Skip to main content
Log in

Efficiency of DNA barcoding for phylogenetic analysis and species identification in flying fish (Exocoetidae)

  • Published:
Journal of Ichthyology Aims and scope Submit manuscript

Abstract

The article reports DNA barcoding (sequencing of the cox 1 mitochondrial gene fragment) of five South Atlantic flying fish species belonging to family Exocoetidae together with the results of the comparative analysis of cox 1 variability in the Exocoetidae and its closely related family Hemiramphidae. It has been demonstrated that DNA barcoding can be used as an extra tool for species identification and phylogenetic analysis in flying fish, since species identification accuracy using the cox 1 gene sequence proved to be 88%, or 78% when intraspecies variability level is taken into account. We have confirmed monophyletic origin of certain species, genera, and subfamilies of flying fish except for the genus Cheilopogon, which was represented on the phylogenetic tree by three paraphyletic clades. One of them shows close relationship to the genus Cypselurus, while another encompasses Hirundichthys genus species. The Exocoetidae is characterized by much lower overall genetic divergence level compared to the Hemiramphidae (average intraspecies differences: 10.2 ± 0.4% vs. 18.1 ± 0.8%; average intrageneric differences: 13.3 ± 1.1% vs. 21.3 ± 1.8%), which may indicate that the former group is relatively young in terms of evolution. No intraspecies differentiation was observed for Exocoetus obtusirostrus across a significant geographic distance (>3000 km). Phylogenetic reconstructions based on the variability of conservative (cox 1 mtDNA) and more variable regions of mitochondrial and nuclear genomes and on the adaptive morphological traits associated with gliding flight development were shown to coincide to a large extent.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Baldwin, C.C., The phylogenetic significance of color patterns in marine teleost larvae, Zool. J. Linn. Soc., 2013, vol. 168, pp. 496–563.

    Article  PubMed  PubMed Central  Google Scholar 

  • Berg, L.S., The system of fish-like species and fishes in present and fossil, Tr. Zool. Inst., Akad. Nauk SSSR, 1940, vol. 5, no. 2.

    Google Scholar 

  • BOLDSystem, Barcode of Life Data Systems, ver. 09.12.2014, 2014. http://www.boldsystems.org.

  • Breder, C.M., On the structural specialization of flying fishes from the standpoint of aerodynamics, Copeia, 1930, no. 4, pp. 114–121.

    Article  Google Scholar 

  • Breder, C.M., A contribution to the life histories of Atlantic Ocean flyingfishes, Bull. Bingham Oceanogr. Coll. Yale Univ., 1938, vol. 6, art. 5.

    Google Scholar 

  • Bruun, A.F., Flying-fishes (Exocoetidae) of the Atlantic. Systematic and biological studies, Dana Rep., 1935, no. 6, pp. 1–108.

    Google Scholar 

  • Chen, C.-H., Studies of the early life history of flying fishes (family Exocoetidae) in the northwestern Pacific, Monogr. Taiwan Prov. Mus., 1987, no. 7, pp. 1–202.

    Google Scholar 

  • Collette, B.B., Family Hemiramphidae Gill 1859—halfbeaks, in Annotated Checklists of Fishes, San Francisco, CA: Calif. Acad. Sci., 2004, vol. 22.

    Google Scholar 

  • Collette, B.B., McGowen, G.E., Parin, N.V., and Mito, S., Beloniformes: development and relationships, Int. Symp. Dedicated to the Memory of Elbert Halvor Ahlstrom Ontogeny and Systematics of Fishes, La Jolla, CA, August 15–18, 1983, Am. Soc. Ichthyol. Herpetol. Spec. Publ. No. 1, Moser, H.G., et al., Eds., Lawrence, KS: Univ. of Kansas, 1984, pp. 335–354.

    Google Scholar 

  • Dasilao, J.C. and Sasaki, K., Phylogeny of the flyingfish family Exocoetidae (Teleostei, Beloniformes), Ichthyol. Res., 1998, vol. 45, no. 4, pp. 347–353.

    Article  Google Scholar 

  • Dasilao, J.C., Sasaki, K., and Okamura, O., The hemiramphid, Oxyporhamphus, is a flyingfish (Exocoetidae), Ichthyol. Res., 1997, vol. 44, no. 2, pp. 101–107.

