliations

  • Valéria Nogueira Machado
    • 1
  • Stuart C. Willis
    • 2
  • Aylton S. Teixeira
    • 3
  • Tomas Hrbek
    • 1
  • Izeni Pires Farias
    • 1
  1. 1.Laboratório de Evolução e Genética Animal (LEGAL)Universidade Federal do Amazonas (UFAM)ManausBrazil
  2. 2.Marine Genomics Lab, Department of Life SciencesTexas A&M University-Corpus ChristiCorpus ChristiUSA
  3. 3.Coordenação de Pesquisas em Biologia Aquática (CPBA)Instituto Nacional de Pesquisas da Amazônia (INPA)ManausBrazil

Personalised recommendations