Skip to main content

Advertisement

SpringerLink
Log in

Species validation and cryptic diversity in the Geophagus brasiliensis Quoy & Gaimard, 1824 complex (Teleostei, Cichlidae) from Brazilian coastal basins as revealed by DNA analyses

  • Primary Research Paper
  • Published:
Hydrobiologia Aims and scope Submit manuscript

Abstract

Many allopatric populations of the pearl cichlid Geophagus brasiliensis show remarkable morphological, chromosomal, and DNA sequence divergence. As a result, Geophagus brasiliensis is regarded as a species complex, combining recent descriptions of new species and several uncertainties about their actual richness. In the present work, we evaluated the number of evolutionary units in this fish complex along hydrographic basins in northeastern Brazil by using the DNA barcode, species delimitation algorithms and phylogenetic analyses. A total of 14 molecular operational taxonomic units (MOTUS) were identified with high support values and mean differentiation within and among groups of 0.4 and 12.7%, respectively. The DNA sequences supported Geophagus itapicuruensis as a valid taxon, besides indicating likely undescribed species. Moreover, the evolutionary units in coastal basins of useful to infer the evolutionary units in a cryptic and widespread fish group from the Neotropical region. Finally, the undescribed taxa in coastal basins of northeastern Brazil were clearly differentiated from Geophagus brasiliensis sensu stricto. The present data highlight the importance of conserving regional ichthyofauna since unique evolutionary lineages are potentially threatened by environmental degradation, invasive species and construction of dams.

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
Fig. 3

Similar content being viewed by others

References

  • Almeida, J. S., P. R. A. M. Affonso, D. Diniz, P. L. Carneiro & A. L. Dias, 2013. Chromosomal variation in the tropical armoured catfish Callichthys callichthys (Siluriformes, Callichthyidae): implications for conservation and taxonomy in a species complex from a Brazilian hotspot. Zebrafish 10: 451–458.

    Article  CAS  PubMed  Google Scholar 

  • Almeida, J. S., V. H. Migues, D. Diniz & P. R. A. M. Affonso, 2014. A unique sex chromosome system in the knifefish Gymnotus bahianus with inferences about chromosomal evolution of Gymnotidae. Journal of Heredity 106: 177–183.

    Article  Google Scholar 

  • Alves-Silva, A. P. & J. A. Dergam, 2015. Cryptic speciation within the Neotropical cichlid Geophagus brasiliensis (Quoy & Gaimard, 1824) (Teleostei Cichlidae): a new paradigm in karyotypical and molecular evolution. Zebrafish 12: 91–101.

    Article  PubMed  Google Scholar 

  • Azpelicueta, M. M., M. Benítez, D. Aichino & C. M. D. Mendez, 2015. A new species of the genus Hoplias (Characiformes, Erythrinidae), a tararira from the lower Paraná River, in Misiones, Argentina. Acta Zoológica Lilloana 59: 71–82.

    Google Scholar 

  • Barrett, R. D. H. & P. D. N. Hebert, 2005. Identifying spiders through DNA barcodes. Canadian Journal of Zoology 83: 481–491.

    Article  CAS  Google Scholar 

  • Barrett, J. C., B. Fry, J. Maller & M. J. Daly, 2005. Haploview: analysis and visualization of LD and haplotype maps. Bioinformatics 21: 263–265.

    Article  CAS  PubMed  Google Scholar 

  • Barreto, S. B., L. A. Nunes, A. T. Silva, R. Juca-Chagas, D. Diniz, I. Sampaio, H. Schneider & P. R. A. M. Affonso, 2016. Is Nematocharax (Actinopterygii, Characiformes) a monotypic fish genus? Genome 58: 191–192.

    Google Scholar 

  • Benine, R. C., R. M. C. Castro & A. C. A. Santos, 2007. A new Moenkhausia Eigenmann, 1903 (Ostariophysi: Characiformes) from Chapada Diamantina, rio Paraguaçu Basin, Bahia, Northeastern Brazil. Neotropical Ichthyology 5: 259–262.

