Hostname: page-component-76fb5796d-45l2p Total loading time: 0 Render date: 2024-04-25T12:55:20.674Z Has data issue: false hasContentIssue false

DNA barcoding reveals cryptic diversity and peculiar phylogeographic patterns in mojarras (Perciformes: Gerreidae) from the Caribbean and South-western Atlantic

Published online by Cambridge University Press:  30 January 2020

Uedson Pereira Jacobina*
Affiliation:
Laboratório de Ictiologia e Conservação, Campus-Penedo/Universidade Federal de Alagoas, Avenida Beira Rio s/n, PenedoCEP 57200-000, Alagoas, Brazil
Rodrigo Augusto Torres
Affiliation:
Laboratório de Genômica Evolutiva e Ambiental, Departamento de Zoologia, Universidade Federal de Pernambuco, Av Prof. Nelson Chaves s/n, Cidade Universitária, CEP 50670-420, Recife, Pernambuco, Brasil
Paulo Roberto Antunes de Mello Affonso
Affiliation:
Department of Biological Sciences, Universidade Estadual do Sudoeste da Bahia, Av. José Moreira Sobrinho, s/n, Jequiezinho, 45206190, Jequié, Bahia, Brazil
Ewerton Vieira dos Santos
Affiliation:
Laboratório de Ictiologia e Conservação, Campus-Penedo/Universidade Federal de Alagoas, Avenida Beira Rio s/n, PenedoCEP 57200-000, Alagoas, Brazil
Leonardo Luiz Calado
Affiliation:
Laboratório de Genética de Recursos Marinhos, Universidade Federal do Rio Grande do Norte, Av. Senador Salgado Filho, S/N, Campus Universitário, 59078970, Natal, Rio Grande do Norte, Brazil
Jamille de Araújo Bitencourt
Affiliation:
Department of Biological Sciences, Universidade Estadual do Sudoeste da Bahia, Av. José Moreira Sobrinho, s/n, Jequiezinho, 45206190, Jequié, Bahia, Brazil
*
Author for correspondence: Uedson Pereira Jacobina, E-mail: uedson.jacobina@penedo.ufal.br

Abstract

The mojarras (Eucinostomus) are a widespread group of coastal fishes of controversial taxonomy because of similarities in their external morphology. In the present study, we assessed the genetic diversity of species and populations of Eucinostomus using DNA barcodes using a systematic and phylogeographic context. In total, 416 COI sequences of all valid Eucinostomus representatives were analysed based on public databases and collected specimens from the north-eastern coast of Brazil (Western South Atlantic). Several cases of misidentification were detected in the barcode dataset (E. argenteus, E. harengulus, E. gula, E. dowii and E. jonesii) that could account for the taxonomic issues in this genus. In contrast, we identified four molecular operational taxonomic units (MOTUs), with divergence above 2% in the Western Atlantic, that correspond to cryptic forms within E. argenteus, E. harengulus, E. gula and E. melanopterus. These data suggest that Plio-Pleistocene events (rise of the Panama isthmus, Amazonas outflow and sea-level fluctuations) played a major role in the diversification of mojarras. While subtle morphological differences have been used as proxies to discriminate Eucinostomus species, the genetic data proved to be efficient in differentiating them and revealing potentially undescribed taxa. Therefore, we recommend that further taxonomic studies in mojarras should incorporate DNA-based evidence.

Type
Research Article
Copyright
Copyright © Marine Biological Association of the United Kingdom 2020

