Skip to main content
SpringerLink
Log in

DNA barcode sheds light on systematics and evolution of neotropical freshwater trahiras

  • Original Paper
  • Published:
Genetica Aims and scope Submit manuscript

Abstract

We assessed the presence of independent evolving lineages of the trahira, Hoplias malabaricus, one of the few freshwater fish species having wide distribution in the Neotropics which is the region with the highest global diversity of freshwater fish. To achieve that goal, 58 mitochondrial sequences of cytochrome c oxidase subunit I (COI; DNA barcoding) were generated from collected samples and 85 obtained from public databases, which were analyzed in comparison to chromosomal and geological data. The magnitude of genetic diversity found among different sampling sites was greater than 2%. Molecular species delimitation methods indicated the existence of a least four distinct lineages. The recognised cytotypes did not form monophyletic groups, suggesting that the karyotypic macrostructure could be a homoplastic character. The haplotype relationships suggested secondary contacts between the ecoregions of Northern and Northeastern Brazil that were shaped by coastal routes between adjacent watersheds during the Pleistocene epoch and probable exchanges of their ichthyofaunas. Our results indicated that multiple factors have driven the diversification of H. malabaricus, from ancient geological events linked to the reactivation of tectonic faults to more recent occurrences related to eustatic changes in ocean levels. Ultimately, the magnitude of its genetic diversity suggests the necessity of revising its taxonomic status.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Ab’Saber AN (1957) O problema das conexões antigas e da separação da drenagem do Paraiba e Tietê. Bol Paul Geogr 26:38–49

    Google Scholar 

  • Ab’Saber AN (1998) Megageomorfologia do território brasileiro. In: Cunha SB, Guerra AJT (eds) Geomorfologia do Brasil. Bertrand Brasil. Bertrand Press, Rio de Janeiro, pp 71–106

    Google Scholar 

  • Albert JS, Reis RE (2011) Introduction to neotropical freshwaters. In: Albert JS, Reis RE (eds) Historical biogeography of neotropical freshwater. Fishes University of California Press, Berkeley, pp 3–20

    Chapter  Google Scholar 

  • Araujo-Lima CARM, Bittencourt MM (2001) A Reprodução e o Inicio da Vida de Hoplias malabaricus (Erythrinidae; Characiformes) na Amazônia Central. Acta Amaz 31(4):693–697. https://doi.org/10.1590/1809-43922001314697

    Article  Google Scholar 

  • Avise JC (2000) Phylogeography: the history and formation of species. Harvard University Press, Cambridge

    Google Scholar 

  • Avise JC (2009) Phylogeography: retrospect and prospect. J Biogeogr 36:3–15. https://doi.org/10.1111/j.1365-2699.2008.02032

    Article  Google Scholar 

  • Azpelicueta MM, Benítez M, Aichino D, Mendez CMD (2015) A new species of the genus Hoplias (Characiformes, Erythrinidae), a tararira from the lower Paraná River, in Missiones, Argentina. Acta Zool Lillo 59:71–82

    Google Scholar 

  • Basílio TH, Godinho WO, Araújo ME, Furtado-Neto MA, Faria VV (2009) Ictiofauna do Estuário do Rio Curu, Ceará, Brasil Ichthyofauna of the Curu River estuary, Ceará State, Brazil. Arq Cien Mar 42(2):81–88

    Google Scholar 

  • Beheregaray LBP, Sunnucks DA, Briscoe DA (2002) A rapid fish radiation associated with the last sea level changes in southern Brazil: the silverside Odontesthes perugiae complex. Proc R Soc Lond B Biol Sci 269:65–73

    Article  Google Scholar 

  • Bertollo LAC, Born GG, Dergam JA, Fenocchio AS, Moreira-Filho O (2000) A biodiversity approach in the neotropical Erythrinidae fish. Hoplias malabaricus. Karyotypic survey, geographic distribution of karyomorphs and cytotaxonomic considerations. Chromosome Res 8:603–613

    Article  CAS  PubMed  Google Scholar 

  • Born GG, Bertollo LAC (2001) An XX/XY sex chromosome in a fish species, Hoplias malabaricus, with a polymorphic NOR-bearing X chromosome. Chromosome Res 8:111–118. https://doi.org/10.1023/A:1017572030350

