Vol.17 – 2011

The systematic status of the Mediterranean Spicara species (Centracanthidae) inferred from mitochondrial 16S rDNA sequence and morphological data

Cemal Turan

Fisheries Genetics Laboratory, Faculty of Fisheries, Mustafa Kemal University, Iskenderun, Hatay, TURKEY

Abstract

The mitochondrial 16S ribosomal DNA together with morphological data were used to elucidate monophyly of the family Centracanthidae and interrelationships of Spicara and Centracanthus genera, including four species, Spicara maena, Spicara flexuosa, Spicara smaris and Centracanthus cirrus. Examination of the gene revealed a moderate amount of thymine and abundance of adenine. The 16S rDNA dataset contained 92 variable and 69 parsimony informative sites with a mean nucleotide diversity of 0.099. Haplotype diversity was found to be 0.71. No genetic differences were observed between S. maena and S. smaris, and the genetic divergence between S. flexuosa and both S. maena and S. smaris was found to be 0.005. The intergeneric divergence was found to be very high (0.237) between S. alta and C. cirrus. For the other Spicara species, intergeneric divergence ranged from 0.170 between C. cirrus and both S. maena and S. smaris to 0.176 between C. cirrus and S. flexuosa. Minumum evolution, neighbor joining and parsimony trees revealed same tree topologies, and the monophyly of the genus Spicara was not supported. S. maena and S. smaris clustered together and showed close relationship and S. flexuosa was nodded with this group. Therefore S. maena was found to be more closely related to S. smaris rather than S. flexuosa. On the other hand, S. alta highly divergently clustered outside of this group and branched with C. cirrus. Multivariate analysis of morphological data was congruent with the genetic data and revealed similar pattern of relationship among Centracanthidae species.

Keywords: Centracanthidae, Spicara, Centracanthus, Systematics, mtDNA, Sequence, Morphology

References

Aksiray, F. (1987) Türkiye Deniz Balıkları ve Tayin Anahtarı. İ.Ü Rektörlüğü Yayınları. No: 3490. Istanbul, 426-430 pp.

Allendorf, F.W. (1988) Conservation biology of fishes. Cons. Biol. 2: 145-148.

Baum, D. (1992) Phylogenetic species concepts. Trends. Ecol. Evol. 7: 1- 2.

Brown, W.M., Prager, E.M., Wang, A., and Wilson, C. (1982) Mitochondrial DNA sequences of primates: tempo and mode of evolution. J. Mol. Evol. 18: 225-239.

Doukakis, P., Birstein, V.J., Ruban, G.I., and Desalle, R. (1999) Molecular genetic analysis among subspecies of two Eurasian sturgeon species, Acipenser baerii and A. stellatus. Mol. Ecol. 8: 117-128.

Dulcic, J., Kraljevic, M., Grbec, B., and Cetinic, P. (2000) Age, growth and mortality of blotched picarel Spicara maena L. (Pisces: Centracanthidae) in the Eastern Central Adriatic. Fish. Res. 48: 69-78.

Dunham, A.E., Smith, G.R., and Taylor, J.N. (1979) Evidence for ecological character displacement in Western American catostomic fishes. Evolution 33: 877-896.

Durand, P., Pointier, J.P. Escoubeyrou, K., Arenas, J., Yong, M., Amarista, M., Bargues, M.D., Mas-Coma, S., and Renaud, F. (2002) Occurrence of a sibling species complex within neotropical Lymnaeids, snail intermediate hosts of fascioliasis. Acta. Trop. 83: 233-240.

Faria, R., Weiss, S., and Alexandrino, P. (2006) A molecular phylogenetic perspective on the evolutionary history of Alosa spp. (Clupeidae). Mol. Phyl. Evol. 40: 298-304.

Felsenstein, J. (1985) Confidence Limits on Phylogenies: An Approach U

Felsenstein, J. (1993) PHYLIP 3.5 (Phylogeny Inference Package). Seattle, Washington, USA, University of Washington.

Ferguson, M.M., Danzmann, R.G., and Hutchings, J.A. (1991) Incongruent estimates of population differentiation among brook charr, Salvelinus fontinalis, from Cape Race, Newfoundland, Canada, based upon allozyme and mitochondrial DNA variation. J. Fish. Biol. 39: 79- 85.

Fischer, W., Schneider, M., and Bauchot, M.L. (1987) Centracanthidae. In: Mediterranee et Mer Noire, Zone de Peãche. Vol. 2. FAO, CEE, Rome. 761-1529 pp.

Haemstra, P.C. (1990) Centracanthidae. In: J.C. Quero, J.C. Hureau, C. Karrer A. Post and L. Saldanha (eds) Check-list of the Fishes of the 18 Eastern Tropical Atlantic (CLOFETA). JNICT, Lisbon SEI, Paris and Unesco, Paris, 2: 769-770 pp.