    Article  Google Scholar 

  • Bertollo, L. A. C., G. G. Born, J. A. Dergam, A. S. Fenocchio & O. Moreira-Filho, 2000. A biodiversity approach in the neotropical Erythrinidae fish, Hoplias malabaricus. Karyotypic survey, geographic distribution of cytotypes and cytotaxonomic considerations. Chromosome Research 8: 603–613.

    Article  CAS  PubMed  Google Scholar 

  • Bitencourt, J. A., P. R. A. M. Affonso, L. Giuliano-Caetano, P. L. S. Carneiro & A. L. Dias, 2012. Population divergence and peculiar karyoevolutionary trends in the loricariid fish Hypostomus aff. unae from northeastern Brazil. Genetics and Molecular Research 11: 933–943.

    Article  CAS  PubMed  Google Scholar 

  • Blessing, J. J., J. C. Marshall & S. R. Balcombe, 2010. Humane killing of fishes for scientific research: a comparison of two methods. Journal of Fish Biology 76: 2571–2577.

    Article  CAS  PubMed  Google Scholar 

  • Bickford, D., D. J. Lohman, N. S. Sodhi, P. K. L. Ng, R. Meier, K. Winker, K. K. Ingram & I. Das, 2007. Cryptic species as a window on diversity and conservation. Trends in Ecology & Evolution 22: 148–155.

    Article  Google Scholar 

  • Carnaval, A. C. & C. Moritz, 2008. Historical climate modeling predicts patterns of current biodiversity in the Brazilian Atlantic Forest. Journal of Biogeography 35: 1187–1201.

    Article  Google Scholar 

  • Carnaval, A. C., M. J. Hickerson, C. F. B. Haddad, M. T. Rodrigues & C. Moritz, 2009. Stability predicts genetic diversity in the Brazilian Atlantic Forest Hotspot. Science 323: 785–789.

    Article  CAS  PubMed  Google Scholar 

  • Carvalho, D. C., D. A. A. Oliveira, O. S. Pompeu, C. G. Leal, C. Oliveira & R. Hanner, 2011. Deep barcode divergence in Brazilian freshwater fishes: the case of the São Francisco River Basin. Mitochondrial DNA 22: 80–86.

    Article  PubMed  Google Scholar 

  • Castro, R. M. C. & R. Jucá-Chagas, 2008. Lignobrycon myersi (Miranda-Ribero, 1956). In: Ministério do Meio Ambiente (ed.), Livro Vermelho da Fauna Brasileira Ameaçada de Extinção. Brasília, DF: 75–77.

  • Cetra, M., L. M. Sarmento-Soares & R. F. Pinheiro-Martins, 2010. Peixes de riachos e novas Unidades de Conservação no sul da Bahia. Pan-American Journal of Aquatic Sciences 5: 11–21.

    Google Scholar 

  • Chemale Jr., F., I. A. Dussin, M. Martins & M. N. Santos, 2011. Nova abordagem tectono-estratigráfica do Supergrupo Espinhaço em sua porção meridional (MG). Geonomos 19: 173–179.

    Google Scholar 

  • Farias, I. P., G. Ortí, I. Sampaio, H. Schneider & A. Meyer, 1999. Mitochondrial DNA phylogeny of the family Cichlidae: monophyly and fast molecular evolution of the Neotropical assemblage. Journal of Molecular Evolution 48: 703–711.

    Article  CAS  PubMed  Google Scholar 

  • Ferreira, D. G., S. C. Lima, W. Frantine-Silva, J. F. Silva, C. Apolinário-Silva, S. H. Sofia, S. Carvalho & B. A. Galindo, 2016. Fine-scale genetic structure patterns in two freshwater fish species, Geophagus brasiliensis (Osteichthyes, Cichlidae) and Astyanax altiparanae (Osteichthyes, Characidae) throughout a Neotropical stream. Genetics and Molecular Research 15: gmr15048124.

