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Molecular phylogenetic analysis of the squid family Mastigoteuthidae (Mollusca, Cephalopoda) based on three mitochondrial genes

Abstract

Mastigoteuthid squids are ecologically important, being prey to many apex predators, yet the diversity and systematics of the family remain poorly understood. Delicate by nature, they are often damaged during capture; there is a need to accurately identify incomplete mastigoteuthid specimens from collections and stomach contents. This study aimed to test a morphological hypothesis for the division of the genera Mastigoteuthis (Mt.), Idioteuthis, Mastigopsis (Mp.), Echinoteuthis, and Magnoteuthis (Mg.) and to assess the utility of DNA barcodes to discriminate species. Three mitochondrial genes (16S rRNA, 12S rRNA, and cytochrome c oxidase subunit I) were analysed for eight different species, representing the largest phylogenetic assessment of the family to date. Evidence was found for a potentially new species in New Zealand that has been previously misidentified as the morphologically similar species Mg. magna. Each species analysed herein exhibited unique mitochondrial DNA haplotypes for all loci, and the morphological distinction between the five proposed genera was strongly supported using a combined Bayesian and maximum-likelihood phylogenies. Of the three loci examined, the DNA barcode region shows the greatest divergence between species and should be used in future systematic work on the Mastigoteuthidae.

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Abbreviations

A.:

Asperoteuthis

C.:

Chiroteuthis

COI:

Cytochrome c oxidase subunit I

BIN:

Barcode Index Number

E.:

Echinoteuthis

GL:

Gladius length

GTR:

General time-reversible

I.:

Idioteuthis

J.:

Joubiniteuthis

Mg. :

Magnoteuthis

Mp. :

Mastigopsis

ML:

Mantle length

Mt.:

Mastigoteuthis

TN:

Tamura–Nei

References

  • Allcock, A. L., I. Barratt, M. Eleaume, K. Linse, M. D. Norman, P. J. Smith, D. Steinke, D. W. Stevens & J. M. Strugnell, 2011. Cryptic speciation and the circumpolarity debate: a case study on endemic Southern Ocean octopuses using the COI barcode of life. Deep Sea Research II 58: 242–249.

    Article  Google Scholar 

  • Arkhipkin, A. I. & V. V. Laptikhovsky, 2008. Discovery of the fourth species of the enigmatic chiroteuthid squid Asperoteuthis (Cephalopoda: Oegopsida) and extension of the range of the genus to the South Atlantic. Journal of Molluscan Studies 74: 203–207.

    Article  Google Scholar 

  • Berry, S. S., 1909. Diagnoses of new cephalopods from Hawaiian Islands. Proceedings US National Museum 37: 407–419.

    Article  Google Scholar 

  • Braid, H. E., 2013. Systematics and ecology of the New Zealand Mastigoteuthidae (Cephalopoda, Oegopsida). Unpublished Master's Thesis, Auckland University of Technology, Auckland: 1–178.

  • Braid, H. E., J. Deeds, S. L. DeGrasse, J. J. Wilson, J. Osborne & R. H. Hanner, 2012. Preying on commercial Fisheries and accumulating paralytic shellfish toxins: a dietary analysis of invasive Dosidicus gigas (Cephalopoda: Ommastrephidae) stranded in Pacific Canada. Marine Biology 159: 25–31.

    CAS  Article  Google Scholar 

  • Buhay, J. E., 2009. COI-like sequences are becoming problematic in molecular systematic and DNA barcoding studies. Journal of Crustacean Biology 29: 96–110.

    Article  Google Scholar 

  • Chun, C., 1908. Uber Cephalopoden der Deutschen Tiefsee-Expedition. Zoologischer Anzeiger 33: 86–89.

    Google Scholar 

  • Chun, C., 1910. Die Cephalopoden. I. Oegopsida. Wissenschaftliche Ergebnisse der Deutschen Tiefsee-Expedition auf dem Dampfer ‘Valdivia’ 1898–1899. [English Translation, Israel Program for Scientific Translations, 1975, 18: 1–552, 92 plates].

  • Chun, C., 1913. Cephalopoda. Report on the scientific results of the ‘Michael Sars’ North Atlantic Deep-Sea. Expedition 1910(3): 1–28.

    Google Scholar 

  • Clare, E., E. E. Fraser, H. E. Braid, M. B. Fenton & P. D. N. Hebert, 2009. Species on the menu of generalist predator, the eastern red bat (Lasiurus borealis): using a molecular approach to detect prey. Molecular Ecology 18: 2532–2542.