    Article  Google Scholar 

  • Brito-Neves BB, Riccomini C, Fernandes TMG, Sant’Anna LG (2004) O sistema tafrogênico Terciário do saliente oriental nordestino na Paraíba: Um legado Proterozóico. Rev Bras Geo 34:127–134

    Article  Google Scholar 

  • Brown SDJ, Collins RA, Boyer S, Lefort MC, Malumbres-Olarte J (2012) Spider: an R package for the analysis of species identity and evolution, with particular reference to DNA barcoding. Mol Ecol Resour 12(3):562–565. https://doi.org/10.1111/j.1755-0998.2011.03108

    Article  PubMed  Google Scholar 

  • Costa WJEM (2010) Historical biogeography of cynolebiasine annual killifishes inferred from dispersal–vicariance analysis. J Biogeogr 37:1995–2004. https://doi.org/10.1111/j.1365-2699.2010.02339

    Article  Google Scholar 

  • Costa WJEM (2014) A new genus of miniature cynolebiasine from the Atlantic Forest and alternative biogeographical explanations for seasonal killifish distribution patterns in South America (Cyprinodontiformes: Rivulidae). Vertebr Zool 64(1):23–33

    Google Scholar 

  • Dergam JC, Bertollo LAC (1990) Karyotypic diversification in Hoplias malabaricus (Ostheichthyes, Erythrinidae) of São Francisco and Alto Paraná basins. Braz J Genet 13:755–766

    Google Scholar 

  • Drummond AJ, Rambaut A (2007) BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol Biol 7:214–221. https://doi.org/10.1186/1471-2148-7-214

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Drummond AJ, Suchard MA, Xie D, Rambaut A (2012) Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol Biol Evol 29:1969–1973. https://doi.org/10.1093/molbev/mss075 (Epub 25 Feb 2012)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fujisawa T, Barraclough TG (2013) Delimiting species using single-locus data and the generalized mixed yule coalescent (GMYC) approach: a revised method and evaluation on simulated datasets. Syst Biol 62:707–724. https://doi.org/10.1093/sysbio/syt033 (Epub 16 May 2013)

    Article  PubMed  PubMed Central  Google Scholar 

  • Grassi DJ, Swarça AC, Dergam JA, Pastori MC, Fenocchio AS (2017) Cytogenetic characterization of Hoplias malabaricus (Bloch, 1794) from the Ctalamochita river (Córdoba, Argentina): first evidence for southernmost populations of this species complex and comments on its biogeography. Comp Cytogenet 11(1):15–28. https://doi.org/10.3897/CompCytogen.v11i1.10262

    Article  PubMed  PubMed Central  Google Scholar 

  • Hebert PDN, Cywinska A, Ball SL, Ward JR (2003) Biological identifications through DNA barcodes. Proc R Soc Lond B Biol Sci 270:313–321. https://doi.org/10.1098/rspb.2002.2218

    Article  CAS  Google Scholar 

  • Hubert N, Renno JF (2006) Historical biogeography of South American freshwater fishes. J Biogeogr 33:1414–1436. https://doi.org/10.1111/j.1365-2699.2006.01518.x

    Article  Google Scholar 

  • Hubert N, Duponchelle F, Nuñez J, Garcia-Davila C, Paugy D, Renno J (2007) Phylogeography of the piranha genera Serrasalmus and Pygocentrus: implications for the diversification of the neotropical ichthyofaunal. Mol Ecol 16:2115–2136. https://doi.org/10.1111/j.1365-294X.2007.03267.x

    Article  CAS  PubMed  Google Scholar 

  • Hubert N, Hanner R, Holm E, Mandrak NE, Taylor E, Burridge M, Watkinson D, Dumont P, Curry A, Bentzen P, Zhang J, April J, Bernatchez L (2008) Identifying Canadian freshwater fishes through DNA barcodes. Plos One 3:1–8. https://doi.org/10.1371/journal.pone.0002490

    Article  CAS  Google Scholar 

  • Jacobina UP, Affonso PRAM, Carneiro PLS, Dergam JA (2009) Biogeography and comparative cytogenetics between two populations of Hoplias malabaricus (Bloch, 1794) (Ostariophysi: Erythrinidae) from coastal basins in the state of Bahia, Brazil. Neotrop Ichthyol 7:617–622. https://doi.org/10.1590/S1679-62252009000400009