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Argolo, LA, Ramos, RTC, Barreto, SB, Bitencourt, JA, Sampaio, I, Schneider, H and Affonso, PRAM (2018) The flounder next door: closer evolutionary relationship between allopatric than sympatric Bothus (Rafinesque, 1810) species (Pleuronectiformes, Bothidae). Zoologischer Anzeiger 277, 131142.CrossRefGoogle Scholar
Bacon, CD, Silvestro, D, Jaramillo, C, Smith, BT, Chakrabarty, P and Antonelli, A (2015) Biological evidence supports an early and complex emergence of the Isthmus of Panama. Proceedings of the National Academy of Sciences USA 112, 61106115.CrossRefGoogle ScholarPubMed
Barreira, AS, Lijtmaer, DA and Tubaro, PL (2016) The multiple applications of DNA barcodes in avian evolutionary studies. Genome 59, 899911.CrossRefGoogle ScholarPubMed
Bickford, D, Lohman, DJ, Sodhi, NS, Ng, PKL, Meier, R, Winker, K, Ingram, KK and Das, I (2007) Cryptic species as a window on diversity and conservation. Trends in Ecology & Evolution 22, 148155.CrossRefGoogle ScholarPubMed
Blessing, JJ, Marshall, JC and Balcombe, SR (2010) Humane killing of fishes for scientific research: a comparison of two methods. Journal of Fish Biology 76, 25712577.CrossRefGoogle ScholarPubMed
Brandão, JHSG, de Bitencourt, JA, Santos, FB, Watanabe, LA, Schneider, H, Sampaio, I and de Affonso, PRAM (2016) DNA barcoding of coastal ichthyofauna from Bahia, northeastern Brazil, South Atlantic: high efficiency for systematics and identification of cryptic diversity. Biochemical Systematics and Ecology 65, 214224.CrossRefGoogle Scholar
Brown, SDJ, Collins, RA, Boyer, S, Lefort, M, Malumbres-Olarte, J, Vink, CJ and Cruickshank, RH (2012) Spider: an R package for the analysis of species identity and evolution, with particular reference to DNA barcoding. Molecular Ecology Resources 12, 562565.CrossRefGoogle Scholar
Calado, LL, Bertollo, LAC, Cioffi, MB, Costa, GWWF, Jacobina, UP and Molina, WF (2014) Evolutionary dynamics of rDNA genes on chromosomes of the Eucinostomus fishes: cytotaxonomic and karyoevolutive implications. Genetics and Molecular Research 13, 99519959.CrossRefGoogle ScholarPubMed
Da Silva, WC, Marceniuk, AP, Sales, JBL and Araripe, J (2016) Early Pleistocene lineages of Bagre bagre (Linnaeus, 1766) (Siluriformes: Ariidae), from the Atlantic coast of South America, with insights into the demography and biogeography of the species. Neotropical Ichthyology 14, e150184.CrossRefGoogle Scholar
Da Silva, TF, Schneider, H, Sampaio, I, Angulo, A, Brito, MFG, de Santos, ACA, Santos, JA, de Carvalho-Filho, A and Santos, S (2018) Phylogeny of the subfamily Stelliferinae suggests speciation in Ophioscion Gill, 1863 (Sciaenidae: Perciformes) in the western South Atlantic. Molecular Phylogenetics and Evolution 125, 5161.CrossRefGoogle Scholar
De Biasse, MB, Richards, VP, Shivji, MS and Hellberg, ME (2016) Shared phylogeographical breaks in a Caribbean coral reef sponge and its invertebrate commensals. Journal of Biogeography 43, 21362146.CrossRefGoogle Scholar
De La Cruz-Agüero, J (2013) The caudal skeleton of mojarras from genus Eucinostomus (Perciformes: Gerreidae) and related species. Journal of Ichthyology 53, 9941006.CrossRefGoogle Scholar
de la Cruz-Agüero, J and Galvan-Magana, F (1993) Morphological discrimination of Eucinostomus spp. from the Pacific coast of Mexico. Bulletin of Marine Science 52, 819824.Google Scholar