    PubMed  Article  Google Scholar 

  • Clarke, M. R., 1966. A review of the systematics and ecology of oceanic squids. Advances in Marine Biology 4: 91–300.

    Google Scholar 

  • Clarke, M. R. & E. R. Trueman, 1988. Paleontology and neontology of cephalopods. The Mollusca 12: 331–340.

    Google Scholar 

  • Dai, L., X. Zheng, L. Kong & Q. Li, 2012. DNA barcoding analysis of Coleoidea (Mollusca: Cephalopoda) from Chinese waters. Molecular Ecology Resources 12: 437–447.

    CAS  PubMed  Article  Google Scholar 

  • Drummond, A. J., M. A. Suchard, D. Xie & A. Rambaut, 2012. Bayesian phylogenetics with BEAUti and the BEAST 1.7. Molecular Biology and Evolution 29: 1969–1973.

    CAS  PubMed  Article  Google Scholar 

  • Dunn, M. R., A. Szabo, M. S. McVeagh & P. J. Smith, 2010. The diet of deepwater sharks and the benefits of using DNA identification of prey. Deep Sea Research I 57: 923–930.

    CAS  Article  Google Scholar 

  • Evans, K. & M. A. Hindell, 2004. The diet of sperm whales (Physeter macrocephalus) in southern Australian waters. ICES Journal of Marine Sciences 61: 1313–1329.

    Article  Google Scholar 

  • Folmer, O., M. Black, W. Hoeh, R. Lutz & R. Vrijenhoek, 1994. DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology 3: 294–299.

    CAS  PubMed  Google Scholar 

  • Grimpe, G., 1922. Systematische Übersicht der europäischen Cephalopoden. Sitzungsberichte der Naturforschenden Gesellschaft zu Leipzig 45: 36–52.

    Google Scholar 

  • Guindon, S. & O. Gascuel, 2003. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Systematic Biology 52: 696–704.

    PubMed  Article  Google Scholar 

  • Hall, T. A., 1999. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series 41: 95–98.

    CAS  Google Scholar 

  • Hebert, P. D. N., A. Cywinska, S. L. Ball & J. R. deWaard, 2003. Biological identifications through DNA barcodes. Proceedings of the Royal Society of London Series B 270: 313–321.

    CAS  PubMed  Article  Google Scholar 

  • Hebert, P. D. N., E. H. Penton, J. M. Burns, D. H. Janzen & W. Hallwachs, 2004. Ten species in one: DNA barcoding reveals cryptic species in the neotropical skipper butterfly Astraptes fulgerator. Proceedings of the National Academy of Sciences of the United States of America 101: 14812–14817.

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  • Hitchmough, R., L. Bull & P. Cromarty, 2005. New Zealand Threat Classification Systems List. Department of Conservation, Wellington.

  • Horn, P. L. & M. R. Dunn, 2010. Inter-Annual Variability of the Diets of Hoki, Hake, and Ling on the Chatham Rise from 1990 to 2009. Ministry of Fisheries, Wellington.

    Google Scholar 

  • Ivanova, N. V., J. R. deWaard & P. D. N. Hebert, 2006. An inexpensive, automation-friendly protocol for recovering high-quality DNA. Molecular Ecology Notes 6: 998–1002.

    CAS  Article  Google Scholar 

  • Joubin, L., 1895. Contribution a l’éstude des céphalopodes de l’Atlantique nord. Résultats des campagnes scientifiques accomplies sur yacht par Albert I Prince souverain de Monaco 9: 1–63.

    Google Scholar 

  • Joubin, L., 1913. Éstudes préliminaires sur les céphalopodes recueillis au cours des croisières de S.A.S. le Prince de Monaco. 3e Note: Mastigoteuthis magna nov. sp. Bulletin de l’Institut Océanographique 275: 1–11.

    Google Scholar 

  • Joubin, L., 1924. Résultas sur campagnes scientifiques de Prince de Monaco accomplies sur son yacht par Albert 1er Prince souverain de Monaco. Contribution à L’Étude des Céphalopodes de l’Atlantique nord 4: 1–113.

    Google Scholar 

  • Joubin, L., 1933. Notes préliminaires sur les Céphalopodes des croisières du Dana (1921–1922), 4e Partie. Annals de l’Institut Océanographiques 13: 1–49.

    Google Scholar 

  • Katoh, K., K. Misawa, K. Kuma & T. Miyata, 2002. MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Research 30: 3059–3066.

