Systematics of the grey mullets (Teleostei: Mugiliformes: Mugilidae): Molecular phylogenetic evidence challenges two centuries of morphology-based taxonomy

Molecular Phylogenetics and Evolution

Volumn 64, Issue 1, 2012, Pages 73-92

  Durand, J D ^a   Shen, K N ^b   Chen, W J ^c   Jamandre, B W ^b   Blel, H ^d   Diop, K ^a   Nirchio, M ^e   Garcia de Leon F J ^f   Whitfield, A K ^g   Chang, C W ^h   Borsa, P ⁱ  

^a UNIVERSITÉ MONTPELLIER 2   (France)

^b NATIONAL TAIWAN UNIVERSITY   (Taiwan)

^c NATIONAL TAIWAN UNIVERSITY   (Taiwan)

^d UNIVERSITY OF MONASTIR   (Tunisia)

^e UNIVERSIDAD DE ORIENTE   (Venezuela)

^f CENTRO DE INVESTIGACIONES BIOLÓGICAS DEL NOROESTE   (Mexico)

^g SOUTH AFRICAN INSTITUTE FOR AQUATIC BIODIVERSITY   (South Africa)

^h NATIONAL DONG HWA UNIVERSITY   (Taiwan)

ⁱ INSTITUT DE RECHERCHE POUR LE DÉVELOPPEMENT   (France)

Author keywords

16S rRNA; Cryptic species; Cytochrome b; Cytochrome oxidase I; Phylogeny

Indexed keywords

MITOCHONDRIAL DNA; PRIMER DNA;

ANIMAL; ARTICLE; BAYES THEOREM; BIOLOGICAL MODEL; CLASSIFICATION; DNA SEQUENCE; GENETICS; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PHYLOGENY; SEA; SMEGMAMORPHA; SPECIES DIFFERENCE; STATISTICAL MODEL;

ANIMALS; BASE SEQUENCE; BAYES THEOREM; DNA PRIMERS; DNA, MITOCHONDRIAL; LIKELIHOOD FUNCTIONS; MODELS, GENETIC; MOLECULAR SEQUENCE DATA; OCEANS AND SEAS; PHYLOGENY; SEQUENCE ANALYSIS, DNA; SMEGMAMORPHA; SPECIES SPECIFICITY;

CESTRAEUS; MUGIL CEPHALUS; MUGILIDAE; MUGILIFORMES; TELEOSTEI;

EID: 84860552354     PISSN: 10557903     EISSN: 10959513     Source Type: Journal    
DOI: 10.1016/j.ympev.2012.03.006     Document Type: Article

References (84)