de Ribeiro, AO, Caires, RA, Mariguela, TC, Pereira, LHG, Hanner, R and Oliveira, C (2012) DNA barcodes identify marine fishes of São Paulo State, Brazil. Molecular Ecology Resources 12, 10121020.CrossRefGoogle Scholar
Drummond, AJ and Rambaut, A (2007) BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evolutionary Biology 7, 214.CrossRefGoogle ScholarPubMed
Drummond, AJ, Suchard, MA, Xie, D and Rambaut, A (2012) Bayesian phylogenetics with BEAUti and the BEAST 1.7. Molecular Biology and Evolution 29, 19691973.CrossRefGoogle ScholarPubMed
Ferreira, M, Kavalco, KF, de Almeida-Toledo, LF and Garcia, C (2014) Cryptic diversity between two Imparfinis species (Siluriformes, Heptapteridae) by cytogenetic analysis and DNA barcoding. Zebrafish 11, 3063017.CrossRefGoogle ScholarPubMed
Fields, AT, Feldheim, KA, Gelsleichter, J, Pfoertner, C and Chapman, DD (2016) Population structure and cryptic speciation in bonnethead sharks Sphyrna tiburo in the south-eastern USA and Caribbean. Journal of Fish Biology 89, 22192233.CrossRefGoogle Scholar
Froese, R and Pauly, D (2019) Fish Base. www.fishbase.org.Google Scholar
Hurtado, LA, Mateos, M and Liu, S (2017) Phylogeographic patterns of a lower intertidal isopod in the Gulf of California and the Caribbean and comparison with other intertidal isopods. Ecology and Evolution 7, 346357.CrossRefGoogle ScholarPubMed
Hyde, JR, Underkoffler, KE and Sundberg, MA (2014) DNA barcoding provides support for a cryptic species complex within the globally distributed and fishery important opah (Lampris guttatus). Molecular Ecology Resources 14, 12391247.CrossRefGoogle 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, Meintjes, P and Drummond, A (2012) Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics (Oxford, England) 28, 16471649.CrossRefGoogle ScholarPubMed
Kenchington, EL, Baillie, SM, Kenchington, TJ and Bentzen, P (2017) Barcoding Atlantic Canada's mesopelagic and upper bathypelagic marine fishes. PLoS ONE 12, e0185173.CrossRefGoogle ScholarPubMed
Lambeck, K and Chappell, J (2001) Sea level change through the last glacial cycle. Science 292, 679686.CrossRefGoogle ScholarPubMed
Landi, M, Dimech, M, Arculeo, M, Biondo, G, Martins, R, Carneiro, M, Carvalho, GR, Lo Brutto, S and Costa, FO (2014) DNA barcoding for species assignment: the case of Mediterranean marine fishes. PLoS ONE 9, e106135.CrossRefGoogle ScholarPubMed
Lanfear, R, Calcott, B, Ho, SYW and Guindon, S (2012) Partitionfinder: combined selection of partitioning schemes and substitution models for phylogenetic analyses. Molecular Biology and Evolution 29, 16951701.CrossRefGoogle ScholarPubMed
Leigh, JW and Bryant, D (2015) Popart: full-feature software for haplotype network construction. Methods in Ecology and Evolution 6, 11101116.CrossRefGoogle Scholar
Luiz, OJ, Madin, JS, Robertson, DR, Rocha, LA, Wirtz, P and Floeter, SR (2012) Ecological traits influencing range expansion across large oceanic dispersal barriers: insights from tropical Atlantic reef fishes. Proceedings of the Royal Society of London B: Biological Sciences 279, 10331040.CrossRefGoogle ScholarPubMed
Luo, A, Ling, C, Ho, SYW and Zhu, C-D (2018) Comparison of methods for molecular species delimitation across a range of speciation scenarios. Systematic Biology 67, 830846. doi: 10.1093/sysbio/syy011.CrossRefGoogle ScholarPubMed
