Scientia Marina, Vol 78, No 4 (2014)

Genetic support for the morphological identification of larvae of Myctophidae, Gonostomatidae, Sternoptychidae and Phosichthyidae (Pisces) from the western Mediterranean


https://doi.org/10.3989/scimar.04072.27A

Ainhoa Bernal
Institut de Ciències del Mar (CSIC) , Spain

Jordi Viñas
Laboratori d’Ictiologia Genètica, Facultat de Ciències, Universitat de Girona , Spain

M. Pilar Olivar
Institut de Ciències del Mar (CSIC) , Spain

Abstract


Mesopelagic fishes experience an extreme body transformation from larvae to adults. The identification of the larval stages of fishes from the two orders Myctophiformes and Stomiiformes is currently based on the comparison of morphological, pigmentary and meristic characteristics of different developmental stages. However, no molecular evidence to confirm the identity of the larvae of these mesopelagic species is available so far. Since DNA barcoding emerged as an accurate procedure for species discrimination and larval identification, we have used the cytochrome c oxidase 1 or the mitochondrial 12S ribosomal DNA regions to identify larvae and adults of the most frequent and abundant species of myctophiforms (family Myctophidae) and stomiiforms (families Gonostomatidae, Sternoptychidae and Phosichthyidae) from the Mediterranean Sea. The comparisons of sequences from larval and adult stages corroborated the value of the morphological characters that were used for taxonomic classification. The combination of the sequences obtained in this study and those of related species from GenBank was used to discuss the consistency of monophyletic clades for different genera. Pairwise nucleotide distances were notably higher inter- than intraspecifically, and were useful to discern between congeners such as Cyclothone braueri and C. pygmaea, Hygophum benoiti and H. hygomii, Lampanyctus crocodilus and L. pusillus, and Notoscopelus bolini and N. elongatus.

Keywords


barcoding; CO1; 12S rRNA; larval identification; western Mediterranean Sea; mesopelagic fish

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References


Ahlstrom E.H. 1974. The diverse patterns of metamorphosis in gonostomatid fishes - An aid to classification. In: Blaxter J.H.S (ed), The early life history of fish. Berlin: Springer-Verlag, pp. 659-674. http://dx.doi.org/10.1007/978-3-642-65852-5_52

Badcock J. 1984. Gonostomatidae, Sternoptychidae, Photichthyidae. In: Whitehead P.J.P., Bauchot M.L., Hureau J.C., Nielsen J., Tortonese E. (eds), Fishes of the north-eastern Atlantic and the Mediterranean, vol. 1. Paris: UNESCO, pp. 284-324.

Barber P., Boyce S.L. 2006. Estimating diversity of Indo-Pacific coral reef stomatopods through DNA barcoding of stomatopod larvae. Proc. R. Soc. Lond., B. 273: 2053-2061. http://dx.doi.org/10.1098/rspb.2006.3540 PMid:16846913 PMCid:PMC1635474

Bartlett S.E., Davidson W.S. 1992. FINS (forensically informative nucleotide sequencing): a procedure for identifying the animal origin of biological specimens. Biotechniques 12: 408-411. PMid:1571152

Berdar A., Cavaliere A. 1975. Stadi larvali e postlarvali di mictofidi: Lobianchia dofleini. Atti Soc. Pelorit. Sci. Fis. Mat. Nat. 21: 115-122.

Blaxter J.H.S. 1984. Ontogeny, systematics and fisheries. In: Moser H.G., Richards W.J., Cohen D.M., Fahay M.P., Kendall A.W., Richardson S.L. (eds), Ontogeny and systematics of fishes, Spec. Publ. 1. Lawrence, KS: Am. Soc. Ichthyol. Herpetol., pp. 1-6.

Burton R.S. 1996. Molecular tools in Marine Ecology. J. Exp. Mar. Biol. Ecol. 200: 85-101. http://dx.doi.org/10.1016/S0022-0981(96)02641-X

Cocco A. 1829. Su du alcuni nuovi pesci de' mari di Messina. Giornale di Scienze, Lettere e Arti per La Sicilia, Anno 7 26(77): 138-147.

Cocco A. 1838. Observazioni intorno taluni pesci del mare di Messina, Lettera di Anastasio Cocco al Prof. Oronzio Gabrièle Costa di Napoli. Giornale Il Faro 4.