    Google Scholar 

  • Freire, C. A., E. M. Amado, L. R. Souza, M. P. Veiga, J. R. Vitule, M. M. Souza & V. Prodocimo, 2008. Muscle water control in crustaceans and fishes as a function of habitat, osmoregulatory capacity, and degree of euryhalinity. Comparative Biochemistry and Physiology, Part A 149: 435–446.

    Article  Google Scholar 

  • Gomes, L. C., T. C. Pessali, N. G. Sales, P. S. Pompeu & D. C. Carvalho, 2015. Integrative taxonomy detects cryptic and overlooked fish species in a neotropical river basin. Genetica 143: 581–588.

    Article  PubMed  Google Scholar 

  • Guindon, S., J. F. Dufayard, V. Lefort, M. Anisimova, W. Hordijk & O. Gascuel, 2010. New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Systematic Biology 59: 307–321.

    Article  CAS  PubMed  Google Scholar 

  • Hajibabaei, M., G. A. C. Singer, P. D. N. Hebert & D. A. Hickey, 2007. DNA barcoding: how it complements taxonomy, molecular phylogenetics and population genetics. Trends in Genetics 23: 167–172.

    Article  CAS  PubMed  Google Scholar 

  • Hebert, P. D. N., A. Cywinska, S. L. Ball & J. R. Dewaard, 2003a. Biological identifications through DNA barcodes. Proceedings of the Royal Society of London B: Biological Sciences 270: 313–321.

    Article  CAS  Google Scholar 

  • Hebert, P. D. N., S. Ratnasingham & J. R. Waard, 2003b. Barcoding animal life: cytochrome c oxidase subunit 1 divergences among closely related species. Proceedings of the Royal Society of London B: Biological Sciences 270: 96–99.

    Article  Google Scholar 

  • Hebert, P. D. N., M. Y. Stoeckle, T. S. Zemlak & C. M. Francis, 2004a. Identification of birds through DNA barcodes. Plos Biology 2: e312.

    Article  PubMed  PubMed Central  Google Scholar 

  • Hebert, P. D. N., E. H. Penton, J. M. Burns, D. H. Janzen & W. Hallwachs, 2004b. Ten species in one: DNA barcoding reveals cryptic species in the neotropical skipper butterfly Astraptes fulgerator. Proceedings of the National Academy of Sciences of the United States of America 101: 14812–14817.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Huelsenbeck, J. P. & F. Ronquist, 2001. MRBAYES: Bayesian inference of phylogeny. Bioinformatics 17: 754–755.

    Article  CAS  PubMed  Google Scholar 

  • Kadry, V. O. & R. E. Barreto, 2010. Environmental enrichment reduces aggression of pearl cichlid, Geophagus brasiliensis, during resident-intruder interactions. Neotropical Ichthyology 8: 329–332.

    Article  Google Scholar 

  • Kearse, M., R. Moir, A. Wilson, S. Stones-Havas, M. Cheung, S. Sturrock, S. Buxton, A. Cooper, S. Markowitz, C. Duran, T. Thierer, B. Ashton, P. Meintjes & A. Drummond, 2012. GENEIOUS Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bionformatics 28: 1647–1649.

    Article  Google Scholar 

  • Kimura, M., 1980. A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. Journal of Molecular Evolution 16: 111–120.

    Article  CAS  PubMed  Google Scholar 

  • Kocher, T. D., 2004. Adaptive evolution and explosive speciation: the cichlid fish model. Nature Reviews Genetics 5: 288–298.

    Article  CAS  PubMed  Google Scholar 

  • Kullander, S. O., 1983. Revision of the South American cichlid genus Cichlasoma. Swedish Museum of Natural History, Stockholm.

    Google Scholar 

  • Kullander, S. O., 1986. Cichlid fishes of the Amazon River drainage of Peru. Swedish Museum of Natural History, Stockholm.

