This Article Statistics
Viewed : 1077 Downloaded : 640


Phylogenetic Relationships of Turbot Species (Scophthalmidae) Inferred from the Mitochondrial COIII Gene and Morphological Characters

Cemal Turan *, Petya Ivanova, Mevlüt Gürlek, Deniz Yağlıoğlu, Deniz Ergüden, Serpil Karan, Servet Ahmet Doğdu, Ali Uyan, Bayram Öztürk, Venelin Nikolov, Violin Raykov, Ivan Dobrovolov, Antonia Khanaychenko

DOI: 10.28978/nesciences.522593


In this study, the validity, distribution and structure of three turbot species, Scophthalmus maeoticus, S. maximus, S. rhombus, belong to Scophthalmidae family in Turkish, Bulgarian and Russian coastal waters were determined with mtDNA sequencing of Cytochrome c oxidase subunit III (COIII). The sequencing of the COIII region revealed 8 bp variable and 6 bp parsimony informative sites between all turbot species. The overall genetic and haplotype diversities among all turbot species were found to be 0.004109 and 0.7655, respectively. Genetic distance analysis showed that the highest nucleotide differences was observed between S. maximus and S. rhombus species with a value of 0.09620 and, the lowest value (0.02482) was observed between S. maximus and S. maeoticus species. Neighbor Joining and Maximum Parsimony phylogenetic approaches resulted in the similar tree topologies that S. maximus and S. maeoticus were found as sister group, whereas S. rhombus was more divergent from this group. The mtDNA COIII gene is a useful genetic marker for species specific identification of the genus Scophthalmus due to its inter-specific heterogeneity producing a species-specific pattern. In morphological analyses, S. rhombus was most differentiated from S. maximus and S. maeoticus. The genetic data was supported by the detected morphometric variations among the turbot species.


Turbot, phylogeny, mtDNA sequencing, morphology, the Black Sea, the Marmara Sea.