    Article  Google Scholar 

  • Davenport, J., How and why do flying fish fly? Rev. Fish Biol. Fish., 1994, vol. 4, pp. 184–214.

    Article  Google Scholar 

  • FishBase, Version 10/2015, Froese, R. and Pauly, D., Eds., 2015. http://www.fishbase.org.

  • Fu, Y.X., New statistical tests of neutrality for DNA samples from a population, Genetics, 1996, vol. 143, pp. 557–570.

    CAS  PubMed  PubMed Central  Google Scholar 

  • GenBank, v. 09.12.2014, 2014. http://www.ncbi.nlm.nih.gov/genbank.

  • Gibbs, R.H. and Staiger, J.C., Eastern tropical Atlantic flyingfishes of the genus Cypselurus (Exocoetidae), Stud. Trop. Oceanogr., 1970, vol. 4, no. 2, pp. 432–466.

    Google Scholar 

  • Gomes, C., Oxenford, H.A., and Dales, R.B.G., Mitochondrial DNA D-loop variation and implications for stock structure of the four-wing flyingfish, Hirundichthys affinis, in the Central Western Atlantic, Bull. Mar. Sci., 1999, vol. 64, no. 3, pp. 485–500.

    Google Scholar 

  • Ivanova, N.V., Zemlak, T.S., Hanner, R.H., and Hebert, P.D.N., Universal primer cocktails for fish DNA barcoding, Mol. Ecol. Notes, 2007, vol. 7, pp. 544–548.

    Article  CAS  Google Scholar 

  • Keane, T.M., Creevey, C.J., Pentony, M.M., et al., Assessment of methods for amino acid matrix selection and their use on empirical data shows that ad hoc assumptions for choice of matrix are not justified, BMC Evol. Biol., 2006, vol. 6, p. 29.

    Article  PubMed  PubMed Central  Google Scholar 

  • Kutschera, U., Predator-driven macroevolution in flyingfishes inferred from behavioral studies: historical controversies and a hypothesis, Ann. Hist. Phil. Biol., 2005, vol. 10, pp. 59–77.

    Google Scholar 

  • Lewallen, E.A., Pitman, R.L., Kjartanson, S.L., and Lovejoy, N.R., Molecular systematics of flyingfishes (Teleostei, Exocoetidae): evolution in the epipelagic zone, Biol. J. Linn. Soc., 2011, vol. 102, pp. 161–174.

    Article  Google Scholar 

  • Lovejoy, N.R., Reinterpreting recapitulation: systematics of needlefishes and their allies (Teleostei: Beloniformes), Evolution, 2000, vol. 54, no. 4, pp. 1349–1362.

    Article  CAS  PubMed  Google Scholar 

  • Lovejoy, N.R., Iranpour, M., and Collette, B.B., Phylogeny and jaw ontogeny of Beloniform fishes, Integr. Comp. Biol., 2004, vol. 44, pp. 366–377.

    Article  CAS  PubMed  Google Scholar 

  • Luiz, O.J., Madin, J.S., Robertson, D.R., et al., Ecological traits influencing range expansion across large oceanic dispersal barriers: insights from tropical Atlantic reef fishes, Proc. R. Soc. B, 2012, vol. 279, pp. 1033–1040.

    Article  PubMed  Google Scholar 

  • Meier, R., Shiyang, K., Vaidya, G., and Ng, P.K.L., DNA barcoding and taxonomy in Diptera: a tale of high intraspecific variability and low identification success, Syst. Biol., 2006, vol. 55, pp. 715–728.

    Article  PubMed  Google Scholar 

  • Nelson, J.S., Fishes of the World, New York: Wiley, 1976.

    Google Scholar 

  • Nelson, D.S., Ryby mirovoi fauny (Fishes of the World), Moscow: Librokom, 2009.

    Google Scholar 

  • Nichols, J.T. and Breder, C.M., An annotated list of the Synentognathi, with remarks of their development and relationships, Zoologica, 1928, vol. 8, no. 7, pp. 423–448.

    Google Scholar 

  • Parin, N.V., The system of flyingfishes (families Oxyporhamphidae and Exocoetidae), Tr. Inst. Okeanol., Akad. Nauk SSSR, 1961, vol. 43, pp. 92–183.