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  • Lanfear, R., B. Calcott, S. Y. W. Ho & S. Guindon, 2012. PartitionFinder: combined selection of partitioning schemes and substitution models for phylogenetic analyses. Molecular Biology and Evolution 29: 1695–1701.

    CAS  PubMed  Article  Google Scholar 

  • Lindgren, A. R., 2010. Molecular inference of phylogenetic relationships among Decapodiformes (Mollusca: Cephalopoda) with special focus on the squid Order Oegopsida. Molecular Phylogenetics and Evolution 56: 77–90.

    PubMed  Article  Google Scholar 

  • Lönnberg, E., 1896. Notes on some rare Cephalopoda. Öfversigt af Kongl. Vetenskaps-Akademiens Förhandlingar 53: 603–612.

    Google Scholar 

  • Meier, R., G. Zhang & F. Ali, 2008. The use of mean instead of smallest interspecific distance exaggerates the size of the ‘barcoding gap’ and leads to misidentification. Systematic Biology 57: 809–813.

    PubMed  Article  Google Scholar 

  • Mintzer, V. J., D. P. Gannon, N. B. Barros & A. J. Read, 2008. Stomach contents of mass-stranded short-finned pilot whales (Globicephala macrorhynchus) from North Carolina. Marine Mammal Science 24: 290–302.

    Article  Google Scholar 

  • Naef, A., 1921–1923. Cephalopoda. Fauna and Flora of the Bay of Naples 35: 1–917.

    Google Scholar 

  • Nesis, K. N., 1987. Cephalopods of the World; Squids, Cuttlefishes, Octopuses, and Allies. TFH Publications, New Jersey.

    Google Scholar 

  • Pattengale, N. D., M. Alipour, O. R. P. Bininda-Emonds, B. M. E. Moret & A. Stamatakis, 2010. How many bootstrap replicates are necessary? Journal of Computational Biology 17: 337–354.

    CAS  PubMed  Article  Google Scholar 

  • Pfeffer, G., 1900. Synopsis der oegopsiden Cephalopoden. Mitteilungen aus dem Naturhistorischen Museum Hamburg 17: 147–198.

    Google Scholar 

  • Pfeffer, G., 1912. Die Cephalopoden der Plankton-Expedition: Zugleich eine monographische Übersicht der Oegopsiden Cephalopoden. Verlag von Lipsius & Tischer, Kiel.

    Book  Google Scholar 

  • Posada, D., 2008. jModelTest: phylogenetic model averaging. Molecular Biology and Evolution 25: 1253–1256.

    CAS  PubMed  Article  Google Scholar 

  • Rambaut, A., & A. J. Drummond, 2009. Tracer. Version 1.5. http://beast.bio.ed.ac.uk.

  • Rancurel, P., 1972. Mastigoteuthis inermis espèce nouvelle de Chiroteuthidae du Golfe de Guinée (Cephalopoda, Oegopsida). Extrait du Bulletin de la Société Zoologique de France 97: 25–34.

    Google Scholar 

  • Rancurel, P., 1973. Mastigoteuthis hjorti Chun 1913 description de trios échantillons provenant du Golfe de Guiée (Cephalopoda, Oegopsida). Cahiers ORSTOM. Série Océanographie 11: 27–32.

    Google Scholar 

  • Ratnasingham, S. & P. D. N. Hebert, 2007. BOLD: The barcode of life data system (http://www.barcodinglife.org). Molecular Ecology Notes 7: 355–364.

  • Ratnasingham, S. & P. D. N. Hebert, 2013. A DNA-based registry for all animal species: the barcode index number (BIN) system. PLoS ONE 8: e66213.

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  • Roper, C. F. E. & G. L. Voss, 1983. Guidelines for taxonomic descriptions of cephalopod species. Memoirs of the National Museum Victoria 44: 48–63.

    Google Scholar 

  • Roper, C. F. E., R. E. Young & G. L. Voss, 1969. An illustrated key to the families of the order Teuthoidea (Cephalopoda). Smithsonian Contributions to Zoology 13: 1–32.

    Article  Google Scholar 

  • Rosecchi, E., D. M. Tracey & W. R. Webber, 1988. Diet of orange roughy, Hoplostethus atlanticus (Pices: Trachichthyidae) on the Challenger Plateau, New Zealand. Marine Biology 99: 293–306.

    Article  Google Scholar 

  • Rosso, J. J., E. Mabragana, M. Gonzalez Castro & J. M. Diaz De Astarloa, 2012. DNA barcoding Neotropical fishes: recent advances from the Pampa Plain, Argentina. Molecular Ecology Resources 12: 999–1011.