Download full text   |   How to Cite   |   Download XML Files

  • Avise, J. C. (Ed.) (1994). Molecular Markers, Natural History and Evolution. Chapman and Hall, New York, NY. pp. 511.
  • Azevedo, M. F. C., Oliveira, C., Pardo, B. G., Martinez, P., & Foresti, F. (2008). Phylogenetic analysis of the order Pleuronectiformes (Teleostei) based on sequences of 12S and 16S mitochondrial genes. Genetics and Molecular Biology, 31, 284-292.
  • Bailly, N. & Chanet, B. (2010). Scophthalmus Rafinesque, 1810: the valid generic name for the turbot, S. maximus (Linnaeus, 1758) [Pleuronectiformes: Scophthalmidae]. Cybium, 34(3), 257-261.
  • Blanquer, A., Alayse, J. P., Berrada‐Rkhami, O., & Berrebi, P. (1992). Allozyme variation in turbot (Psetta maxima) and brill (Scophthalmus rhombus) (Osteichthyes, Pleuronectoformes, Scophthalmidae) throughout their range in Europe. Journal of Fish Biology, 41(5), 725-736.
  • Brooks, D. R., & McLennan, D. A. (2012). The Nature of Diversity: An Evolutionary Voyage of Discovery. University of Chicago Press.
  • Brown, J. M., Pellmyr, O., Thompson, J. N., & Harrison, R. G. (1994). Phylogeny of Greya (Lepidoptera: Prodoxidae), based on nucleotide sequence variation in mitochondrial cytochrome oxidase I and II: congruence with morphological data. Molecular Biology and Evolution, 11(1), 128-141.
  • Chanet, B. (2003). Interrelationships of scophthalmid fishes (Pleuronectiformes: Scophthalmidae). Cybium, 27(4), 275-286.
  • Durand, P., Pointier, J. P., Escoubeyrou, K., Arenas, J., Yong, M., Amarista, M., Bargues, M. D., Mas-Coma, S., & Renaud, F. (2002). Occurrence of a sibling species complex within neotropical lymnaeids, snail intermediate hosts of fascioliasis. Acta Tropica, 83, 233-240.
  • Elliott, N. C., Farrell, J. A., Gutierrez, A. P., van Lenteren, J. C., Walton, M. P., & Wratten, S. (1995). Integrated pest management. Springer Science & Business Media.
  • Eschmeyer, W. N. (2011). Catalog of Fishes: Genera, Species, References. (http://research.calacademy.org/research/ichthyology/catalog/fishcatmain.asp). Accessed on 07 March 2016.
  • Evseenko, S. A. (2003). An annotated catalogue of pleuronectiform fishes (order Pleuronectiformes) of the seas of Russia and adjacent countries. Journal of Ichthyology, 43(1), 57-74.
  • Felsenstein, J. (1985). Confidence limits on phylogenies: An approach using the bootstrap. Evolution, 39(4), 783-791.
  • Feng, Y., Jing, L., Peijun, Z., & Jianhai, X. (2005). Preliminary study on mitochondrial 16S rRNA gene sequences and phylogeny of flatfishes (Pleuronectiformes). Chinese Journal of Oceanology and Limnology, 23(3), 335-339.
  • Froese, R., & Pauly. D. (Editors). 2017. FishBase. World Wide Web electronic publication. www.fishbase.org, version (05/2017).
  • Hall, T. A. (1999). BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium, 41, 95-98.
  • Hansen, T. F. (2014). Use and misuse of comparative methods in the study of adaptation. In: Modern phylogenetic comparative methods and their application in evolutionary biology (pp. 351-379). Springer, Berlin, Heidelberg.
  • Hauser, L., Turan, C., & Carvalho, G. R. (2001). Haplotype frequency distribution and discriminatory power of two mtDNA fragments in a marine pelagic teleost (Atlantic herring, Clupea harengus). Heredity, 87, 621-630.
  • Ivanov, L. & Beverton, R. J. H. (1985). The fisheries resources of the Mediterranean. pt. 2: Black Sea. FAO.
  • Jónsson, G. (1992). Íslenskir fiskar. Reykjavík: Fjölvaútgáfan. 568p.
  • Jukes, T. H. & Cantor, C. R. (1969). Evolution of protein molecules. Pp. 21-132 in H.N. Munro, ed. Mammalian protein metabolism III. Academic Press, New York.
  • Junquera, S., & Perez-Gandaras, G. (1993). Population diversity in Bay of Biscay anchovy (Engraulis encrasicolus L. 1758) as revealed by multivariate analysis of morphometric and meristic characters. ICES Journal of Marine Science, 50(4), 383-391.
  • Karan, S. & Turan, C. (2019). Evaluation of Molecular and Phenotypic Markers for Phylogeographic Analysis of Black Sea Turbot Scopthalmus maeoticus. Acta zoologica bulgarica, accepted.
  • Karapetkova, M. (1980). Morphological characteristics of the Black Sea Turbot Scophthalmus maeoticus (Pallas). Khidrobiologiya, 12, 73-78
  • Kocher, T.D. & Stepien, C.A. (Eds.) (1997). Molecular systematics of fishes. Academic Press.
  • Meyer, A. (1993). Evolution of mitochondrial DNA in fishes. In: Biochemistry and Molecular Biology of Fishes. Elsevier Science Publishers, 2, 1-38.
  • Mohindra, V., Singh, R. K., Palanichamy, M., Ponniah, A. G., & Lal, K. K. (2007). Genetic identification of three species of the genus Clarias using allozyme and mitochondrial DNA markers. Journal of Applied Ichthyology, 23(1), 104-109.