    Google Scholar 

  • Kullander, S. O., 2003. Family Cichlidae. In Reis, R. E., S. O. Kullander & C. J. Ferraris (eds), Check List of Freshwater Fishes of South and Central America. Edipucs, Porto Alegre: 605–655.

    Google Scholar 

  • Librado, P. & J. Rozas, 2009. DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25: 1451–1452.

    Article  CAS  PubMed  Google Scholar 

  • López-Fernández, H. & D. C. Taphorn, 2004. Geophagus abalios, G. dicrozoster and G. winemilleri (Perciformes: cichlidae), three new species from Venezuela. Zootaxa 439: 1–27.

    Article  Google Scholar 

  • Lopez-Fernández, H., R. L. Honeycutt & K. O. Winemiller, 2005. Molecular phylogeny and evidence for an adaptive radiation of geophagine cichlids from South America (Perciformes: Labroidei). Molecular Phylogenetics and Evolution 34: 227–244.

    Article  PubMed  Google Scholar 

  • Mattos, J. L. O., 2010. Revisão taxonômica do grupo de espécies Geophagus brasiliensis (Quoy e Gaimard, 1824) do leste do Brasil (Perciformes: Cichlidae). Master’s thesis, Universidade Federal do Rio de Janeiro, Rio de Janeiro.

  • Mayden, R., 1997. A hierarchy of species concepts: the denouement in the saga of the species problem. In Claridge, M. F., H. A. Dawah & M. R. Wilson (eds), Species: The Units of Biodiversity. Chapman & Hall, London: 381–424.

    Google Scholar 

  • Medrado, A. S., M. S. Ribeiro, P. R. A. M. Affonso, P. L. S. Carneiro & M. A. Costa, 2012. Cytogenetic divergence in two sympatric fish species of the genus Astyanax Baird and Girard, 1854 (Characiformes, Characidae) from northeastern Brazil. Genetics and Molecular Biology 35: 797–801.

    Article  PubMed  PubMed Central  Google Scholar 

  • Ministério do Meio Ambiente. 2000. Avaliação e ações prioritárias para a conservação da biodiversidade da Mata Atlântica e Campos Sulinos por: Conservation International of Brazil, Fundação SOS Mata Atlântica, Fundação Biodiversitas, Instituto de Pesquisas Ecológicas, Secretaria do Meio Ambiente do Estado de São Paulo, SEMAD/Instituto Estadual de Florestas-MG. Brasília: MMA/SBF.

  • Nogueira, C., P. A. Buckup, N. A. Menezes, O. T. Oyakawa, T. P. Kasecker, M. B. Ramos Neto & J. M. C. Silva, 2010. Restricted-range fishes and the conservation of Brazilian freshwaters. PloS ONE 5: e11390.

    Article  PubMed  PubMed Central  Google Scholar 

  • Oliveira, I. A., L. A. Argolo, J. A. Bitencourt, D. Diniz, M. R. Vicari & P. R. A. M. Affonso, 2016. Cryptic chromosomal diversity in the complex “Geophagus” brasiliensis (Perciformes, Cichlidae). Zebrafish 13: 33–44.

    Article  CAS  PubMed  Google Scholar 

  • Pamponet, V. C. C., P. L. S. Carneiro, P. R. A. M. Affonso, V. S. Miranda, J. C. Silva Jr., C. G. Oliveira & F. A. Gaiotto, 2008. A multi-approach analysis of the genetic diversity in populations of Astyanax aff. bimaculatus Linnaeus, 1758 (Teleostei, Characidae) from Northeastern Brazil. Neotropical Ichthyology 6: 621–630.

    Article  Google Scholar 

  • Pereira, R., 1986. Peixes de nossa terra, Primeira ed. Nobel, São Paulo.

    Google Scholar 

  • Pereira, L. H. G., R. Hanner, F. Foresti & C. Oliveira, 2013. Can DNA barcoding accurately discriminate megadiverse Neotropical freshwater fish fauna? BMC Genetics 14: 14–20.