    CAS  PubMed  Article  Google Scholar 

  • Salcedo-Vargas, M. A., 1993. Revision of the Squid Family Mastigoteuthidae (Mollusca: Cephalopoda) from the Northwest Pacific. Unpublished Doctoral Thesis, Tokyo University of Fisheries, Tokyo: 1–253.

  • Salcedo-Vargas, M. A., 1995. Systematic value of the ultrastructure of the sucker surface in the squid family Mastigoteuthidae (Mollusca: Cephalopoda). Contributions to Zoology 65: 65–77.

    Google Scholar 

  • Salcedo-Vargas, M. A., 1997. Cephalopods from the Netherlands Indian Ocean Programme (NIOP)-II. Mastigoteuthid lineage and related forms. Beaufortia 47: 91–108.

    Google Scholar 

  • Salcedo-Vargas, M. A. & T. Okutani, 1994. New classification of the squid family Mastigoteuthidae (Cephalopoda: Oegopsida). Venus 53: 119–127.

    Google Scholar 

  • Santos, M. B., G. J. Pierce, J. Herman, A. López, A. Guerra, E. Mente & M. R. Clarke, 2001. Feeding ecology of Cuvier’s beaked whale (Ziphius cavirostris): a review with new information on the diet of this species. Journal of the Marine Biological Association of the UK 81: 687–694.

    Google Scholar 

  • Sasaki, M., 1916. Notes on oegopsid cephalopods found in Japan. Annotationes Zoologicae Japonenses 9: 89–120.

    Google Scholar 

  • Sasaki, M., 1929. A monograph of the dibranchiate cephalopods of the Japanese and adjacent waters. Journal of the College of Agriculture 20: 1–357.

    Google Scholar 

  • Simon, C., F. Frati, A. Beckenbach, B. Crespi, H. Liu & P. Flook, 1994. Evolution, weighting, and phylogenetic utility of mitochondrial gene sequences and a compilation of conserved polymerase chain reaction primers. Annals of the Entomological Society of America 87: 651–701.

    CAS  Google Scholar 

  • Sin, Y. W., C. Yau & K. H. Chu, 2009. Morphological and genetic differentiation of two loliginid squids, Uroteuthis (Photololigo) chinensis and Uroteuthis (Photololigo) edulis (Cephalopoda: Loliginidae), in Asia. Journal of Experimental Marine Biology and Ecology 369: 22–30.

    Article  Google Scholar 

  • Song, H., J. E. Buhay, M. F. Whiting & K. A. Crandall, 2008. Many species in one: DNA barcoding overestimates the number of species when nuclear mitochondrial pseudogenes are coamplified. Proceedings of the National Academy of Sciences of the United States of America 105: 13486–13491.

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  • St-Onge, M., B. LaRue & G. Charpentier, 2008. A molecular revision of the taxonomic status of mermithid parasites of black flies from Quebec (Canada). Journal of Invertebrate Pathology 98: 299–306.

    CAS  PubMed  Article  Google Scholar 

  • Strugnell, J. M. & A. R. Lindgren, 2007. A barcode of life database for the Cephalopoda? Considerations and concerns. Reviews in Fish Biology and Fisheries 17: 337–344.

    Article  Google Scholar 

  • Tamura, K., D. Peterson, N. Peterson, G. Stecher, M. Nei & S. Kumar, 2011. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Marine Biology and Evolution 28: 2731–2739.

    CAS  Article  Google Scholar 

  • Thiele, J., 1935. Handbook of Systematic Malacology Part 3. English translation by J. S. Bhatti, 1998. Smithsonian Institution Libraries, Washington.

  • Toussiant, R. K., D. Scheel, G. K. Sage & S. L. Talbot, 2012. Nuclear and mitochondrial markers reveal evidence for genetically segregated cryptic speciation in giant Pacific octopuses from Prince William Sound, Alaska. Conservation Genetics 13: 1483–1497.

    Article  Google Scholar 

  • Vecchione, M. & R. E. Young, 2007a. Mastigoteuthis danae (Joubin, 1933). http://tolweb.org/Mastigoteuthis_danae/19511/2007.11.19. Accessed 2013 April 5.

  • Vecchione, M. & R. E. Young, 2007b. Mastigoteuthis atlantica Joubin, 1933. http://tolweb.org/Mastigoteuthis_atlantica/19509/2007.11.19. Accessed 2013 April 5.