1. Aurelle D., Barthelemy R.-M., Quignard J.-P., Trabelsi M., Faure E. Molecular phylogeny of Mugilidae (Teleostei: Perciformes). Open Mar. Biol. J. 2008, 2:29-37.
2. Autem M., Bonhomme F. Eléments de systématique biochimique chez les Mugilidés de Méditerranée. Biochem. Syst. Ecol. 1980, 8:305-308.
3. Avise J.C. Phylogeography: The History and Formation of Species 2000, Harvard Univ. Press, Cambridge, MA, 447pp.
4. Blel H., Chatti N., Besbes R., Farjallah S., Elouaer A., Guerbej H., Said K. Phylogenetic relationships in grey mullets (Mugilidae) in a Tunisian lagoon. Aquaculture Res. 2008, 39:268-275.
5. Briggs J.C. Fishes of worldwide (circumtropical) distribution. Copeia 1960, 1960:171-180.
6. Caldara F., Bargelloni L., Ostellari L., Penzo E., Colombo L., Patarnello T. 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. 1996, 6:416-424.
7. Chen W.-J., Mayden R.L. Molecular systematics of the Cyprinoidea (Teleostei: Cypriniformes), the world's largest clade of freshwater fishes: further evidence from six nuclear genes. Mol. Phylogenet. Evol. 2009, 52:544-549.
8. Chen W.-J., Mayden R.L. A phylogenomic perspective on the new era of ichthyology. BioScience 2010, 60:421-432.
9. Chen W.-J., Bonillo C., Lecointre G. Repeatability of clades as a criterion of reliability: a case study for molecular phylogeny of acanthomorph (teleostei) with larger number of taxa. Mol. Phylogenet. Evol. 2003, 26:262-288.
10. Chen W.-J., Ruiz-Carus R., Orti G. Relationships among four genera of mojarras (Teleostei: Perciformes: Gerreidae) from the western Atlantic and their tentative placement among percomorph fishes. J. Fish Biol. 2007, 70:202-218.
11. Crosetti D., Avise J.C., Placidi F., Rossi A.R., Sola L. Geographic variability in the grey mullet Mugil cephalus: preliminary results of mtDNA and chromosome analyses. Aquaculture 1993, 111:95-101.
12. Crosetti D., Nelson W.S., Avise J.C. Pronounced genetic structure of mitochondrial DNA among populations of the circumglobally distributed grey mullet (Mugil cephalus Linnaeus). J. Fish Biol. 1994, 44:47-58.
13. Edgar R.C. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucl. Acids Res. 2004, 32:1792-1797.
14. Erguden D., Gurlek M., Yaglioglu D., Turan C. Genetic identification and taxonomic relationship of Mediterranean mugilid species based on mitochondrial 16S rDNA sequence data. J. Anim. Vet. Adv. 2010, 9:336-341.
15. Eschmeyer, W.N., Fricke, R. (Eds.), 2011. Catalog of Fishes, Electronic Version. (accessed 05.05.11). http://research.calacademy.org/research/ichthyology/catalog/fishcatmain.asp.
16. Felsenstein J. Confidence limits on phylogenies: an approach using the bootstrap. Evolution 1985, 39:783-791.
17. Fraga E., Schneider H., Nirchio M., Santa-Brigida E., Rodrigues-Filho L.F., Sampaio I. Molecular phylogenetic analyses of mullets (Mugilidae, Mugiliformes) based on two mitochondrial genes. J. Appl. Ichthyol. 2007, 23:598-604.
18. Ghasemzadeh, J., 1998. Phylogeny and Systematics of Indo-Pacific mullets (Teleostei: Mugilidae) with Special Reference to the Mullets of Australia. Ph.D. Dissertation. Macquarie University, Sydney, 397pp.
19. Ghasemzadeh J., Ivantsoff W., Aarn Historical overview of mugilid systematics, with descriptions of Paramugil (Teleostei: Mugiliformes: Mugilidae), new genus. Aqua. J. Ichthyol. Aquat. Biol. 2004, 8:9-22.
20. Goldman N. Statistical tests of models of DNA substitution. J. Mol. Evol. 1993, 36:182-198.
21. Gornung E., Colangelo P., Annesi F. 5S ribosomal RNA genes in six species of Mediterranean grey mullets: genomic organization and phylogenetic inference. Genome 2007, 50:787-795.