    Article  Google Scholar 

  • Jacobina UP, Paiva E, Dergam JA (2011) Pleistocene karyotypic divergence in Hoplias malabaricus (Bloch, 1974) (Teleostei: Erythrinidae) populations in southeastern Brazil. Neotrop Ichthyol 9:325–333. https://doi.org/10.1590/S1679-62252011005000023

    Article  Google Scholar 

  • Jacobina UP, Martinez PA, Torres RA, Souza G (2016) Trends on the karyotype acrocentrization within Carangidae (Perciformes): a new phylogenetic evidence about a traditional marine paradigm. Zebrafish 13(1):45–53. https://doi.org/10.1089/zeb.2015.1143 (Epub 30 Dec 2015)

    Article  PubMed  Google Scholar 

  • Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M, Sturrock S, Buxton S, Cooper A, Markowitz S, Duran C, Thierer T, Ashton B, Mentjies P, Drummond A (2012) Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28(12):1647–1649. https://doi.org/10.1093/bioinformatics/bts199 (Epub 27 Apr 2012)

    Article  PubMed  PubMed Central  Google Scholar 

  • Lanfear R, Calcott B, Ho SYW, Guindon S (2012) PartitionFinder: combined selection of partitioning schemes and substitution models for phylogenetic analyses. Mol Bio Evol 29(6):1695–1701. https://doi.org/10.1093/molbev/mss020 (Epub 20 Jan 2012)

    Article  CAS  Google Scholar 

  • Lara A, De León JLP, Rodriguez R, Casane D, Côte G, Bernatchez L, Garcia-Machado E (2010) DNA barcoding of Cuban freshwater fishes: evidence for cryptic species and taxonomic conflicts. Mol Ecol Resour 10:421–430. https://doi.org/10.1111/j.1755-0998.2009.02785.x (Epub 22 Oct 2009)

    Article  CAS  PubMed  Google Scholar 

  • Leigh JW, Bryant D (2015) POPART: full-feature software for haplotype network construction. Methods Ecol Evol 6:1110–1116. https://doi.org/10.1111/2041-210X.12410

    Article  Google Scholar 

  • Lima SMQ, Vasconcellos AV, Berbel-Filho WM, Lazoski C, Russo CAM, Sazima I, Solé-Cava AM (2016) Effects of Pleistocene climatic and geomorphological changes on the population structure of the restricted-range catfish Trichogenes longipinnis (Siluriformes: Trichomycteridae). Syst Biodivers 14(2):155–170. https://doi.org/10.1080/14772000.2015.1104398

    Article  Google Scholar 

  • Lundberg JG, Marshall LG, Guerrero J, Horton JB, 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 13–48

    Google Scholar 

  • Mai ACG, Robe LJ, Marins LF, Vieira JP (2016) Genetic relationships between landlocked and coastal populations of Lycengraulis grossidens (Engraulidae) in south-eastern South America: evidence for a continental colonization route with secondary transitions to the coastal region. Mar Freshw Res 67:1–10. https://doi.org/10.1071/MF15355

    Article  Google Scholar 

  • Malabarba MCSL (2003) Os peixes da Formação Tremembé e paleobiogeografia da Bacia de Taubaté, Estado de São Paulo, Brasil. UNG 5:36–46

    Google Scholar 

  • Marques DF, Santos FA, Silva SS, Sampaio IS, Rodrigues LRR (2013) Cytogenetic and DNA barcoding reveals high divergence within the trahira, Hoplias malabaricus (Characiformes: Erythrinidae) from the lower Amazon river. Neotrop Ichthyol 11:459–466. https://doi.org/10.1590/S1679-62252013000200015 1937

    Article  Google Scholar 

  • Melo BF, Ochoa LE, Vari RP, Oliveira C (2016) Cryptic species in the neotropical fish genus Curimatopsis (Teleostei, Characiformes) Zool Scr 45: 650–658. https://doi.org/10.1111/zsc.12178