    Article  Google Scholar 

  • Pereira, L. H., G. M. Maia, R. Hanner, F. Foresti & C. Oliveira, 2011a. DNA barcodes discriminate freshwater fishes from the Paraíba do Sul River Basin, São Paulo, Brazil. Mitochondrial DNA 21: 71–79.

    Article  Google Scholar 

  • Pereira, L. H., M. F. Pazian, R. Hanner, F. Foresti & C. Oliveira, 2011b. DNA barcoding reveals hidden diversity in the Neotropical freshwater fish Piabina argentea (Characiformes: Characidae) from the Upper Paraná Basin of Brazil. Mitochondrial DNA 22: 87–96.

    Article  CAS  PubMed  Google Scholar 

  • Pires, L. B., L. Giuliano-Caetano & A. L. Dias, 2009. Cytogenetic characterization of Geophagus brasiliensis and two species of Gymnogeophagus (Cichlidae: Geophaginae) from Guaíba Lake, RS, Brazil. Folia Biologica 58: 29–34.

    Article  Google Scholar 

  • Poletto, A. B., I. A. Ferreira, D. C. Cabral-de-Mello, R. T. Nakajima, J. Mazzuchelli, H. B. Ribeiro, P. C. Venere, M. Nirchio, T. D. Kocher & C. Martins, 2010. Chromosome differentiation patterns during cichlid fish evolution. BMC Genetics 11: 50.

    Article  PubMed  PubMed Central  Google Scholar 

  • Posada, D., 2008. jModelTest: phylogenetic model averaging. Molecular Biology and Evolution 25: 1253–1256.

    Article  CAS  PubMed  Google Scholar 

  • Puillandre, N., A. Lambert, S. Brouillet & G. Achaz, 2012. ABGD, Automatic Barcode Gap Discovery for primary species delimitation. Molecular Ecology 21: 1864–1877.

    Article  CAS  PubMed  Google Scholar 

  • Ratnasingham, S. & P. D. N. Hebert, 2007. “Bold: The Barcode of Life Data System (http://www.barcodinglife.org).” Molecular Ecology Notes 7: 355–364.

  • Ratnasingham, S. & P. D. N. Hebert, 2013. A DNA-Based registry for all animal species: the Barcode Index Number (BIN) system. PLoS ONE 8: e66213.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Razkin, O., B. J. Gómez-Moliner, K. Vardinoyannis, A. Martínez-Ortí & M. J. Madeira, 2017. Species delimitation for cryptic species complexes: case study of Pyramidula (Gastropoda, Pulmonata). Zoologica Scripta 46: 55–72.

    Article  Google Scholar 

  • Saitou, N. & M. Nei, 1987. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Molecular Biology and Evolution 4: 406–425.

    CAS  PubMed  Google Scholar 

  • Sarmento-Soares, L. M. & R. F. Martins-Pinheiro, 2014. Uso inadequado das águas: a grande ameaça a sobrevivência das UCs na Mata Atlântica: o caso da REBIO Sooretama- ES. Boletim Sociedade Brasileira de Ictiologia 110: 16–18.

    Google Scholar 

  • Sarmento-Soares, L. M., A. M. Zanata & R. F. Martins-Pinheiro, 2011. Trichomycterus payaya, new catfish (Siluriformes: Trichomycteridae) from headwaters of rio Itapicuru, Bahia, Brazil. Neotropical Ichthyology 9: 261–271.

    Article  Google Scholar 

  • Severi, W., A. C. A. El-Deir, R. T. S. Félix, I. M. S. Araújo, S. C. S. Luz, A. V. Calado-Neto, B. D. F. Costa, R. J. Chagas & M. G. Barretto, M.G., 2010. Composição e abundância da ictiofauna na área de influência dos reservatórios de Pedra e Funil, bacia do rio de contas, Bahia. In: Moura, A. N., E. L. Araújo, M. C. Bittencourt-Oliveira, R. M. M. Pimentel & U. P. Albuquerque (eds), Reservatórios do nordeste do Brasil: biodiversidade, ecologia e manejo. Canal 6, Bauru, 1–576.