Costa O.G. 1844. Fauna del Regno di Napoli ossia enumerazione di tutti gli animali che abitano le diverse regioni di questo Regno e le acque che le bagnano contenente la descrizione de' nuovi o poco esattamente conosciuti, con figure ricavate da originali riventi e dipinte al naturale. Dalla Stamperia di Azzolino e Compagno, Napoli.

Fink W.L. 1984. Stomiiforms: relationships. In: Moser H.G., Richards W.J., Cohen D.M., Fahay M.P., Kendall A.W., Jr. Richardson S.L. (eds), Amer. Soc. Ichthyol. Herpetol., Spec. Publ. 1: 181-184.

Fink W.L. 1985. Phylogenetic interrelationships of the stomiid fishes (Teleostei: Stomiiformes). Misc. Publ. Mus. Zool. Univ. Mich. 171: 1-127.

Gjøsaeter J., Kawaguchi K. 1980. A review of the world resources of mesopelagic fish. FAO Fish. Tech. Pap. 193: 1-151.

Gmelin J.F. 1789. Pisces. In: Caroli a Linné, Systema Naturae per regna tria naturae secundum classes, ordines, genera, species, cum characteribus, differentiis, synonymis, locis (13th ed), 1 (3): 1126-1516.

Goode G.B., Bean T.H. 1896. Oceanic Ichthyology, a treatise on the deep-sea and pelagic fishes of the world, based chiefly upon the collections made by the steamers "Blake", "Albatross", and "Fish Hawk" in the northwestern Atlantic, with an atlas contain ing 417 figures. Spec. Bull. U.S. Nat. Mus. 2: 553 p.

Goodyear R.H., Zahuranec B.J., Pugh W.L., et al. 1972. Ecology and vertical distribution of Mediterranean midwater fishes. In: Mediterranean Biological Studies (ed). Final report, vol. 1. Washington, D.C.: Smithsonian Institution, pp. 91-229.

Hall T.A. 1999. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp. Ser. 41: 95-98.

Hare J.A., Cowen R.K., Zehr J.P., et al. 1994. Biological and oceanographic insights from larval labrid (Pisces: Labridae) identification using mtDNA sequences. Mar. Biol. 118: 17-24. http://dx.doi.org/10.1007/BF00699215

Hebert P.D.N., Cywinska A., Ball S.L., et al. 2003. Biological identifications through DNA barcodes. Proc. R. Soc. Lond., B. 270: 313-322. http://dx.doi.org/10.1098/rspb.2002.2218 PMid:12614582 PMCid:PMC1691236

Hebert P.D.N., Stoeckle M.Y., Zemlak T.S., et al. 2004. Identification of birds through DNA barcodes. PLoS Biol. 2(10): 1657-1663. http://dx.doi.org/10.1371/journal.pbio.0020312 PMid:15455034 PMCid:PMC518999

Hulley P.A. 1981. Results of the research cruises of FRV "Walther Herwig" to South America: LVIII. Family Myctophidae (Osteichthyes, Myctophiformes). Archiv. FischWiss. 31: 1-303.

Hulley P.A. 1984. Myctophidae. In: Whitehead P.J.P, Bauchot M.L., Hureau J.C., Nielsen J., Tortonese E. (eds), Fishes of the North-eastern Atlantic and the Mediterranean, vol. 1. Paris: UNESCO, pp. 429-483.

Jespersen P., Tåning A.V. 1926. Mediterranean Sternoptychidae. Report on the Danish Oceanographical Expeditions 1908-1910 2: 59.

Johnson J.Y. 1890. On some new species of fishes from Madeira. Proc. Zool. Soc. Lond. 1890: 452-459.

Johnson G.D., Paxton J.R., Sutton T.T, et al. 2009. Deep-sea mystery solved: astonishing larval transformations and extreme sexual dimorphism unite three fish families. Biol. Lett. 5: 235-239. http://dx.doi.org/10.1098/rsbl.2008.0722 PMid:19158027 PMCid:PMC2667197

Ko H-L, Wang Y-T, Chiu T-S, et al. 2013. Evaluating the accuracy of morphological identification of larval fishes by applying DNA barcoding. Plos One 8: e53451. http://dx.doi.org/10.1371/journal.pone.0053451 PMid:23382845 PMCid:PMC3561387

Kochzius M., Seidel C., Antoniou A., et al. 2010. Identifying fishes through DNA barcodes and microarrays. PLoS One 5: e12620. http://dx.doi.org/10.1371/journal.pone.0012620 PMid:20838643 PMCid:PMC2935389

Lowe R.T. 1839. A supplement to a synopsis of the fishes of Madeira. Trans. Zool. Soc. Lond. 3: 1-20.