Hall, T.A. (1999). BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nuc. Acid. Symp. 41: 95-98.

Hansen, M.M., and Loeschcke, V. (1996) Temporal variation in mitochondrial NA haplotype frequencbies in a brown trout (Salmo trutta L.) Population that shows stability in nuclear allele frequencies. Evolution 50: 454-457.

Harvey, W.D. (1990) Electrophoretic techniques in forensics and law enforcement. In: Electrophoretic and Isoelectric Focusing Techniques in Fisheries Management. DH. Whitmore (eds), CRC press, Boca Raton, Florida, 31-322 pp.

Hasegawa, M., Kishino, K., and Yano, T. (1985) Dating the human–ape splitting by a molecular clock of mitochondrial DNA. J. Mol. Evol. 31: 113-121.

Ismen, A. (1995) Growth, mortality and yield per recruit model of picarel (Spicara smaris L.) on the Eastern Turkish Black Sea Coast. Fish. Res. 22: 299-308.

Karaiskou, N., Apostolidis, A.P., Triantafyllidis, A., Kouvatsi, A., and Triantaphyllidis, C. (2003) Genetic identification and phylogeny of three species of the genus Trachurus Based on Mitochondrial DNA Analysis. Mar. Biot.5: 493-504.

Kocher, T.D., and Stepien, C.A. (1997) Molecular Systematics of Fishes. Academic Press, San Diego.

Kumar, S., Tamura, K., and Nei, M. (2004) MEGA 3: Integrated software for molecular evolutionary genetics analysis and sequence alignment. Briefings in Bioinformatics 5: 150-163.

Meyer, A., Kocher T.D., and Basasibwaki, P. (1990) Monophyletic origin of Victoria cichlid fish suggested by mitochondrial DNA sequences. Nature 347: 550-553.

Meyer, A. (1992) Cichlid fishes: behaviour, ecology and evolution. In: M.H.A. Keenleyside (eds). Q. Rev. Biol. 67: 221-222.

Nelson, J.S. (1994) Fishes of the World. Third Edition. John Wiley & Sons, Inc., New York. 600 pp.

Normark, B.B., Mccune, A.R., and Harrison, R.G. (1991) Phylogenetic relationships of Neopterygian fishes, inferred from mitochondrial DNA sequences. Mol. Biol. Evol. 8: 819-534.

Orrell, T.M., Carpente,r K.E. Musick, J.A. and J.E. Graves, (2002) Phylogenetic and analysis of the Sparidae (Perciformes: Percoidei) from cytochrome b sequences. Copeia 3: 618-631.

Orrell, T.M., and Carpenter, K.E. (2004) A phylogeny of the fish family (porgies) inferred from mitochondrial sequence data. Mol. Phyl. Evol. 32: 425-434.

Perez, J., Alvarez , P., Martinez, J.L., and Garcia-Vazquez, E. (2005) Genetic identification of hake and megrim eggs in formaldehyde-fixed plankton samples. ICES J. Mar. Sci. 62: 908-914.

Pollard, D.A., and Pichot, P. (1971) The systematic status of the Mediterranean fishes of the genus Spicara and in particular S. chrselis (Val.) as indicated by electrophoretic studies of their eye-lens proteins. J. Biol. 3: 59-72.

Posada, D., and Crandall, K.A. (1998) Modeltest: testing the model of DNA. Bioinformatics 14: 817-818.

Reeb, C.A., and Avise J.C. (1990) A genetic discontinuity in a continuously distributed species: mitochondrial DNA in the American oyster, Crassostrea virginica. Genetics 124: 397-406.

Saitou, N., and Nei, M. (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 4: 406- 425.

Somers, K.M. (1986) Multivariate allometry and removal of size with principal component analysis. Syst. Zool. 35: 359-368.

Thompson, J.D., Higgins, D.G., and Gibson, T.J. (1994) Clustal W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position specific gap penalties and weight matrix choice. Nuc. Acid. Res. 22: 4673-4680

Tinti F., and Piccinetti, C. (2000). Molecular systematics of the AtlantoMediterranean Solea species. J. Fish. Biol. 56: 604-614.

Tortonese, E. (1986) Carangidae in Fishes of the North-Eastern Atlantic and the Mediterranean. In: P.J.P. Whitehead, ML., Bauchot, JC., Hureau, Nielsen J. and Tortonese E. (eds.) Unesco, Paris. 908-911 pp.

Turan, C., Carvalho, G.R., and Mork, J. (1998) molecular genetic analysis of Atlanto Scandian herring (Clupea harengus) populations using allozymes and mitochondrial DNA markers. J. Mar. Biol. Assoc. U. K. 78: 269-283.

Turan C., Öztürk, B., Ergüden, D., Gürlek, M., Yağlıoğlu, D., and Uygur, N. (2007) Atlas of marine bony fishes of Turkey. In: Atlas and Systematic of Marine Bony Fishes of Turkey ((ed.) C. Turan). Nobel Publishing House, Adana, Turkey.