    Article  Google Scholar 

  • Menezes NA, Ribeiro AC, Weitzman S, Torres RA (2008) Biogeography of Glandulocaudinae (Teleostei: Characiformes: Characidae) revisited: phylogenetic patterns, historical geology and genetic connectivity. Zootaxa 1726:33 – 48

    Google Scholar 

  • Montoya-Burgos JI (2003) Historical biogeography of the catfish genus Hypostomus (Siluriformes: Loricariidae), with implications on the diversification of neotropical ichthyofauna. Mol Ecol 12:1855–1867. https://doi.org/10.1046/j.1365-294X.2003.01857.x

    Article  CAS  PubMed  Google Scholar 

  • Myers GS (1938) Fresh-water fishes and West Indian zoogeography. Annu Rep Smith Inst 339–364

  • Oyakawa OT (2003) Family Erythrinidae. In: Reis RE, Kullander SO, Ferraris C Jr (eds) Check list of the freshwater fishes of South America. Edipucrs, Porto Alegre, pp 238–240

    Google Scholar 

  • Oyakawa OT, Mattox GMT (2009) Revision of the neotropical trahiras of the Hoplias lacerdae species-group (Ostariophysi: Characiformes: Erythrinidae) with descriptions of two new species. Neotrop Ichthyol 7:117–140. https://doi.org/10.1590/S1679-62252009000200001

    Article  Google Scholar 

  • Padial JM, Miralles A, De La Riva I, Vences M (2010) Frontiers in the integrative future of taxonomy. Zoology 1:7–16. https://doi.org/10.1186/1742-9994-7-16

    Article  Google Scholar 

  • Pazza R, Julio HF Jr (2003) Occurrence of three sympatric cytotypes of Hoplias malabaricus (Pisces, Erythrinidae) in the upper Paraná river foodplain (Brazil). Cytologia 68:159–163. https://doi.org/10.1508/cytologia.68.159

    Article  Google Scholar 

  • Pereira TL, Santos U, Schaefer CE, Souza GO, Paiva SR, Malabarba LR, Schmidt EE, Dergam JA (2012) Dispersal and vicariance of Hoplias malabaricus (Bloch, 1794) (Teleostei, Erythrinidae) populations of the Brazilian continental margin. J Biogeogr 40:905–914. https://doi.org/10.1111/jbi.12044

    Article  Google Scholar 

  • 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 55:595–609. https://doi.org/10.1080/10635150600852011

    Article  PubMed  Google Scholar 

  • Potter PE (1997) The Mesozoic and Cenozoic Paleodrainage of South America: a natural history. J South Am Earth Sci 10:331–344

    Article  Google Scholar 

  • Ratnasingham S, Hebert PDN (2007) BOLD: the barcode of life data system (www.barcodinglife.org). Mol Ecol Notes 7:355–364. https://doi.org/10.1111/j.1471-8286.2007.01678.x

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Reis RE, Kullander SO, Ferraris CJ (2003) Check list of the freshwater fishes of South and Central America. Edipucrs, Porto Alegre

    Google Scholar 

  • Reis RE, Albert JS, Di Mario F, Mincarone MM, Petry P, Rocha LA (2016) Fish biodiversity and conservation in South America. J Fish Biol 12(47):1–1. https://doi.org/10.1111/j.1471-8286.2007.01678.x

    Article  Google Scholar 

  • Ribeiro AC (2006) Tectonic history and the biogeography of the freshwater fishes from the coastal drainages of eastern Brazil: an example of faunal evolution associated with a divergent continental margin. Neotrop Ichthyol 4:225–246. https://doi.org/10.1590/S1679-62252006000200009

    Article  Google Scholar 

  • Ribeiro AC, Lima FCL, Menezes NA, Carvalho CJB, Almeida EAB (2016) Biogeografia de Peixes de Água Doce da América do Sul. In: Biogeografia da América do Sul: Analise de Tempo, Espaço e Forma, 2nd edn. Rocca, Rio de Janeiro, pp 245–258

    Google Scholar 

  • Riccomini C (1990) O rift continental do sudeste do Brasil. PhD Thesis, Instituto de Geociências, Universidade de São Paulo, São Paulo

  • Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A, Hohna 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 61:539–542. https://doi.org/10.1093/sysbio/sys029. (Epub 22 Feb 2012)