Lütken C.F. 1892. Nogle nordiske Laxesild (Scopeliner). Korte bidrag til Nordisk ichthyographi, VIII. Vidensk. Medd. Dan. Naturhist. Foren. 43: 203-233.

Miya M., Nishida M. 1998. Molecular phylogeny and evolution of the deep-sea fish genus Sternoptyx. Mol. Phylogenet. Evol. 10: 11-22. http://dx.doi.org/10.1006/mpev.1997.0479 PMid:9751914

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. http://dx.doi.org/10.1006/mpev.2000.0839 PMid:11133198

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. http://dx.doi.org/10.1093/oxfordjournals.molbev.a003741 PMid:11606696

Moreau E. 1888. Le scopele de Verany, Scopelus veranyi. Bull. Soc. Philomath. Paris (Ser. 7), 12 (3): 108-111.

Moore W.S. 1995. Inferring phylogenies from mtDNA variation: mitochondrial-gene trees versus nuclear-gene trees. Evolution 49: 718-726. http://dx.doi.org/10.2307/2410325

Moser H.G., Ahlstrom E.H. 1974. The role of larval stages in systematic investigations of marine teleosts: The Myctophidae, a case study. In: Blaxter J.H.S (ed), The early life history of fish. Berlin: Springer-Verlag, pp.605-607. http://dx.doi.org/10.1007/978-3-642-65852-5_48

Moser H.G., Ahlstrom E.H., Paxton J.R. 1984. Myctophidae: Development. In: Moser H.G., Richards W.J., Cohen D.M., et al. (eds), Ontogeny and systematics of fishes, Spec. Publ. 1. Lawrence, KS: Am. Soc. Ichthyol. Herpetol., pp. 218-239.

Moura T., Silva M.C., Figueiredo I., et al. 2008. Molecular barcoding of north-east Atlantic deep-water sharks: species identification and application to fisheries management and conservation. Mar. Freshw. Res. 59: 214-223. http://dx.doi.org/10.1071/MF07192

Nafpaktitis B.G. 1975. Review of the lanternfish genus Notoscopelus (family Myctophidae) in the North Atlantic and the Mediterranean. Bull. Mar. Sci. 25 (1): 75-87.

Nafpaktitis B.G., Backus R.H., Craddock J.E., et al. 1977. Family Myctophidae. In: Mem. Sears Found. Mar. Res (ed), Fishes of the western North Atlantic. New Haven: Yale University 1, pp. 13-265.

Olivar M.P., Beckley L.E., Moser H.G. 1999. Lanternfish larvae from the Agulhas Current (Sw Indian Ocean). Sci. Mar. 63: 101-120.

Olivar M.P., Bernal A., Molí B., et al. 2012. Vertical distribution, diversity and assemblages of mesopelagic fishes in the western mediterranean. Deep-Sea Res. Part I. 62 (0): 53-69. http://dx.doi.org/10.1016/j.dsr.2011.12.014

Palomera I. 1983. Desarrollo larvario de Notoscopelus elongatus elongatus (Costa, 1844) y Notoscopelus bolini Nafpaktitis, 1975. Invest. Pesq. (Spain) 47 (2): 263-276.

Parin N.V., Kobyliansky S.G. 1996. Diagnoses and distribution of fifteen species recognized in genus Maurolicus Cocco (Sternoptychidae, Stomiiformes) with a key to their identification. Cybium 20(2): 185-195.

Paxton J.R. 1972. Osteology and relationships of the lanternfishes (Family Myctophidae). Sci. Bull. 13: 1-81.

Paxton J.R., Ahlstrom E.H., Moser H.G. 1984. Myctophidae: Relationships. In: Moser H.G., Richards W.J., Cohen D.M., et al. (eds), Ontogeny and systematics of fishes. Lawrence, KS: Am. Soc. Ichthyol. Herpetol. Spec. Publ. 1: 239-244.

Pegg G.G., Sinclair B., Briskey L., et al. 2006. MtDNA barcode identification of fish larvae in the southern Great Barrier Reef, Australia. Sci. Mar. 70S2: 7-12.

Poulsen J., Byrkjedal I., Willassen E.,et al. 2013. Mitogenomic sequences and evidence from unique gene rearrangements corroborate evolutionary relationships of myctophiformes (Neoteleostei). BMC Evol. Biol. 13 (1): 1-22. http://dx.doi.org/10.1186/1471-2148-13-111 PMid:23731841 PMCid:PMC3682873

Rafinesque C.S. 1810. Indice d'Ittiologia Siciliana. Messina. 70 p.