  • Tamura, K., D. Peterson, N. Peterson, G. Stecher, M. Nei & S. Kumar, 2011. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution 28: 2731–2739.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vasconcelos, M. F., A. V. Chaves & F. R. Santos, 2012. First record of Augastes scutatus for Bahia refines the location of a purported barrier promoting speciation in the Espinhaço range, Brazil. Revista Brasileira de Ornitologia 20: 443–446.

    Google Scholar 

  • Zhang, J., A. M. Mamlouk, T. Martinetz, S. Chang, J. Wang & R. Hilgenfeld, 2011. PhyloMap: an algorithm for visualizing relationships of large sequence data sets and its application to the influenza A virus genome. BMC bioinformatics 12: 248–267.

    Article  PubMed  PubMed Central  Google Scholar 

  • Ward, R. D., 2009. DNA barcode divergence among species and genera of birds and fishes. Molecular Ecology Resources 9: 1077–1085.

    Article  CAS  PubMed  Google Scholar 

  • Ward, R. D., T. S. Zemlak, B. H. Innes, P. R. Last & P. D. N. Hebert, 2005. DNA barcoding Australia’s fish species. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 360: 1847–1857.

    Article  CAS  Google Scholar 

  • Wimberger, P. H., 1992. Plasticity of fish body shape. The effects of diet, development, family and age in two species of Geophagus (Pisces: Cichlidae). Biological Journal of the Linnean Society 45: 197–218.

    Article  Google Scholar 

Download references

Acknowledgements

The authors would like to thank FAPESB (RED0009/2013), “Rede de DNA barcoding da ictiofauna do Brasil” (MCT/CNPq/FNDCT 50/2010), and CNPq (610013/2011-4) for the financial support.

Author information

Authors and Affiliations

  1. Department of Biological Sciences, Universidade Estadual do Sudoeste da Bahia, Av José Moreira Sobrinho, s/n, Jequié, BA, 45208-091, Brazil

    Cássio Ribeiro Souza, Paulo Roberto Antunes de Mello Affonso, Jamille de Araújo Bitencourt & Paulo Luiz Souza Carneiro

  2. Institute of Coastal Studies, Universidade Federal do Pará, Alameda Leandro Ribeiro, s/n, Aldeia, Bragança, PA, 68600-000, Brazil

    Iracilda Sampaio

Authors
  1. Cássio Ribeiro Souza
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Paulo Roberto Antunes de Mello Affonso
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jamille de Araújo Bitencourt
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Iracilda Sampaio
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Paulo Luiz Souza Carneiro
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Paulo Roberto Antunes de Mello Affonso.

Additional information

Handling editor: Christian Sturmbauer

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 60 kb)

10750_2017_3482_MOESM2_ESM.tif

Online Resource 2 PhyloMap PTP tree based on COI sequences of the samples of Geophagus brasiliensis complex from the present study and related species available in BOLD. The circles in the graph represent the taxa and species are indicated by distinct colors. The horizontal and vertical axis explained 65.80% and 13.56% of total variation, respectively. The thicker lines indicate that the length of branches in the original species tree is longer than those shown in the graph. Supplementary material 2 (TIFF 6962 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Souza, C.R., de Mello Affonso, P.R.A., de Araújo Bitencourt, J. et al. Species validation and cryptic diversity in the Geophagus brasiliensis Quoy & Gaimard, 1824 complex (Teleostei, Cichlidae) from Brazilian coastal basins as revealed by DNA analyses. Hydrobiologia 809, 309–321 (2018). https://doi.org/10.1007/s10750-017-3482-y

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10750-017-3482-y

Keywords

Search

Navigation