Matheson, RE Jr and McEachran, JD (1984) Taxonomic studies of the Eucinostomus argenteus complex (Pisces: Gerreidae): preliminary studies of external morphology. Copeia 4, 893902.CrossRefGoogle Scholar
Mayden, RL (1997) A hierarchy of species concepts: the denouement in the saga of the species problem. In Claridge, MF, Dawah, HA and Wilson, MR (eds), Species: The Units of Diversity. London: Chapman & Hall, pp. 381423.Google Scholar
Müller, RD, Sdrolias, M, Gaina, C, Steinberger, B and Heine, C (2008) Long-term sea-level fluctuations driven by ocean basin dynamics. Science 319, 13571362.CrossRefGoogle ScholarPubMed
Nelson, JS, Grande, TC and Wilson, MVH (2016) Fishes of the World. New York, NY: John Wiley & Sons.CrossRefGoogle Scholar
Neves, JMM, Lima, SMQ, Mendes, LF, Torres, RA, Pereira, RJ and Mott, T (2016) Population structure of the rockpool blenny Entomacrodus vomerinus shows source-sink dynamics among ecoregions in the tropical Southwestern Atlantic. PLoS ONE 11, e0157472.CrossRefGoogle ScholarPubMed
Nirchio, M, Paim, FG, Milana, V, Rossi, AR and Oliveira, C (2018) Identification of a new mullet species complex based on an integrative molecular and cytogenetic investigation of Mugil hospes (Mugilidae: Mugiliformes). Frontiers in Genetics 9, 17.CrossRefGoogle Scholar
O'Dea, A, Lessios, HA, Coates, AG, Eytan, RI, Restrepo-Moreno, SA, Cione, AL, Collins, LS, de Queiroz, A, Farris, DW, Norris, RD, Stallard, RF, Woodburne, MO, Aguilera, O, Aubry, M-P, Berggren, WA, Budd, AF, Cozzuol, MA, Coppard, SE, Duque-Caro, H, Finnegan, S, Gasparini, GM, Grossman, EL, Johnson, KG, Keigwin, LD, Knowlton, N, Leigh, EG, Leonard-Pingel, JS, Marko, PB, Pyenson, ND, Rachello-Dolmen, PG, Soibelzon, E, Soibelzon, L, Todd, JA, Vermeij, GJ and Jackson, JBC (2016) Formation of the Isthmus of Panama. Science Advances 2, e1600883.CrossRefGoogle ScholarPubMed
Pappalardo, AM, Cuttitta, A, Sardella, A, Musco, M, Maggio, T, Patti, B, Mazzola, S and Ferrito, V (2015) DNA barcoding and COI sequence variation in Mediterranean lanternfishes larvae. Hydrobiologia 749, 155167.CrossRefGoogle Scholar
Pinheiro, HT, Rocha, LA, Macieira, RM, Carvalho-Filho, A, Anderson, AB, Bender, MG, Carlos, FDD, Ferreira, EL, Figueiredo-Filho, J, Francini-Filho, R, Gasparini, JL, Joyeux, J, Luiz, OJ, Mincarone, MM, Moura, RL, de Nunes, JACC, Quimbayo, JP, Rosa, RS, Sampaio, CLS, Sazima, I, Simon, T, Vila-Nova, DA, Floeter, SR and Treml, E (2018) South-western Atlantic reef fishes: zoogeographical patterns and ecological drivers reveal a secondary biodiversity centre in the Atlantic Ocean. Diversity and Distributions 24, 951965.CrossRefGoogle Scholar
Pons, J, Barraclough, TG, Gomez-Zurita, J, Cardoso, A, Duran, DP, Hazell, S, Kamoun, S, Sumlin, WD and Vogler, AP (2006) Sequence-based species delimitation for the DNA taxonomy of undescribed insects. Systematic Biology 55, 595609.CrossRefGoogle ScholarPubMed
Puillandre, N, Lambert, A, Brouillet, S and Achaz, G (2012) ABGD, Automatic Barcode Gap Discovery for primary species delimitation. Molecular Ecology 21, 18641877.CrossRefGoogle ScholarPubMed
Rambaut, A and Drummond, AJ (2009) FigTree version 1.3. 1. http://Tree. Bio. Ed. Ac. Uk/Software/Figtree/.Google Scholar
Ratnasingham, S and Hebert, PDN (2013) A DNA-based registry for all animal species: the Barcode Index Number (BIN) system. PLoS ONE 8, e66213.CrossRefGoogle ScholarPubMed