Reinhardt J.C.H. 1837. Ichthyologiske bidrag til den grönlandske fauna. København. Col. Pl. I-VIII: 1-114.

Richards W.J. 2006. Order stomiiformes. In: Richards W.J. (ed), Early stages of Atlantic fishes: An identification guide for the western Central North Atlantic. CRC Mar. Biol. Ser. 1: 177-182.

Risso A. 1810. Ichthyologie de Nice, ou histoire naturelle des poissons du départament des Alpes Maritimes. Tome 26. Paris. 388 pp.

Ronquist F., Huelsenbeck J.P. 2003. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19: 1572-1574. http://dx.doi.org/10.1093/bioinformatics/btg180 PMid:12912839

Rozen S., Skaletsky H.J. 2000. Primer 3 on the WWW for general users and for biologist programmers. Bioinformatics methods and protocols: methods in Molecular Biology. Krawetz S.M.S. Totowa N.J. (eds). Humana Press: 365-386. PMid:10547847

Sanzo L. 1931. Stomiatoidei, Sternoptichidae. Uova, larve e stadi giovanili di teleostei. Fauna e Flora Golfo di Napoli. 38: 42-92.

Steinke D., Zemlak T., Boutillier J.A., et al. 2009. DNA barcoding of Pacific Canada's fishes. Mar. Biol. 156 (12): 2641-2647. http://dx.doi.org/10.1007/s00227-009-1284-0

Takeyama H., Chow S., Tsuzuki H., et al. 2001. Mitochondrial DNA sequence variation within and between tuna Thunnus species and its application to species identification. J. Fish Biol. 58 (6): 1646-1657. http://dx.doi.org/10.1111/j.1095-8649.2001.tb02319.x

Tamura K., Stecher G., Peterson D., et al. 2013. Mega 6: Molecular Evolutionary Genetics Analysis Version 6.0, Mol. Biol. Evol. 30: 1725-2729. http://dx.doi.org/10.1093/molbev/mst197 PMid:24132122 PMCid:PMC3840312

Tåning Å.V. 1918. Mediterranean Scopelidae: (Saurus, Aulopus, Chlorophthalmus and Myctophum). Rep. Dan. Oceanogr. Exped. 1908-1910. 2: 1-154.

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 Res. 22 (22): 4673-4680. http://dx.doi.org/10.1093/nar/22.22.4673 PMid:7984417 PMCid:PMC308517

Valdez-Moreno M., Vásquez-Yeomans L., Elías-Gutiérrez M., et al. 2010. Using DNA barcodes to connect adults and early life stages of marine fishes from the Yucatan Peninsula, Mexico: Potential in fisheries management. Mar. Freshw. Res. 61 (6): 655-671. http://dx.doi.org/10.1071/MF09222

Vi-as J., Tudela S. 2009. A validated methodology for genetic identification of tuna species (genus Thunnus). PLoS One 4: e7606. http://dx.doi.org/10.1371/journal.pone.0007606 PMid:19898615 PMCid:PMC2764144

Ward R.D., Zemlak T.S., Innes B.H., et al. 2005. DNA barcoding Australia's fish species. Philos. Trans. R. Soc. Lond. B. 360 (1462): 1847-1857. http://dx.doi.org/10.1098/rstb.2005.1716 PMid:16214743 PMCid:PMC1609232

Webb K.E., Barnes D.K.A., Clark M.S., et al. 2006. DNA barcoding: a molecular tool to identify Antarctic marine larvae. Deep-Sea Res. Part II 53: 1053-1060. http://dx.doi.org/10.1016/j.dsr2.2006.02.013

Weitzman S.H. 1974. Osteology and evolutionary relationships of the Sternoptychidae, with a new classification of stomiatoid families. Bull. Am. Mus. Nat. Hist. 153 (3): 327-478.

Yamaguchi M., Miya M., Okiyama M., et al. 2000. Molecular phylogeny and larval morphological diversity of the lanternfish genus Hygophum (Teleostei: Myctophidae). Mol. Phylogenet. Evol. 15 (1): 103-114. http://dx.doi.org/10.1006/mpev.1999.0726 PMid:10764538

Zugmayer E. 1911. Diagnoses des poissons nouveaux. Bull. Inst. Oceanogr. 193: 1-14.




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