Reviews in Fish Biology and Fisheries

, Volume 19, Issue 2, pp 217–231

Molecular phylogeny of Mugilidae fishes revised

  • Sandra Heras
  • María Inés Roldán
  • Mariano González Castro
Research Paper

Abstract

Systematics derived from morphological characters often does not correspond with the evolutionary processes underlying the divergence within a group of organisms. In the family Mugilidae (Teleostei) morphological similarities have resulted in inconsistencies between taxonomy and phylogeny among its species, and particularly for the genera Mugil, Liza and Chelon where both intrageneric and intergeneric phylogenetic clarifications are needed. To address these issues, the direct sequencing of the mitochondrial region that encodes Phenylalanine (69 bp), 12S rRNA (842 bp), cytochrome c oxidase subunit I (651 bp) and cytochrome b (702 bp) was carried out. The data reveal that Mugil platanus and Mugil liza represent a continuum of a single species, closely related to but distinct from Mugil cephalus which itself appears to comprise a grouping of multiple and closely related species. This species complex was genetically distinct from Mugil curema, which, based on three clearly diverged species identified in this study along the Atlantic coast of the Americas, requires extensive taxonomic revision throughout its world-wide distribution. Unlike the monophyly supported within Mugil, relationships within Liza are paraphyletic, and a taxonomic revision of the genera Liza, Chelon and Oedalechilus is needed.