  • Vecchione, M. & R. E. Young, 2010. Mastigoteuthis magna Joubin, 1913. http://tolweb.org/Mastigoteuthis_magna/19520/2010.08.15. Accessed 2013 April 5.

  • Vecchione, M., R. E. Young & A. Lindgren, 2007. Mastigoteuthidae Verrill, 1881. Mastigoteuthis Verrill, 1881. Whip-lash squid. http://tolweb.org/Mastigoteuthis/19453/2007.11.19. Accessed 2013 April 5.

  • Verrill, A., 1881. Report on the cephalopods and on some additional species dredged by the U.S. Fish Commission Steamer ‘Fish-hawk’, during the season of 1880. Bulletin of the Museum of Comparative Zoology Harvard 8: 99–116.

    Google Scholar 

  • Victor, B. C., R. H. Hanner, M. Shivji, J. Hyde & C. Caldow, 2009. Identification of the larval and juvenile stages of the Cubera Snapper, Lutjanus cyanopterus, using DNA barcoding. Zootaxa 2215: 24–36.

    Google Scholar 

  • Voss, G. L., 1956. A review of the cephalopods of the Gulf of Mexico. Bulletin of the Marine Science of the Gulf and Caribbean 6: 85–178.

    Google Scholar 

  • Xiong, B. & T. D. Kocher, 1991. Comparison of mitochondrial DNA sequences of seven morphospecies of black flies (Diptera: Simuliidae). Genome 34: 306–311.

    CAS  PubMed  Article  Google Scholar 

  • Young, R. E. & M. Vecchione, 2007. Mastigoteuthis pyrodes Young, 1972. http://tolweb.org/Mastigoteuthis_pyrodes/19523. Accessed 2013 June 13.

  • Young, R. E. & M. Vecchione, 2008. Chiroteuthid families. http://tolweb.org/Chiroteuthid_families/19410/2008.04.21. Accessed 2013 April 5.

  • Young, R. E., 1991. Chiroteuthid and related paralarvae from Hawaiian waters. Bulletin of Marine Science 49: 162–185.

    Google Scholar 

  • Young, R., 1972. The systematic and areal distribution of pelagic cephalopods from the seas off southern California. Smithsonian Contributions to Zoology 97: 1–159.

    Article  Google Scholar 

  • Young, R., A. Lindgren & M. Vecchione, 2008. Mastigoteuthis microlucens, a new species of the squid family Mastigoteuthidae (Mollusca: Cephalopoda). Proceedings of the Biological Society of Washington 121: 276–282.

    Article  Google Scholar 

  • Zwickl, D. J., 2006. Genetic algorithm approaches for the phylogenetic analysis of large biological sequence datasets under the maximum likelihood criterion. Ph.D. dissertation, The University of Texas at Austin.

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Acknowledgments

Many thanks to Mike Vecchione for tissue samples, and Tyjuana Nickens for assistance at the Smithsonian National Museum of Natural History. We would like to thank the Museum of New Zealand Te Papa Tongarewa, particularly Bruce Marshall, and the National Institute of Water and Atmospheric Research, Ltd. (NIWA), particularly Sadie Mills, Kareen Schnabel, Dean Stotter, and Darren Stevens, for access to specimens. Thanks to Colleen Higgins, Jesse Kelly, and Aaron Boyd Evans from Auckland University of Technology (AUT); Robert Hanner, Dirk Steinke, Jeff Gross, Natasha Serrao, and Jinzhong Fu from the University of Guelph; and Dick Young, Mike Vecchione, and Annie Lindgren for their contributions of other sequences to GenBank. Special thanks to Steve O’Shea for advice and to AUT and the Natural Sciences and Engineering Research Council of Canada (NSERC) for funding assistance with this research, and for support of the Canadian Centre for DNA Barcoding at the Biodiversity Institute of Ontario, and the BOLD team for efficient informatics support. Finally, we would like to thank the anonymous reviewers for their helpful comments.

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Correspondence to Heather E. Braid.

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Guest editors: Erica A. G. Vidal, Mike Vecchione & Sigurd von Boletzky / Cephalopod Life History, Ecology and Evolution

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Braid, H.E., McBride, P.D. & Bolstad, K.S.R. Molecular phylogenetic analysis of the squid family Mastigoteuthidae (Mollusca, Cephalopoda) based on three mitochondrial genes. Hydrobiologia 725, 145–164 (2014). https://doi.org/10.1007/s10750-013-1775-3

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Keywords

  • Mastigoteuthidae
  • DNA barcode
  • Cephalopod
  • Phylogeny
  • Integrative taxonomy