    Article  PubMed  PubMed Central  Google Scholar 

  • Rosa RS, Menezes NA, Britski HA, Costa WJEM, Groth F (2004) Diversidade, padrões de distribuição e conservação dos peixes da caatinga. In: Tabarelli IRM, da Silva JMC (eds) Ecologia e conservação da Caatinga. Edufpe, Recife, pp 135–180

    Google Scholar 

  • Rosa R, Caetano-Filho M, Shibatta OA, Giuliano-Caetano L (2009) Cytotaxonomy in distinct populations of Hoplias aff. malabaricus (Characiformes, Erythrinidae) from lower Paranapanema river basin. J Fish Biol 75:2682–2694. https://doi.org/10.1111/j.1095-8649.2009.02467.x

    Article  CAS  PubMed  Google Scholar 

  • Rosa R, Vicari MR, Dias AL, Giuliano-Caetano L (2014) New insights into the biogeographic and karyotypic evolution of Hoplias malabaricus. ZebraFish 11:198–206. https://doi.org/10.1089/zeb.2013.0953. (Epub 10 Mar 2014)

    Article  CAS  PubMed  Google Scholar 

  • Rosso JJ, Mabragaña E, González-Castro M, Delpiani MS, Avigliano E, Schenone N, Astarloa JMD (2016) A new species of the Hoplias malabaricus species complex (Characiformes: Erythrinidae) from the La Plata river basin. Cybium 40(3):199–208

    Google Scholar 

  • Roxo FF, Albert JS, Silva GS, Zawadzki CH, Foresti F, Oliveira C (2014) Molecular phylogeny and biogeographic history of the armored neotropical catfish subfamilies Hypoptopomatinae, Neoplecostominae and Otothyrinae (Siluriformes: Loricariidae). PLoS One 9(8):1–17. https://doi.org/10.1371/journal.pone.0105564

    Article  CAS  Google Scholar 

  • Santos U, Völcker CM, Belei FA, Cioffi MB, Bertollo LAC, Paiva SR, Dergam JA (2009) Molecular and karyotypic phylogeography in the Neotropical Hoplias malabaricus (Erythrinidae) fish in eastern Brazil. J Fish Biol 75:2326–2343. https://doi.org/10.1111/j.1095-8649.2009.02489.x

    Article  CAS  PubMed  Google Scholar 

  • Sempere T, Herail G, Oller J, Bohnomme M (1990) Late Oligocene–early Miocene major tectonic crisis and related basin in Bolivia. Geology 18:946–949

    Article  Google Scholar 

  • Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729. https://doi.org/10.1093/molbev/mst197

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 11(22):73–80

    Google Scholar 

  • Torres RA, Ribeiro J (2009) The remarkable species complex Mimagoniates microlepis (Characiformes: Glandulocaudinae) from the Southern Atlantic Rain forest (Brazil) as revealed by molecular systematic and population genetic analyses. Hydrobiologia 617:157–170. https://doi.org/10.1007/s10750-008-9543-5

    Article  CAS  Google Scholar 

  • Vari RP (1988) The Curimatidae, a lowland neotropical fish family (Pisces: Characiformes): distribution, endemism, and phylogenetic biogeography. In: Vanzolini PE, Heyer WR (eds) Proceedings of workshop on neotropical distribution patterns, Academia Brasileira de Ciências, Rio de Janeiro, pp 313–348

  • Vitule JRS, da Costa APL, Frehse FA, Bezerra LAV, Occhi TVT, Daga VS (2017) Comment on ‘Fish biodiversity and conservation in South America by Reis et al. (2016). J Fish Biol 90:1182–1190. https://doi.org/10.1111/jfb.13239

    Article  CAS  PubMed  Google Scholar 

  • Ward RW, Zemlak TS, Innes BH, Last PR, Hebert PDN (2005) DNA barcoding Australia’s fish species. Philos Trans R Soc Lond B Biol Sci 360:1847–1857. https://doi.org/10.1098/rstb.2005.1716

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ward RD, Hanner R, Hebert PDN (2009) The campaign to DNA barcode all fishes, FISH-BOL. J Fish Biol 74:329–356. https://doi.org/10.1111/j.1095-8649.2008.02080.x

