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.
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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.
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.
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.
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.
Barrett, R. D. H. & P. D. N. Hebert, 2005. Identifying spiders through DNA barcodes. Canadian Journal of Zoology 83: 481–491.
Barrett, J. C., B. Fry, J. Maller & M. J. Daly, 2005. Haploview: analysis and visualization of LD and haplotype maps. Bioinformatics 21: 263–265.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
Hebert, P. D. N., M. Y. Stoeckle, T. S. Zemlak & C. M. Francis, 2004a. Identification of birds through DNA barcodes. Plos Biology 2: e312.
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.
Huelsenbeck, J. P. & F. Ronquist, 2001. MRBAYES: Bayesian inference of phylogeny. Bioinformatics 17: 754–755.
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.
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.
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.
Kocher, T. D., 2004. Adaptive evolution and explosive speciation: the cichlid fish model. Nature Reviews Genetics 5: 288–298.
Kullander, S. O., 1983. Revision of the South American cichlid genus Cichlasoma. Swedish Museum of Natural History, Stockholm.
Kullander, S. O., 1986. Cichlid fishes of the Amazon River drainage of Peru. Swedish Museum of Natural History, Stockholm.
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.
Librado, P. & J. Rozas, 2009. DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25: 1451–1452.
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.
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.
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.
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.
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.
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.
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.
Pereira, R., 1986. Peixes de nossa terra, Primeira ed. Nobel, São Paulo.
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.
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.
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.
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.
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.
Posada, D., 2008. jModelTest: phylogenetic model averaging. Molecular Biology and Evolution 25: 1253–1256.
Puillandre, N., A. Lambert, S. Brouillet & G. Achaz, 2012. ABGD, Automatic Barcode Gap Discovery for primary species delimitation. Molecular Ecology 21: 1864–1877.
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.
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.
Saitou, N. & M. Nei, 1987. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Molecular Biology and Evolution 4: 406–425.
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.
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.
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.
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.
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.
Ward, R. D., 2009. DNA barcode divergence among species and genera of birds and fishes. Molecular Ecology Resources 9: 1077–1085.
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.
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.
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.
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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)
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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
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DOI: https://doi.org/10.1007/s10750-017-3482-y