22. Hall T.A. BioEdit: a user-friendly biological sequence alignement editor and analysis program for windows 95/98/NT. Nucl. Acids Symp. Ser. 1999, 41:95-98.
23. Harrison I.J., Howes G.J. The pharyngobranchial organ of mugilid fishes; its structure, variability, ontogeny, possible fonction and taxonomic utility. Bull. Brit. Mus. Nat. Hist. Zool. 1991, 57:111-132.
24. Harrison, I.J., Senou, H., 1999. Mugilidae. In: Carpenter, K.E., Niem, V.H. (Eds.), FAO Species Identification Guide for Fishery Purposes. The Living Marine Resources of the Western Central Pacific, vol. 4. Bony Fishes Part 2 (Mugilidae to Carangidae). FAO, Rome, pp. 2069-2108.
25. Harrison I.J., Nirchio M., Oliveira C., Ron E., Gaviria J. A new species of mullet (Teleostei: Mugilidae) from Venezuela, with a discussion on the taxonomy of Mugil gaimardianus. J. Fish Biol. 2007, 71:76-97.
26. Hennig W. Phylogenetic Systematics 1966, University of Illinois Press, Urbana, IL.
27. Heras S., Gonzalez Castro M., Roldan M.I. Mugil curema in Argentinean waters: combined morphological and molecular approach. Aquaculture 2006, 261:473-478.
28. Heras S., Roldán M.I., Gonzalez Castro M. Molecular phylogeny of Mugilidae fishes revised. Rev. Fish Biol. Fish. 2009, 19:217-231.
29. Hillis D.M. Inferring complex phylogenies. Nature 1996, 383:130-131.
30. Hillis D.M. Taxonomic sampling, phylogenetic accuracy, and investigator bias. Syst. Biol. 1998, 47:3-8.
31. Huelsenbeck J.P., Ronquist F. MrBayes. Bayesian inference of phylogeny. Bioinformatics 2001, 17:754-755.
32. Imsiridou A., Minos G., Katsares V., Karaiskou N., Tsiora A. Genetic identification and phylogenetic inferences in different Mugilidae species using 5S rDNA markers. Aquaculture Res. 2007, 38:1370-1379.
33. Jamandre B.W., Durand J.-D., Tzeng W.-N. Phylogeography of the flathead mullet Mugil cephalus in the Northwest Pacific inferred from the mtDNA control region. J. Fish Biol. 2009, 75:393-407.
34. Ke H.M., Lin W.W., Kao H.W. Genetic diversity and differentiation of grey mullet (Mugil cephalus) in the coastal waters of Taiwan. Zool. Sci. 2009, 26:421-428.
35. Kluge A.G. A concern for evidence and a phylogenetic hypothesis of relationships among Epicrates (Boidae, Serpentes). Syst. Zool. 1989, 38:7-25.
36. Lee S.C., Chang J.T., Tsu Y.Y. Genetic relationships of four Taiwan mullets (Pisces: Perciformes: Mugilidae). J. Fish Biol. 1995, 46:159-162.
37. Li B., Dettaï A., Cruaud C., Couloux A., Desoutter-Meniger M., Lecointre G. RNF213, a new nuclear marker for acanthomorph phylogeny. Mol. Phylogenet. Evol. 2009, 50:345-363.
38. Linnaeus, C., 1758. Systema naturae per regna tria naturae, secundum classes, ordines, genera, species, cum characteribus, differentiis, synonymis, locis. Tomus I, editio decima, reformata. Holmiae, Stockholm, ii+824pp.
39. Liu J.-Y., Brown C.L., Yang T.-B. Population genetic structure and historical demography of grey mullet, Mugil cephalus, along the coast of China, inferred by analysis of the mitochondrial control region. Biochem. Syst. Ecol. 2009, 37:556-566.
40. Liu J.Y., Brown C.L., Yang T.B. Phylogenetic relationships of mullets (Mugilidae) in China Seas based on partial sequences of two mitochondrial genes. Biochem. Syst. Ecol. 2010, 38:647-655.
41. Livi S., Sola L., Crosetti D. Phylogeographic relationships among worldwide populations of the cosmopolitan marine species, the striped gray mullet (Mugil cephalus), investigated by partial cytochrome b gene sequences. Biochem. Syst. Ecol. 2011, 39:121-131.
42. Lüther G. New characters for consideration in the taxonomy appraisal of grey mullets. J. Mar. Biol. Ass. Ind. 1982, 169:1-9.