    Google Scholar 

  • Parin, N.V., Ikhtiofauna okeanskoi epipelagiali (Ichthyofauna of the Ocean Epipelagial), Moscow: Nauka, 1968.

    Google Scholar 

  • Parin, N.V., Assessment of the abundance of flying fishes by visual observations, Biol. Oceanogr., 1983a, vol. 2, nos. 2–4, pp. 341–355.

    Google Scholar 

  • Parin, N.V., Order Beloniformes, in Zhizn’ zhivotnykh. Tom 4. Ryby (Life of the Animals, Vol. 4: Fishes), Rass, T.S., Ed., Moscow: Prosveshchenie, 1983b, pp. 300–309.

    Google Scholar 

  • Parin, N.V., Species composition of flyingfishes in the western central part of tropical Pacific, Vopr. Ikhtiol., 1996, vol. 36, no. 3, pp. 300–307.

    Google Scholar 

  • Parin, N.V. and Shakhovskoy, I.B., A review of the flying fish genus Exocoetus (Exocoetidae) with descriptions of two new species from the Southern Pacific Ocean, J. Ichthyol., 2000, vol. 40, suppl. 1, pp. S3I–S63.

    Google Scholar 

  • Puillandre, N., Lambert, A., Brouillet, S., and Achaz, G., ABGD, automatic barcode gap discovery for primary species delimitation, Mol. Ecol., 2012, vol. 21, pp. 1864–1877.

    Article  CAS  PubMed  Google Scholar 

  • Regan, C.T., The classification of the teleostean fishes of the order Synentognathi, Ann. Mag. Nat. Hist., 1911, vol. 7, pp. 327–335.

    Article  Google Scholar 

  • Rozas, J., Sánchez-DelBarrio, J.C., Messeguer, X., and Rozas, R., DnaSP, DNA polymorphism analyses by the coalescent and other methods, Bioinformatics, 2003, vol. 19, no. 18, pp. 2496–2497.

    Article  CAS  PubMed  Google Scholar 

  • Shakhovskoy, I.B. and Parin, N.V., A review of flying fishes of the subgenus Hirundichthys (genus Hirundichthys, Exocoetidae). Part 2. Nerito-oceanic species: H. oxycephalus, H. affinis, J. Ichthyol., 2013, vol. 53, no. 8, pp. 509–540.

    Article  Google Scholar 

  • Staiger, J.C., Atlantic flyingfishes of the genus Cypselurus, with descriptions of the juveniles, Bull. Mar. Sci., 1965, vol. 15, no. 3, pp. 672–725.

    Google Scholar 

  • Tajima, F., Statistical methods to test for nucleotide mutation hypothesis by DNA polymorphism, Genetics, 1989, vol. 123, pp. 585–595.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Tamura, K. and Nei, M., Estimation of the number of nucleotide substitution in the control region of mitochondrial DNA in humans and chimpanzees, Mol. Biol. Evol., 1993, vol. 10, pp. 512–526.

    CAS  PubMed  Google Scholar 

  • Tamura, K., Peterson, D., Peterson, N., et al., MEGA5: Molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods, Mol. Biol. Evol., 2011, vol. 22, pp. 2731–2739.

    Article  Google Scholar 

  • Tibbetts, I.R., Collette, B.B., Isaac, R., and Kreiter, P., Functional and phylogenetic implications of the vesicular swimbladder of Hemiramphus and Oxyporhamphus convexus (Beloniformes: Teleostei), Copeia, 2007, no. 4, pp. 808–817.

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to N. V. Gordeeva.

Additional information

Original Russian Text © N.V. Gordeeva, I.B. Shakhovskoi, 2017, published in Voprosy Ikhtiologii, 2017, Vol. 57, No. 2, pp. 212–221.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Gordeeva, N.V., Shakhovskoi, I.B. Efficiency of DNA barcoding for phylogenetic analysis and species identification in flying fish (Exocoetidae). J. Ichthyol. 57, 287–296 (2017). https://doi.org/10.1134/S0032945217020096

Download citation

  • Received:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S0032945217020096

Keywords

Navigation