Keywords

Phe 12S rRNA Cytochrome b COI Mugilidae phylogeny Taxonomy 

References

  1. Agapow PM, Bininda-Edmonds ORP, Crandall KA, Gittleman JL, Mace GM, Marshall JC, Purvis A (2004) The impact of species concept on biodiversity studies. Q Rev Biol 79:162–179CrossRefGoogle Scholar
  2. Avise JC (1994) Why employ molecular genetic markers? In: molecular markers, natural history and evolution. Chapman and Hall, New York, pp 5–15Google Scholar
  3. Avise JC, Walker D (2000) Abandon all species concepts? A response. Conserv Genet 1:77–88CrossRefGoogle Scholar
  4. Bernardi G, Goswami U (1997) Molecular evidence for cryptic species among the Antarctic fish Trematomus vernacchii and Trematomus hansoni. Antarct Sci 4:81–385Google Scholar
  5. Briggs JC (1960) Fishes of worldwide (circumtropical) distribution. Copeia 3:171–180CrossRefGoogle Scholar
  6. Caldara F, Bargelloni L, Ostellari L, Penzo E, Colombo L, Patarnello T (1996) Molecular phylogeny of grey mullets based on mitochondrial DNA sequence analysis: evidence of a differential rate of evolution at the intrafamily level. Mol Phylogenet Evol 6:416–424PubMedCrossRefGoogle Scholar
  7. Cousseau MB, González Castro M, Figueroa DE, Gosztonyi AE (2005) Does Mugil liza Valenciennes 1836 (Teleostei: Mugiliformes) occur in Argentinean waters? Rev Biol Mar Oceanogr 40:133–140CrossRefGoogle Scholar
  8. Crosetti D, Nelson WS, Avise JC (1994) Pronounced genetic structure of mitochondrial DNA among populations of the circumglobally distributed grey mullet (Mugil cephalus). J Fish Biol 44:47–58CrossRefGoogle Scholar
  9. Eiras-Stofella DR, Charvet-Almeida P, Fanta E, Vianna AC (2001) Surface ultrastructure of the gills of the mullets Mugil curema, M. liza and M. platanus (Mugilidae, Pisces). J Morphol 2:122–133CrossRefGoogle Scholar
  10. FAO (2004) Species identification sheet: Mugil cephalus. www.fao.org/figis/servlet/FiRerServlet
  11. FAO (2005) Fishery statistics. http://www.fao.org/fi/statist
  12. Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791CrossRefGoogle Scholar
  13. Fontdevila A, Moya A (2003) La especiación: modelos y casos de estudio. In: evolución: origen, adaptación y divergencia de las especies. Síntesis, Madrid, pp 165–224Google Scholar
  14. Fraga E, Schneider H, Nirchio M, Santa-Brigida E, Rodrigues-Filho LF, Sampaio I (2007) Molecular phylogenetic analyses of mullets (Mugilidae, Mugiliformes) based on two mitochondrial genes. J Appl Ichthyol 23:598–604CrossRefGoogle Scholar
  15. Gilbert CR (1993) Geographic distribution of the striped mullet (Mugil cephalus) in the Atlantic and Eastern Pacific oceans. Fla Sci 56:204–210Google Scholar
  16. González Castro M, Díaz de Astarloa JM, Cousseau MB (2006) First record of a tropical affinity mullet, Mugil curema (Mugilidae), in a temperate southwestern Atlantic coastal lagoon. Cybium 30:90–91Google Scholar
  17. González Castro M, Heras S, Cousseau MB, Roldán MI (2008) Assessing species validity of Mugil platanus Günther, 1880 in relation to Mugil cephalus Linnaeus, 1758 (Actinopterygii). Ital J Zool 75:319–325CrossRefGoogle Scholar
  18. Gornung E, Cordisco CA, Rossi AR, De Innocentiis S, Crosetti D, Sola L (2001) Chromosomal evolution in Mugilidae: karyotype characterization of Liza saliens and comparative localization of major and minor ribosomal genes in the six Mediterranean mullets. Mar Biol 139:55–60CrossRefGoogle Scholar
  19. Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl Acids Symp Ser 41:95–98Google Scholar
  20. Harrison IJ (2002) Mugilidae: mullets. In: Carpenter K (ed) The living marine resources of the western central Atlantic, vol 2. Bony fishes part 1 (Acipenseridae to Grammatidae). FAO species identification guide for fisheries purposes. FAO, Rome, pp 1071–1085Google Scholar
  21. Harrison IJ, Howes GJ (1991) The pharyngobranchial organ of mugilid fishes; its structure, variability, ontogeny, possible function and taxonomic utility. Bull Br Mus Nat Hist (Zool) 5:111–132Google Scholar
  22. Harrison IJ, Nirchio M, Oliveireas C, Ron E, Gaviria J (2007) A new species of mullet (Teleostei: Mugilidae) from Venezuela, with a discussion on the taxonomy of Mugil gaimardianus. J Fish Biol 71:76–97CrossRefGoogle Scholar
  23. Hendry AP, Vamosi SM, Latham SJ, Heilbuth JC, Day T (2000) Questioning species realities. Conserv Genet 1:67–76CrossRefGoogle Scholar
  24. Heras S, González Castro M, Roldán MI (2006) Mugil curema in Argentinean waters: combined morphological and molecular approach. Aquaculture 261:473–478CrossRefGoogle Scholar
  25. Heras S, Roldán MI, González Castro M, Cousseau MB (2007) Mugil cephalus: cosmopolitan species or species complex? Rapp Comm Int Mer Méditerr 38:499Google Scholar
  26. Hey J (2001) Genes categories and species: the evolutionary and cognitive cases of the species problem. Oxford Univ Press, NYGoogle Scholar
  27. Johns GC, Avise C (1998) A comparative summary of genetic distances in the vertebrates from the mitochondrial cytochrome b gene. Mol Biol Evol 15:1481–1490PubMedGoogle Scholar
  28. Knowlton N (1993) Sibling species in the sea. Annu Rev Ecol Syst 24:189–216CrossRefGoogle Scholar
  29. Kocher TD, Thomas WK, Meyer A, Edwards SV, Paabo S, Villablanca FX, Wilson AC (1989) Dynamics of mitochondrial DNA evolution in animals: amplification and sequencing with conserved primers. Proc Natl Acad Sci USA 86:6196–6200PubMedCrossRefGoogle Scholar
  30. Kumar S, Tamura K, Nei M (2004) MEGA3: integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief Bioinf 5:150–163CrossRefGoogle Scholar
  31. Lefébure T, Douady CJ, Malard F, Gibert J (2007) Testing dispersal and cryptic diversity in a widely distributed groundwater amphipod (Niphargus rhenorhodanensis). Mol Phylogenet Evol 42:676–686PubMedCrossRefGoogle Scholar
  32. LeGrande WH, Fitzsimons JM (1976) Karyology of the mullets Mugil curema and Mugil cephalus (Perciformes: Mugilidae) from Louisiana. Copeia 2:388–391CrossRefGoogle Scholar
  33. Maddison WP (1996) Molecular approaches and the growth of phylogenetic biology. In: Ferraris JD, Palumbi SR (eds) Molecular zoology. Wiley, New York, pp 47–61Google Scholar
  34. Menezes NA (1983) Guia prático para conhecimento e identificação das tainhas e paratis (Pisces, Mugilidae) do litoral brasileiro. Rev Bras Zool 2:1–12CrossRefGoogle Scholar
  35. Miya M, Nishida M (1999) Organization of the mitochondrial genome of a deep-sea fish, Gonostoma gracile (Teleostei: Stomiiformes): first example of transfer RNA gene rearrangements in bony fishes. Mar Biotechnol 1:416–426PubMedCrossRefGoogle Scholar
  36. Miya M, Nishida M (2000) Use of mitogenomic information in teleostean molecular phylogenetics: a tree-based exploration under the maximum-parsimony optimality criterion. Mol Phylogenet Evol 17:437–455PubMedCrossRefGoogle Scholar
  37. Miya M, Kawaguchi A, Nishida M (2001) Mitogenomic exploration of higher teleostean phylogenies: a case study for moderate-scale evolutionary genomics with 38 newly determined complete mitochondrial DNA sequences. Mol Biol Evol 18:1993–2009PubMedGoogle Scholar
  38. Nelson JS (2006) Fishes of the world, 4th edn. Wiley, New York, pp 262–263Google Scholar
  39. Nirchio M, Cequea H (1998) Karyology of Mugil liza and M. curema from Venezuela. Bol Inv Mar Cost 27:45–50Google Scholar
  40. Nirchio M, Cervigón F, Revelo Porto JI, Pérez JE, Gómez JA, Villalaz J (2003) Karyotype supporting Mugil curema Valenciennes, 1836 and Mugil gaimardianus Desmarest, 1831 (Mugilidae: Teleostei) as two valid nominal species. Sci Mar 67:113–115CrossRefGoogle Scholar
  41. Nirchio M, Cipriano R, Cestari M, Fenocchio A (2005) Cytogenetical and morphological features reveal significant differences among Venezuelan and Brazilian samples of Mugil curema (Teleostei: Mugilidae). Neotrop Ichthyol 3:99–102CrossRefGoogle Scholar
  42. Nirchio M, Oliveira C, Ferreira IA, Pérez JE, Gaviria JI, Harrison I, Rossi AR, Sola L (2007) Comparative cytogenetic and allozyme analysis of Mugil rubrioculus and M. curema (Teleostei: Mugilidae) from Venezuela. Interciencia 32:757–762Google Scholar
  43. Nylander JAA (2004) MrModeltest v2. Program distributed by the author. Evolutionary biology centre, Uppsala UniversityGoogle Scholar
  44. Palumbi S, Martin A, Romano S, McMillan WO, Stice L, Grabowski G (1991) The simple fool’s guide to PCR, version 2.0. Department of Zoology and Kewalo Marine Laboratory, University of Hawaii, HonoluluGoogle Scholar
  45. Papasotiropoulos V, Klossa-Kilia E, Kilias G, Alahiotis S (2001) Genetic divergence and phylogenetic relationships in grey mullets (Teleostei: Mugilidae) using allozyme data. Biochem Genet 39:155–168PubMedCrossRefGoogle Scholar
  46. Papasotiropoulos V, Klossa-Kilia E, Kilias G, Alahiotis S (2002) Genetic divergence and phylogenetic relationships in grey mullets (Teleostei: Mugilidae) based on PCR–RFLP analysis of mtDNA segments. Biochem Genet 40:71–86PubMedCrossRefGoogle Scholar
  47. Papasotiropoulos V, Klossa-Kilia E, Kilias G, Alahiotis S, Kilias G (2007) Molecular phylogeny of grey mullets (Teleostei: Mugilidae) in Greece: evidence from sequence analysis of mtDNA segments. Biochem Genet 45:623–636PubMedCrossRefGoogle Scholar
  48. Peregrino-Uriarte AB, Pacheco-Aguilar R, Varela-Romero A, Yepiz-Plasencia G (2007) Differences in the 16S rRNA and cytochrome c oxidase subunit I genes in the mullets Mugil cephalus and Mugil curema, and snooks Centropomus viridis and Centropomus robalito. Cienc Mar 33:95–104Google Scholar
  49. Posada D, Crandall KA (1998) Modeltest: testing the model of DNA substitution. Bioinformatics 14:817–818PubMedCrossRefGoogle Scholar
  50. Price PW (1996) Species concept. In: biological evolution. Saunders College Publishing, Philadelphia, pp 59–73Google Scholar
  51. Rivas LR (1980) Synopsis of knowledge on the taxonomy, biology, distribution, and fishery of the Gulf of Mexico mullets (Pisces: Mugilidae). In: Flandorfer M, Skupien L (eds) Proceedings of a workshop for potential fishery resources of the northern Gulf of Mexico. Mississippi–Alabama Sea grant consortium publication MASGP-80-012, pp 34–53Google Scholar
  52. Rocha-Olivares A, Garber NM, Stuck KC (2000) High genetic diversity, large inter-oceanic divergence and historical demography of the striped mullet. J Fish Biol 57:1134–1149CrossRefGoogle Scholar
  53. Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574PubMedCrossRefGoogle Scholar
  54. Rossi AR, Capula M, Crosetti D, Sola L, Campton DE (1998a) Allozyme variation in global populations of striped mullet, Mugil cephalus (Pisces: Mugilidae). Mar Biol 131:203–212CrossRefGoogle Scholar
  55. Rossi AR, Capula M, Crosetti D, Campton DE, Sola L (1998b) Genetic divergence and phylogenetic inferences in five species of Mugilidae (Pisces: Perciformes). Mar Biol 131:213–218CrossRefGoogle Scholar
  56. Rossi AR, Ungaro A, De Innocentiis S, Crosetti D, Sola L (2004) Phylogenetic analysis of Mediterranean mugilids by allozymes and 16S mt-rRNA genes investigation: are the Mediterranean species of Liza monophyletic? Biochem Genet 42:301–315PubMedCrossRefGoogle Scholar
  57. Semina AV, Polyakova NE, Brykov VA (2007) Analysis of mitochondrial DNA: taxonomic phylogenetic relationships in two fish taxa (Pisces: Mugilidae and Cyprinidae). Biochemistry (Moscow) 72:1349–1355CrossRefGoogle Scholar
  58. Swofford DL (2002) PAUP* Phylogenetic analysis using parsimony (*and other methods), version 4. Sinauer Associates, SunderlandGoogle Scholar
  59. Tamura K, Nei M (1993) Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol Biol Evol 10:512–526PubMedGoogle Scholar
  60. Thomson JM (1997) The Mugilidae of the world. Mem Qld Mus 41:457–562Google Scholar
  61. Tiedemann R, Harder J, Gmeiner C, Haase E (1996) Mitochondrial DNA sequence patterns of Harbour porpoises (Phocoena phocoena) from the North and the Baltic Sea. Z Säugetierkunde 61:104–111Google Scholar
  62. Turan C, Caliskan M, Kucuktas H (2005) Phylogenetic relationships of nine mullet species (Mugilidae) in the Mediterranean Sea. Hydrobiologia 532:45–51CrossRefGoogle Scholar
  63. Ward RD, Zemlak TS, Innes BH, Last PR, Hebert PDN (2005) DNA barcoding Australia’s fish species. Philos Trans R Soc Lond B Biol Sci 360:1847–1857PubMedCrossRefGoogle Scholar
  64. Xia X, Xie Z (2001) DAMBE: data analysis in molecular biology and evolution. J Hered 92:371–373PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2008

Authors and Affiliations

  • Sandra Heras
    • 1
  • María Inés Roldán
    • 2
  • Mariano González Castro
    • 3
  1. 1.Laboratori d’Ictiologia Genètica, Facultat de CiènciesUniversitat de GironaGironaSpain
  2. 2.Laboratori d’Ictiologia Genètica, Facultat de CiènciesUniversitat de GironaGironaSpain
  3. 3.Laboratorio de Ictiología, Departamento de Ciencias MarinasUniversidad Nacional de Mar del PlataMar del PlataArgentina

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