Turan C., Gunduz I., Gurlek M., Yaglıoglu D., and Erguden D. (2008). Molecular systematics of Scorpaenidae species inferred from mitochondrial 16S rDNA sequence data. Folia Biol. (Krakow) 57: 219- 226.

Vidalis K., Markakis G., and Tsimenides N. (1997). Discrimination between populations of spicare (Spicara smaris L. 1758) in the Aegean Sea, using multivariate analysis of phenetic characters. Fish. Res. 30: 191-197.

Ward R.D., and Grewe P.M. (1994). Appraisal of molecular genetic techniques in fisheries. Rev. Fish. Biol. Fish. 4: 300-325.

Ward, R.D., Billington, N., and Hebert, P.D.N. (1989) Comparison of allozyme and mitochondrial DNA variation in populations of walleye, Stizostedion vitreum. Can. J. Fish. Aquat. Sci. 46: 2074-2084.

Wimberger, P.H. (1992) Plasticity of fish body shape the effects of diet, development, family and age in two species of Geophagus (Pisces: Cichlidae) biological. J. Lin. Soc. 45: 197-218.

Zardoya, R., and Doadrio, I. (1999) Molecular evidence on the evolutionary and patterns of European cyprinids. J. Mol. Evol. 49: 227- 237.

A collection of recent ctenophore sightings from the Maltese Islands

Alan Deidun

Physical Oceanography Unit, University of Malta, Msida, MSD 2080 MALTA

Abstract

The only ctenophore reports from Maltese coastal waters ever published date back to over 40 years ago, with only two comb jelly species being previously recorded from such waters. A collection of recent ctenophore sightings from Maltese coastal waters, all substantiated through underwater photography or video footage and pertaining to Leucothea multicornis, Beroe cucumis and Beroe forskalii, is hereby reported. These sightings were submitted by members of the public as part of the citizen science initiative known as “Spot the Jellyfish”.

Keywords: Ctenophore, Maltese Islands, Leucothea multicornis, Beroe cucumis, Beroe forskalii, citizen science

References

Agassiz, L. (1860) Contribution to the Natural History of the United States of America. Vol. 3.Little, Brown, 1-301, Boston.

Boero, F., Putti, M., Trainito, E., Prontera, E., Piraino, S., and Shiganova, T. (2009) First records of Mnemiopsis leidyi (Ctenophora) from the Ligurian, Thyrrhenian and Ionian Seas (Western Mediterranean) and First Record of Phyllorhiza punctata (Cnidaria) from the Western Mediterranean. Aquatic Invasions 4(4): 675-680.

Claustre, H., Kerherve, P., Marty, J. C., Prieur, L., Videau, C., and Hecq, J.H. (1994) Phytoplankton Dynamics Associated with a Geostrophic front: Ecological and Biogeochemical Implications. J. Mar. Res. 52: 711–742.

Chun, C. (1880) Die Ctenophoren des Golfes von Neapel. Fauna und Flora des Golfes von Neapel, 1: 1–313.

Deidun, A. (2010) Notes on the Recent Occurrence of Uncommon Pelagic “jellyfish” Species in Maltese Coastal Waters. Naturalista Siciliano S. IV, XXXIV (3-4): 375-284.

Deidun, A., Drago, A., Galea, A., Azzopardi, J., Gauci, A., and Melin, F. (in preparation). A first attempt at testing correlation between MODIS ocean colour data and in situ chlorophyll a measurements within Maltese coastal waters.

Evans, F. (1968) Le zooplankton de Malte. Pelagos, 9: 5-20.

Fuentes, V.L, Atienza D, Gili, J-M, and Purcell, J.E. (2009) First Record of Mnemiopsis leidyi A. Agassiz 1865 off the NW Mediterranean Coast of Spain. Aquatic Invasions 4: 671- 674, doi:10.3391/ai.2009.4.4.12

Mayer, A. G. (1912) Ctenophores of the Atlantic Coast of North America. Publs. Carnegie Inst., 162, 1–58.

Micallef, H. and Evans, F. (1968) The Marine Fauna of Malta. Marine Science Royal University, Malta, 1: 143-172.

Mills, C.E., Hugh, P.R., Harbison, G.R., and Haddock, S.H.D. (1996) Medusae, Siphonophores and Ctenophores of the Alboran Sea, South Western Mediterranean Source. Scientia Marina 60(1):145 -163.

Shiganova, T.A, and Malej, A. (2009) Native and Non-native Ctenophores in the Gulf of Trieste, Northern Adriatic Sea. Journal of Plankton Research 31 (1): 61-71, doi:10.1093/ plankt/fbn102

Wrobel, D. and Mills, C. (1998) Pacific Coast Pelagic Invertebrates. A Guide to the Common Gelatinous Animals. Monterey Bay Aquarium, Monterey, pp. 108.