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, Volume 146, Issue 6, pp 505–515 | Cite as

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

  • U. P. Jacobina
  • S. M. Q. Lima
  • D. Gama Maia
  • G. Souza
  • H. Batalha-Filho
  • R. A. Torres
Original Paper

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.

Keywords

Hoplias malabaricus Phylogeography Cryptic diversity Characiformes Species delimitation 

Notes

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).

Compliance with ethical standards

Conflict of interest

All authors declare that have no conflict of interest.

Supplementary material

10709_2018_43_MOESM1_ESM.xlsx (16 kb)
Supplementary material 1 List of the 143 specimens analyzed (XLSX 15 KB)

References

  1. Ab’Saber AN (1957) O problema das conexões antigas e da separação da drenagem do Paraiba e Tietê. Bol Paul Geogr 26:38–49Google Scholar
  2. 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 71–106Google Scholar
  3. 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 3–20CrossRefGoogle Scholar
  4. 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 CrossRefGoogle Scholar
  5. Avise JC (2000) Phylogeography: the history and formation of species. Harvard University Press, CambridgeGoogle Scholar
  6. Avise JC (2009) Phylogeography: retrospect and prospect. J Biogeogr 36:3–15.  https://doi.org/10.1111/j.1365-2699.2008.02032 CrossRefGoogle Scholar
  7. 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 59:71–82Google Scholar
  8. 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):81–88Google Scholar
  9. 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 269:65–73CrossRefGoogle Scholar
  10. 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 8:603–613CrossRefGoogle Scholar
  11. 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 CrossRefGoogle Scholar
  12. 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 34:127–134CrossRefGoogle Scholar
  13. 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 CrossRefPubMedGoogle Scholar
  14. 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 CrossRefGoogle Scholar
  15. 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):23–33Google Scholar
  16. Dergam JC, Bertollo LAC (1990) Karyotypic diversification in Hoplias malabaricus (Ostheichthyes, Erythrinidae) of São Francisco and Alto Paraná basins. Braz J Genet 13:755–766Google Scholar
  17. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  18. 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) CrossRefPubMedPubMedCentralGoogle Scholar
  19. 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) CrossRefPubMedPubMedCentralGoogle Scholar
  20. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  21. 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 CrossRefGoogle Scholar
  22. 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 CrossRefGoogle Scholar
  23. 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 CrossRefPubMedGoogle Scholar
  24. 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 CrossRefGoogle Scholar
  25. 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 CrossRefGoogle Scholar
  26. 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 CrossRefGoogle Scholar
  27. 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) CrossRefPubMedGoogle Scholar
  28. 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) CrossRefPubMedPubMedCentralGoogle Scholar
  29. 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) CrossRefGoogle Scholar
  30. 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) CrossRefPubMedGoogle Scholar
  31. 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 CrossRefGoogle Scholar
  32. 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 CrossRefGoogle Scholar
  33. 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 13–48Google Scholar
  34. 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 CrossRefGoogle Scholar
  35. Malabarba MCSL (2003) Os peixes da Formação Tremembé e paleobiogeografia da Bacia de Taubaté, Estado de São Paulo, Brasil. UNG 5:36–46Google Scholar
  36. 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 1937CrossRefGoogle Scholar
  37. 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 CrossRefGoogle Scholar
  38. 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 – 48Google Scholar
  39. 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 CrossRefPubMedGoogle Scholar
  40. Myers GS (1938) Fresh-water fishes and West Indian zoogeography. Annu Rep Smith Inst 339–364Google Scholar
  41. 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 238–240Google Scholar
  42. 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 CrossRefGoogle Scholar
  43. 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 CrossRefGoogle Scholar
  44. 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 CrossRefGoogle Scholar
  45. 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 CrossRefGoogle Scholar
  46. 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 CrossRefPubMedGoogle Scholar
  47. Potter PE (1997) The Mesozoic and Cenozoic Paleodrainage of South America: a natural history. J South Am Earth Sci 10:331–344CrossRefGoogle Scholar
  48. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  49. Reis RE, Kullander SO, Ferraris CJ (2003) Check list of the freshwater fishes of South and Central America. Edipucrs, Porto AlegreGoogle Scholar
  50. 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 CrossRefGoogle Scholar
  51. 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 CrossRefGoogle Scholar
  52. 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 245–258Google Scholar
  53. Riccomini C (1990) O rift continental do sudeste do Brasil. PhD Thesis, Instituto de Geociências, Universidade de São Paulo, São PauloGoogle Scholar
  54. 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) CrossRefPubMedPubMedCentralGoogle Scholar
  55. 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 135–180Google Scholar
  56. 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 CrossRefPubMedGoogle Scholar
  57. 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) CrossRefPubMedGoogle Scholar
  58. 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):199–208Google Scholar
  59. 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 CrossRefGoogle Scholar
  60. 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 CrossRefPubMedGoogle Scholar
  61. Sempere T, Herail G, Oller J, Bohnomme M (1990) Late Oligocene–early Miocene major tectonic crisis and related basin in Bolivia. Geology 18:946–949CrossRefGoogle Scholar
  62. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  63. 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):73–80Google Scholar
  64. 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 CrossRefGoogle Scholar
  65. 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 313–348Google Scholar
  66. 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 CrossRefPubMedGoogle Scholar
  67. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  68. 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 CrossRefPubMedGoogle Scholar
  69. 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 379–427Google Scholar
  70. 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 CrossRefGoogle Scholar
  71. White MJD (1978) Chain processes in chromosomal speciation. Syst Zool 27:285CrossRefGoogle Scholar
  72. 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) CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2018

Authors and Affiliations

  • U. P. Jacobina
    • 1
  • S. M. Q. Lima
    • 2
  • D. Gama Maia
    • 3
  • G. Souza
    • 4
  • H. Batalha-Filho
    • 5
    • 6
  • R. A. Torres
    • 3
  1. 1.Laboratório de Ictiologia e ConservaçãoUniversidade Federal de AlagoasPenedoBrazil
  2. 2.Laboratório de Ictiologia Sistemática e Evolutiva, Departamento de Botânica e ZoologiaUniversidade Federal do Rio Grande do NorteNatalBrazil
  3. 3.Laboratório de Genômica Evolutiva e Ambiental, Departamento de ZoologiaUniversidade Federal de PernambucoRecifeBrazil
  4. 4.Laboratório de Citogenética e Evolução Vegetal, Departamento de BotânicaUniversidade Federal de PernambucoRecifeBrazil
  5. 5.Laboratório de Evolução e Biogeografia, Instituto de BiologiaUniversidade Federal da BahiaSalvadorBrazil
  6. 6.National Institute of Science and Technology in Interdisciplinary and Transdisciplinary Studies in Ecology and Evolution (INCT IN-TREE), Instituto de BiologiaUniversidade Federal da BahiaSalvadorBrazil

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