  • Muus, B., & Dahlström, P. (1978). Meeresfische der Ostsee, der Nordsee, des Atlantiks. BLV Verlagsgesellschaft, München. 244 p.
  • Nelson, J. S. (1994). Fishes of the World, 3rd edn. Wiley, New York.
  • Pardo, B. G., Machordom, A., Foresti, F., Porto-Foresti, F., Azevedo, M. F., Bañon, R., Sánchez, L., & Martínez, P. (2005). Phylogenetic analysis of flatfish (Order Pleuronectiformes) based on mitochondrial 16S rRNA sequences. Scientia Marina, 531-543.
  • Prado Do, F. D., Vera, M., Hermida, M., Bouza, C., Pardo, B. G., Vilas, R., Blanco, A., Fernández, C., Maroso, F., E. Maes, G., Turan, C., A. M. Volckaert , F., B. Taggart , J., Carr, A., Ogden , R., Nielsen, E., The Aquatrace Consortium, Martínez, P. (2018). Parallel evolution and adaptation to environmental factors in a marine flatfish: Implications for fisheries and aquaculture management of the turbot (Scophthalmus maximus). Evolutionary Applications, 11:1322–1341.
  • Pardo, B. G., Bouza, C., Castro, J., Martínez, P., & Sánchez, L. (2001). Localization of ribosomal genes in Pleuronectiformes using Ag‐, CMA3‐banding and in situ hybridization. Heredity, 86(5), 531-536.
  • Posada, D., & Crandall, K. A. (1998). Modeltest: Testing the model of DNA substitution. Bioinformatics, 14(9), 817-818.
  • Sambrook, J., Fritsch, E. F., & Maniatis, T. (1989). Molecular cloning: a laboratory manual (No. Ed. 2). Cold spring harbor laboratory press.
  • Sanger, F., Nicklen, S., & Coulson, A. R. (1977). DNA Sequencing with chain- terminating inhibitors. Proceedings of the National Academy of Sciences, 74, 5463-5467.
  • Slastenenko, E. (1956). Karadeniz Havzasi Baliklari (The fishes of the Black Sea basin). E.B.K. Yayini, Istanbul. 711 pp. (in Turkish).
  • Suzuki, N., Nishida, M., Yoseda, K., Ustundag, C., Sahin, T., & Amaoka, K., (2004). Phylogeographic relationships within the Mediterranean turbot inferred by mitochondrial DNA haplotype variation. Journal of Fish Biology, 65(2), 580- 585.
  • Tabata, K., & Taniguchi, N. (2000). Differences between Pagrus major and Pagrus auratus through mainly mtDNA control region analysis. Fisheries Science, 66(1), 9-18.
  • Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M. & Kumar, S. (2011). MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution, 28(10), 2731-2739.
  • Thompson, J. D., Higgins, D. G., 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. Nucleic Acids Research, 22(22), 4673-4680.
  • Turan, C., (1999). A note on the examination of morphometric differentiation among fish populations: The truss system. Turkish Journal of Zoology, 23, 259-264.
  • Turan, C. (Ed.) (2007). Atlas and Systematics of Marine Bony Fishes of Turkey. 1st edition, Nobel Publishing House, Adana, Turkey.
  • Turan, C. (2008). Molecular systematic analyses of Mediterranean skates (Rajiformes). Turkish Journal of Zoology, 32(4), 437-442.
  • Turan, C., Gündüz, İ, Gürlek, M., & Yağlıoğlu, D. (2008). Systematics of Scorpaenidae species in the Mediterranean Sea inferred from mitochondrial 16S rDNA sequence and morphological data. Folia Biologica, 57, 219-226.
  • Turan, C., Ergüden, D., Çevik, C., Gürlek, M., & Turan, F. (2015a). Molecular systematic analysis of shad species (Alosa spp.) from Turkish marine waters using mtDNA genes. Turkish Journal of Fisheries and Aquatic Sciences, 15 (1), 149-155.
  • Turan, C., Gürlek, M., Ergüden, D., Yağlıoğlu, D., Öztürk, B., Uyan, A., Reyhaniye, A. N., Özbalcılar, B., Erdoğan, Z. A., Ivanova, P., & Soldo, A. (2015b). Population Genetic Analysis of Atlantic Bonito Sarda sarda (Bloch, 1793) using Sequence Analysis of mtDNA D-Loop Region. Fresenius Environmental Bulletin, 45(3), 231-237.
  • Turan, C., Yağlıoğlu, D., Ergüden, D., Gürlek, M., Uyan, A., Karan, S., & Doğdu, S. (2016). Threatened brill species in marine waters of Turkey: Scopthalmus rhombus (Linnaeus, 1758) (Scopthalmidae). Natural and Engineering Sciences, 1(1), 1-6.
  • Valles-Jiménez, R. (2005). Estudios sobre la estructura genética del camarón blanco (Litopenaeus vannamei), del Pacífico Oriental inferidos del análisis de microsatélites y ADN mitocondrial. PhD thesis. Centro de Investigaciones Biológicas Del Noroeste, S.C. 74 pp.
  • Voronina, E. P. (2010). On Morphology and Taxonomy of Scophthalmids. Journal of Ichthyology, 50(9), 695-703.
  • Zaharia, T. (2002). Researches for elaborating the technology for reproducing and rearing of the flounder and turbot, in order to renew their natural populations. PhD thesis. University, Dunarea de Jos” Galaţi, 156 pp. [In Romanian].
  • Zardoya, R., Economidis, P. S. & Doadrio, I. (1999). Phylogenetic relationships of Greek Cyprinidae: molecular evidence for at least two origins of the Greek cyprinid fauna. Molecular Phylogenetics and Evolution, 13(1), 122-131.