43. Mabuchi K., Miya M., Azuma Y., Nishida M. Independent evolution of the specialized pharyngeal jaw apparatus in cichlid and labrid fishes. BMC Evol. Biol. 2007, 7:10.
44. Mandelik Y., Dayan T., Chikatunov V., Kravchenko V. Reliability of a higher-taxon approach to richness, rarity, and composition assessments at the local scale. Conserv. Biol. 2007, 21:1506-1515.
45. Menezes M.R., Martin M., Naik S. Interspecific genetic divergence in grey mullets from the Goa region. Aquaculture 1992, 105:117-129.
46. Miya M., Takeshima H., Endo H., Ishiguro N.B., Inoue J.G., Mukai T., Satoh T.P., Yamaguchi M., Kawaguchi A., Mabuchi K., Shirai S.M., Nishida M. Major patterns of higher teleostean phylogenies: a new perspective based on 100 complete mitochondrial DNA sequences. Mol. Phylogenet. Evol. 2003, 26:121-138.
47. Murgia R., Tola G., Archer S.N., Vallerga S., Hirano J. Genetic identification of grey mullet species (Mugilidae) by analysis of mitochondrial DNA sequence. application to identify the origin of processed ovary products (bottarga). Mar. Biotechnol. 2002, 4:119-126.
48. Nelson J.S. Fishes of the World 2006, John Wiley and Sons, New York.
49. Nirchio M., Cequea H. Karyology of Mugil liza and M. curema from Venezuela. Bol. Invest. Mar. Cost. 1998, 27:45-50.
50. Nylander, J.A.A., 2004. MrModeltest v. 2. Program Distributed by the Author. Evolutionary Biology Centre, Uppsala University, Uppsala.
51. Palumbi, S., Martin, A., Romano, S., McMillan, W.O., 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, 47pp.
52. Papasotiropoulos V., Klossa-Kilia E., Kilias G., Alahiotis S. Genetic divergence and phylogenetic relationships in grey mullets (Teleostei: Mugilidae) using allozyme data. Biochem. Genet. 2001, 39:155-168.
53. Papasotiropoulos V., Klossa-Kilia E., Kilias G., Alahiotis S. Genetic divergence and phylogenetic relationships in grey mullets (Teleostei: Mugilidae) based on PCR RFLP analysis of mtDNA segments. Biochem. Genet. 2002, 40:71-86.
54. Papasotiropoulos V., Klossa-Kilia E., Alahiotis S., Kilias G. Molecular phylogeny of grey mullets (Teleostei: Mugilidae) in Greece. Evidence from sequence analysis of mtDNA segments. Biochem. Genet. 2007, 45:623-636.
55. Philippe, H., Chenuil, A., Adoutte, A., 1994. Can the Cambrian explosion be inferred through molecular phylogeny? Development Suppl. S, 15-25.
56. Rambaut, A., 1996. Se-Al: Sequence Alignment Editor ver. 2.0 (Program Distributed by the Author, Department of Zoology, University of Oxford, Oxford. http://tree.bio.ed.ac.uk/software/seal/.
57. Rocha-Olivares A., Garber N.M., Stuck K.C. High genetic diversity, large inter-oceanic divergence and historical demography of the striped mullet. J. Fish Biol. 2000, 57:1134-1149.
58. Rossi A.R., Capula M., Crosetti D., Campton D.E., Sola L. Genetic divergence and phylogenetic inferences in five species of Mugilidae (Pisces: Perciformes). Mar. Biol. 1998, 131:213-218.
59. Rossi A.R., Capula M., Crosetti D., Sola L., Campton D.E. Allozyme variation in global populations of striped mullet, Mugil cephalus (Pisces: Mugilidae). Mar. Biol. 1998, 131:203-212.
60. Rossi A.R., Ungaro A., De Innocentiis S., Crosetti D., Sola L. Phylogenetic analysis of mediterranean Mugilids by allozymes and 16S mt-rRNA genes investigation: are the Mediterranean species of Liza monophyletic?. Biochem. Genet. 2004, 42:301-315.
61. Sambrook J., Fritschi E.F., Maniatis T. Molecular Cloning: A Laboratory Manual 1989, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY. 2nd edn.
62. Schultz L.P. A revision of the genera of mullets, fishes of the family Mugilidae, with descriptions of three new genera. Proc. U.S. Natl. Mus. 1946, 96:377-395.