    Article  CAS  PubMed  Google Scholar 

  • Weitzman SH, Menezes NA, Weitzman MJ (1988) Phylogenetic biogeography of the Glandulocaudini (Teleostei: Characiformes, Characidae) with comments on the distribution of other freshwater fishes in eastern and southeastern Brazil. In: Vanzolini PE, Heyer WR (eds) Proceedings of workshop on neotropical distribution patterns, Academia Brasileira de Ciências, Rio de Janeiro, pp 379–427

  • Werneck FP, Leite RN, Geurgas SR, Rodrigues MT (2015) Biogeographic history and cryptic diversity of saxicolous Tropiduridae lizards endemic to the semiarid Caatinga. BMC Evol Biol 15:94:1–24. https://doi.org/10.1186/s12862-015-0368-3

    Article  Google Scholar 

  • White MJD (1978) Chain processes in chromosomal speciation. Syst Zool 27:285

    Article  Google Scholar 

  • Zhang J, Kapli P, Pavlidis P, Stamatakis AA (2013) General species delimitation method with applications to phylogenetic placements. Bioinformatics 29(22):2869–2876. https://doi.org/10.1093/bioinformatics/btt499 (Epub 29 Aug 2013)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

UPJ thanks Fundação de Amparo à Ciência e Tecnologia do Estado de Pernambuco (FACEPE) for research funding (BCT-0125-2.04/15), and Conselho Nacional de Desenvolvimento Científico e Tecnológico CNPq (425080/2016-1). HBF thanks FAPESB (RED0045/2014; JCB0026/2016), CNPq (443249/2014-8) and National Institute of Science and Technology in Interdisciplinary and Transdisciplinary Studies in Ecology and Evolution (INCT IN-TREE) for funding. SMQL thanks CNPq (552086/2011-8 and 483878/2013-8). RAT is grateful to Fundação de Amparo à Ciência e Tecnologia do estado de Pernambuco (FACEPE; grant. no. APQ-0551-2.04/15) and to CNPq for the research fellowship provided (grant no.306290/2015-4).

Author information

Authors and Affiliations

  1. Laboratório de Ictiologia e Conservação, Universidade Federal de Alagoas, Campus-Arapiraca-Penedo, Avenida Beira Rio s/n, Penedo, AL, CEP 57200-000, Brazil

    U. P. Jacobina

  2. Laboratório de Ictiologia Sistemática e Evolutiva, Departamento de Botânica e Zoologia, Universidade Federal do Rio Grande do Norte, Lagoa Nova, Natal, RN, CEP 59978-970, Brazil

    S. M. Q. Lima

  3. Laboratório de Genômica Evolutiva e Ambiental, Departamento de Zoologia, Universidade Federal de Pernambuco, Av Prof. Nelson Chaves s/n, Cidade Universitária, Recife, PE, CEP 50670-420, Brazil

    D. Gama Maia & R. A. Torres

  4. Laboratório de Citogenética e Evolução Vegetal, Departamento de Botânica, Universidade Federal de Pernambuco, Recife, PE, CEP 50670-420, Brazil

    G. Souza

  5. Laboratório de Evolução e Biogeografia, Instituto de Biologia, Universidade Federal da Bahia, Rua Barão de Jeremoabo, Ondina, Salvador, BA, CEP 40170-115, Brazil

    H. Batalha-Filho

  6. National Institute of Science and Technology in Interdisciplinary and Transdisciplinary Studies in Ecology and Evolution (INCT IN-TREE), Instituto de Biologia, Universidade Federal da Bahia, Rua Barão de Jeremoabo, Ondina, Salvador, BA, CEP 40170-115, Brazil

    H. Batalha-Filho

Authors
  1. U. P. Jacobina
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. S. M. Q. Lima
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. D. Gama Maia
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. G. Souza
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. H. Batalha-Filho
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. R. A. Torres
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to U. P. Jacobina.

Ethics declarations

Conflict of interest

All authors declare that have no conflict of interest.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 List of the 143 specimens analyzed (XLSX 15 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Jacobina, U.P., Lima, S.M.Q., Maia, D.G. et al. DNA barcode sheds light on systematics and evolution of neotropical freshwater trahiras. Genetica 146, 505–515 (2018). https://doi.org/10.1007/s10709-018-0043-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10709-018-0043-x

Keywords

Search

Navigation