Skip to main content Accessibility help
×
Home

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

  • Uedson Pereira Jacobina (a1), Rodrigo Augusto Torres (a2), Paulo Roberto Antunes de Mello Affonso (a3), Ewerton Vieira dos Santos (a1), Leonardo Luiz Calado (a4) and Jamille de Araújo Bitencourt (a3)...

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.

Copyright

Corresponding author

Author for correspondence: Uedson Pereira Jacobina, E-mail: uedson.jacobina@penedo.ufal.br

References

Hide All
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.
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.
Barreira, AS, Lijtmaer, DA and Tubaro, PL (2016) The multiple applications of DNA barcodes in avian evolutionary studies. Genome 59, 899911.
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.
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.
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.
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.
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.
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.
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.
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.
De La Cruz-Agüero, J (2013) The caudal skeleton of mojarras from genus Eucinostomus (Perciformes: Gerreidae) and related species. Journal of Ichthyology 53, 9941006.
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.
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.
Drummond, AJ and Rambaut, A (2007) BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evolutionary Biology 7, 214.
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.
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.
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.
Froese, R and Pauly, D (2019) Fish Base. www.fishbase.org.
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.
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.
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.
Kenchington, EL, Baillie, SM, Kenchington, TJ and Bentzen, P (2017) Barcoding Atlantic Canada's mesopelagic and upper bathypelagic marine fishes. PLoS ONE 12, e0185173.
Lambeck, K and Chappell, J (2001) Sea level change through the last glacial cycle. Science 292, 679686.
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.
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.
Leigh, JW and Bryant, D (2015) Popart: full-feature software for haplotype network construction. Methods in Ecology and Evolution 6, 11101116.
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.
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.
Matheson, RE Jr and McEachran, JD (1984) Taxonomic studies of the Eucinostomus argenteus complex (Pisces: Gerreidae): preliminary studies of external morphology. Copeia 4, 893902.
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.
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.
Nelson, JS, Grande, TC and Wilson, MVH (2016) Fishes of the World. New York, NY: John Wiley & Sons.
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.
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.
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.
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.
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.
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.
Puillandre, N, Lambert, A, Brouillet, S and Achaz, G (2012) ABGD, Automatic Barcode Gap Discovery for primary species delimitation. Molecular Ecology 21, 18641877.
Rambaut, A and Drummond, AJ (2009) FigTree version 1.3. 1. http://Tree. Bio. Ed. Ac. Uk/Software/Figtree/.
Ratnasingham, S and Hebert, PDN (2013) A DNA-based registry for all animal species: the Barcode Index Number (BIN) system. PLoS ONE 8, e66213.
Rocha, LA (2003) Patterns of distribution and processes of speciation in Brazilian reef fishes. Journal of Biogeography 30, 11611171.
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.
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.
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.
Thacker, CE (2017) Patterns of divergence in fish species separated by the Isthmus of Panama. BMC Evolutionary Biology 17, 111.
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.
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.
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.
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.
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.
Winker, K (2005) Sibling species were first recognized by William Derham (1718). The Auk 122, 706707.
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.
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.
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.

Keywords

Type Description Title
UNKNOWN
Supplementary Material

Jacobina et al. supplementary material
Jacobina et al. supplementary material 1

 Unknown (21 KB)
21 KB
UNKNOWN
Supplementary materials

Jacobina et al. supplementary material
Jacobina et al. supplementary material 2

 Unknown (12 KB)
12 KB

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

  • Uedson Pereira Jacobina (a1), Rodrigo Augusto Torres (a2), Paulo Roberto Antunes de Mello Affonso (a3), Ewerton Vieira dos Santos (a1), Leonardo Luiz Calado (a4) and Jamille de Araújo Bitencourt (a3)...

Metrics

Altmetric attention score

Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed