Skip to main content
SpringerLink
Log in

Molecular phylogeny of Mugilidae fishes revised

  • Research Paper
  • Published:
Reviews in Fish Biology and Fisheries Aims and scope Submit manuscript

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.

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
Fig. 4

Similar content being viewed by others

References

  • 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 79:162–179

    Article  Google Scholar 

  • Avise JC (1994) Why employ molecular genetic markers? In: molecular markers, natural history and evolution. Chapman and Hall, New York, pp 5–15

  • Avise JC, Walker D (2000) Abandon all species concepts? A response. Conserv Genet 1:77–88

    Article  CAS  Google Scholar 

  • Bernardi G, Goswami U (1997) Molecular evidence for cryptic species among the Antarctic fish Trematomus vernacchii and Trematomus hansoni. Antarct Sci 4:81–385

    Google Scholar 

  • Briggs JC (1960) Fishes of worldwide (circumtropical) distribution. Copeia 3:171–180

    Article  Google Scholar 

  • 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 6:416–424

    Article  PubMed  CAS  Google Scholar 

  • 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 40:133–140

    Article  Google Scholar 

  • 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 44:47–58

    Article  CAS  Google Scholar 

  • 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 2:122–133

    Article  Google Scholar 

  • FAO (2004) Species identification sheet: Mugil cephalus. www.fao.org/figis/servlet/FiRerServlet

  • FAO (2005) Fishery statistics. http://www.fao.org/fi/statist

  • Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791

    Article  Google Scholar 

  • Fontdevila A, Moya A (2003) La especiación: modelos y casos de estudio. In: evolución: origen, adaptación y divergencia de las especies. Síntesis, Madrid, pp 165–224

  • 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 23:598–604

    Article  CAS  Google Scholar 

  • Gilbert CR (1993) Geographic distribution of the striped mullet (Mugil cephalus) in the Atlantic and Eastern Pacific oceans. Fla Sci 56:204–210

    Google Scholar 

  • 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 30:90–91

    Google Scholar 

  • 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 75:319–325

    Article  Google Scholar 

  • 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 139:55–60

    Article  CAS  Google Scholar 

  • Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl Acids Symp Ser 41:95–98

    CAS  Google Scholar 

  • 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 1071–1085

    Google Scholar 

  • 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) 5:111–132

    Google Scholar 

  • 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 71:76–97

    Article  Google Scholar 

  • Hendry AP, Vamosi SM, Latham SJ, Heilbuth JC, Day T (2000) Questioning species realities. Conserv Genet 1:67–76

    Article  CAS  Google Scholar 

  • Heras S, González Castro M, Roldán MI (2006) Mugil curema in Argentinean waters: combined morphological and molecular approach. Aquaculture 261:473–478

    Article  CAS  Google Scholar 

  • Heras S, Roldán MI, González Castro M, Cousseau MB (2007) Mugil cephalus: cosmopolitan species or species complex? Rapp Comm Int Mer Méditerr 38:499

    Google Scholar 

  • Hey J (2001) Genes categories and species: the evolutionary and cognitive cases of the species problem. Oxford Univ Press, NY

    Google Scholar 

  • Johns GC, Avise C (1998) A comparative summary of genetic distances in the vertebrates from the mitochondrial cytochrome b gene. Mol Biol Evol 15:1481–1490

    PubMed  CAS  Google Scholar 

  • Knowlton N (1993) Sibling species in the sea. Annu Rev Ecol Syst 24:189–216

    Article  Google Scholar 

  • 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 86:6196–6200

    Article  PubMed  CAS  Google Scholar 

  • Kumar S, Tamura K, Nei M (2004) MEGA3: integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief Bioinf 5:150–163

    Article  CAS  Google Scholar 

  • 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 42:676–686

    Article  PubMed  CAS  Google Scholar 

  • LeGrande WH, Fitzsimons JM (1976) Karyology of the mullets Mugil curema and Mugil cephalus (Perciformes: Mugilidae) from Louisiana. Copeia 2:388–391

    Article  Google Scholar 

  • Maddison WP (1996) Molecular approaches and the growth of phylogenetic biology. In: Ferraris JD, Palumbi SR (eds) Molecular zoology. Wiley, New York, pp 47–61

    Google Scholar 

  • Menezes NA (1983) Guia prático para conhecimento e identificação das tainhas e paratis (Pisces, Mugilidae) do litoral brasileiro. Rev Bras Zool 2:1–12

    Article  Google Scholar 

  • 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 1:416–426

    Article  PubMed  CAS  Google Scholar 

  • 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 17:437–455

    Article  PubMed  CAS  Google Scholar 

  • 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 18:1993–2009

    PubMed  CAS  Google Scholar 

  • Nelson JS (2006) Fishes of the world, 4th edn. Wiley, New York, pp 262–263

    Google Scholar 

  • Nirchio M, Cequea H (1998) Karyology of Mugil liza and M. curema from Venezuela. Bol Inv Mar Cost 27:45–50

    Google Scholar 

  • 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 67:113–115

    Article  Google Scholar 

  • 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 3:99–102

    Article  Google Scholar 

  • 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 32:757–762

    Google Scholar 

  • Nylander JAA (2004) MrModeltest v2. Program distributed by the author. Evolutionary biology centre, Uppsala University

  • 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, Honolulu

    Google Scholar 

  • 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 39:155–168

    Article  PubMed  CAS  Google Scholar 

  • 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 40:71–86

    Article  PubMed  CAS  Google Scholar 

  • 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 45:623–636

    Article  PubMed  CAS  Google Scholar 

  • 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 33:95–104

    CAS  Google Scholar 

  • Posada D, Crandall KA (1998) Modeltest: testing the model of DNA substitution. Bioinformatics 14:817–818

    Article  PubMed  CAS  Google Scholar 

  • Price PW (1996) Species concept. In: biological evolution. Saunders College Publishing, Philadelphia, pp 59–73

  • 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 34–53

  • 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 57:1134–1149

    Article  CAS  Google Scholar 

  • Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574

    Article  PubMed  CAS  Google Scholar 

  • 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 131:203–212

    Article  CAS  Google Scholar 

  • 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 131:213–218

    Article  CAS  Google Scholar 

  • 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 42:301–315

    Article  PubMed  CAS  Google Scholar 

  • Semina AV, Polyakova NE, Brykov VA (2007) Analysis of mitochondrial DNA: taxonomic phylogenetic relationships in two fish taxa (Pisces: Mugilidae and Cyprinidae). Biochemistry (Moscow) 72:1349–1355

    Article  CAS  Google Scholar 

  • Swofford DL (2002) PAUP* Phylogenetic analysis using parsimony (*and other methods), version 4. Sinauer Associates, Sunderland

    Google Scholar 

  • 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 10:512–526

    PubMed  CAS  Google Scholar 

  • Thomson JM (1997) The Mugilidae of the world. Mem Qld Mus 41:457–562

    Google Scholar 

  • 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 61:104–111

    Google Scholar 

  • Turan C, Caliskan M, Kucuktas H (2005) Phylogenetic relationships of nine mullet species (Mugilidae) in the Mediterranean Sea. Hydrobiologia 532:45–51

    Article  Google Scholar 

  • 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 360:1847–1857

    Article  PubMed  CAS  Google Scholar 

  • Xia X, Xie Z (2001) DAMBE: data analysis in molecular biology and evolution. J Hered 92:371–373

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This study was made possible through the generous contribution of mullets samples by Quim Pou, Jordi Viñas, William H Dailey, Alicia Acuña, Daniel Figueroa, Hicham Nouiri, Joao Paes Vieira, Darío Colautti and Marcelo Beiz. We would like to thank Fred Utter for helpful comments and corrections of the English style. Funding was provided to SHM by BRAE predoctoral fellowship and to MIR by 910305 grant from Universitat de Girona. MGC was supported by a Comisión de Investigaciones Científicas graduate fellowship and AL.E./2003 grant for his stay in Girona, Spain.

Author information

Authors and Affiliations

  1. Laboratori d’Ictiologia Genètica, Facultat de Ciències, Universitat de Girona, Campus Montilivi, 17071, Girona, Spain

    Sandra Heras

  2. Laboratori d’Ictiologia Genètica, Facultat de Ciències, Universitat de Girona, Campus Montilivi, 17071, Girona, Spain

    María Inés Roldán

  3. Laboratorio de Ictiología, Departamento de Ciencias Marinas, Universidad Nacional de Mar del Plata, Mar del Plata, Argentina

    Mariano González Castro

Authors
  1. Sandra Heras
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. María Inés Roldán
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Mariano González Castro
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to María Inés Roldán.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Heras, S., Roldán, M.I. & Castro, M.G. Molecular phylogeny of Mugilidae fishes revised. Rev Fish Biol Fisheries 19, 217–231 (2009). https://doi.org/10.1007/s11160-008-9100-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11160-008-9100-3

Keywords

Search

Navigation