63. Schultz, L.P., 1953. Family Mugilidea. In: Schultz, L.P., Herald, E.S., A. Lachner, E., Welander, A.D., Woods, L.P. (Eds.), Fishes of the Marshall and Marianas Islands, vol. I. Families from Asymmetrontidae through Siganidae. Bull. U.S. Natl Mus. 202, pp. 310-322.
64. Semina A.V., Polyakova N.E., Makhotkin M.A., Brykov V.A. Mitochondrial DNA divergence and phylogenetic relationships in mullets (Pisces: Mugilidae) of the Sea of Japan and the Sea of Azov revealed by PCR-RFLP-analysis. Russ. J. Mar. Biol. 2007, 33:187-192.
65. Senou, H., 1988. Phylogenetic Interrelationships of the Mullets (Pisces: Mugilidae). Ph.D. Dissertation. Tokyo University, Tokyo.
66. Setiamarga D.H.E., Miya M., Yamanoue Y., Mabuchi K., Satoh T.P., Inoue J.G., Nishida M. Interrelationships of Atherinomorpha (medakas, flyingfishes, killifishes, silversides, and their relatives): the first evidence based on whole mitogenome sequences. Mol. Phylogenet. Evol. 2008, 49:598-605.
67. Sevilla R.G., Diez A., Noren M., Mouchel O., Jerome M., Verrez-Bagnis V., Van Pelt H., Favre-Krey L., Krey G., Bautista J.M. Primers and polymerase chain reaction conditions for DNA barcoding teleost fish based on the mitochondrial cytochrome b and nuclear rhodopsin genes. Mol. Ecol. Notes 2007, 7:730-734.
68. Shen K.-N., Jamandre B.W., Hsu C.-C., Tzeng W.-N., Durand J.-D. Plio-Pleistocene sea level and temperature fluctuations in the northwestern Pacific promoted speciation in the globally-distributed flathead mullet Mugil cephalus. BMC Evol. Biol. 2011, 11:83.
69. Shimodaira H., Hasegawa M. Multiple comparisons of log-likelihoods with applications to phylogenetic inference. Mol. Biol. Evol. 1999, 16:1114-1116.
70. Smith W.L., Craig M.T. Casting the percomorph net widely: the importance of broad taxonomic sampling in the search for the placement of serranid and percid fishes. Copeia 2007, 2007:35-55.
71. Smith W.L., Wheeler W.C. Venom evolution widespread in fishes: a phylogenetic road map for the bioprospecting of piscine venoms. J. Hered. 2006, 97:206-217.
72. Stamatakis A. RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 2006, 22:2688-2690.
73. Stamatakis A., Hoover P., Rougemont J. A rapid bootstrap algorithm for the RAxML web-servers. Syst. Biol. 2008, 57:758-771.
74. Stiassny M.L.J. What are grey mullets?. Bull. Mar. Sci. 1993, 52:197-219.
75. *and Other Methods), Version 4. Sinauer Associates, Sunderland, MA.
76. Tamura K., Peterson D., Peterson N., Stecher G., Nei M., Kumar S. MEGA 5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol. Biol. Evol. 2011, 28:2731-2739.
77. Thomson J.M. The Mugilidae of Australia and adjacent seas. Austr. J. Mar. Freshw. Res. 1954, 5:70-131.
78. Thomson J.M. The grey mullets. Oceanogr. Mar. Biol. Annu. Rev. 1966, 4:301-355.
79. Thomson J.M. The Mugilidae of the world. Mem. Queensl. Mus. 1997, 43:457-562.
80. Turan C., Caliskan M., Kucuktas H. Phylogenetic relationships of nine mullet species (Mugilidae) in the Mediterranean Sea. Hydrobiologia 2005, 532:45-51.
81. Villaseñor J.L., Ibarra-Manriquez G., Meave J.A., Ortiz E. Higer taxa as surrogates of plant biodiversity in a megadiverse country. Conserv. Biol. 2005, 19:232-238.
82. Ward R.D., Zemlak T.S., Innes B.H., Last P.R., Hebert P.D.N. DNA barcoding Australia's fish species. Philos. Trans. R. Soc. Lond. B 2005, 360:1847-1857.
83. Wiens J.J., Morrill M.C. Missing data in phylogenetic analysis: reconciling results from simulations and empirical data. Syst. Biol. 2011, 60:719-731.
84. Zemlak T.S., Ward R.D., Connell A.D., Holmes B.H., Hebert P.D.N. DNA barcoding reveals overlooked marine fishes. Mol. Ecol. Resour. 2009, 9:237-242.