Rocha, LA (2003) Patterns of distribution and processes of speciation in Brazilian reef fishes. Journal of Biogeography 30, 11611171.CrossRefGoogle Scholar
Rocha, L, Claudia, R, Ross, RD and Brian, B (2008) Comparative phylogeography of Atlantic reef fishes indicates both origin and accumulation of diversity in the Caribbean. BMC Evolutionary Biology 8, 157.CrossRefGoogle ScholarPubMed
Stamatakis, A, Aberer, AJ, Goll, C, Smith, SA, Berger, SA and Izquierdo-Carrasco, F (2012) RAxML-Light: a tool for computing terabyte phylogenies. Bioinformatics (Oxford, England) 28, 20642066.CrossRefGoogle ScholarPubMed
Tamura, K, Stecher, G, Peterson, D, Filipski, A and Kumar, S (2013) MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Molecular Biology and Evolution 30, 27252729.CrossRefGoogle ScholarPubMed
Thacker, CE (2017) Patterns of divergence in fish species separated by the Isthmus of Panama. BMC Evolutionary Biology 17, 111.CrossRefGoogle ScholarPubMed
Valdez-Moreno, M, Vásquez-Yeomans, L, Elías-Gutiérrez, M, Ivanova, NV and Hebert, PDN (2010) Using DNA barcodes to connect adults and early life stages of marine fishes from the Yucatan Peninsula, Mexico: potential in fisheries management. Marine and Freshwater Research 61, 655671.CrossRefGoogle Scholar
Ward, RD, Zemlak, TS, Innes, BH, Last, PR and Hebert, PD (2005) DNA barcoding Australia's fish species. Philosophical Transactions of the Royal Society of London B: Biological Sciences 360, 18471857.CrossRefGoogle ScholarPubMed
Weigt, LA, Baldwin, CC, Driskell, A, Smith, DG, Ormos, A and Reyier, EA (2012) Using DNA barcoding to assess Caribbean reef fish biodiversity: expanding taxonomic and geographic coverage. PLoS ONE 7, e41059.CrossRefGoogle ScholarPubMed
Williams, ST and Duda, TF Jr (2008) Did tectonic activity stimulate Oligo–Miocene speciation in the Indo-West Pacific? Evolution: International Journal of Organic Evolution 62, 16181634.CrossRefGoogle ScholarPubMed
Williams, ST, Smith, LM, Herbert, DG, Marshall, BA, Warén, A, Kiel, S, Dyal, P, Linse, K, Vilvens, C and Kano, Y (2013) Cenozoic climate change and diversification on the continental shelf and slope: evolution of gastropod diversity in the family Solariellidae (Trochoidea). Ecology and Evolution 3, 887917.CrossRefGoogle Scholar
Winker, K (2005) Sibling species were first recognized by William Derham (1718). The Auk 122, 706707.CrossRefGoogle Scholar
Winterbottom, R, Hanner, R, Burridge, M and Zur, M (2014) A cornucopia of cryptic species – a DNA barcode analysis of the gobiid fish genus Trimma (Percomorpha, Gobiiformes). ZooKeys 381, 79111. https://doi.org/10.3897/zookeys.381.6445.CrossRefGoogle Scholar
Woodland, DJ (2006) Gerreidae. Silver-biddies. In Carpenter, KE and Niem, V (eds), FAO species Identification Guide for Fishery Purposes. The Living Marine Resources of the Western Central Pacific, 6th Edn.Rome: FAO, pp. 29462960.Google Scholar
Zhang, J, Kapli, P, Pavlidis, P and Stamatakis, A (2013) A general species delimitation method with applications to phylogenetic placements. Bioinformatics (Oxford, England) 29, 28692876.CrossRefGoogle ScholarPubMed
Supplementary material: File

Jacobina et al. supplementary material

Jacobina et al. supplementary material 1

Download Jacobina et al. supplementary material(File)
File 21.3 KB
Supplementary material: File

Jacobina et al. supplementary material

Jacobina et al. supplementary material 2

Download Jacobina et al. supplementary material(File)
File 12.1 KB