Invertebrate Systematics Invertebrate Systematics Society
Systematics, phylogeny and biogeography
RESEARCH ARTICLE

Investigating the taxonomy and systematics of marine wood borers (Bivalvia : Teredinidae) combining evidence from morphology, DNA barcodes and nuclear locus sequences

L. M. S. Borges A E , H. Sivrikaya B , A. le Roux C , J. R. Shipway D , S. M. Cragg D and F. O. Costa A

A Centre of Molecular and Environmental Biology (CBMA), Department of Biology, University of Minho, Campus de Gualtar, 4710-057 Braga, Portugal.

B Bartın University, Faculty of Forestry, 74100 Bartın, Turkey.

C 1 Impasse de mouettes, 56000 Vannes, France.

D Institute of Marine Science, School of Biological Sciences, University of Portsmouth, Ferry Road, Portsmouth PO4 9LY, England.

E Corresponding author. Email: luisa.borges@bio.uminho.pt; luisaborges2000@yahoo.co.uk

Invertebrate Systematics 26(6) 572-582 http://dx.doi.org/10.1071/IS12028
Submitted: 18 April 2012  Accepted: 13 September 2012   Published: 19 December 2012

Abstract

Marine wood-boring teredinids, some of the most destructive wood borers in the sea, are a particularly difficult group to identify from morphological features. While in most bivalve species shell features are used as diagnostic characters, in the teredinids shell morphology shows high intraspecific variation and thus identification is based almost entirely on the morphology of the pallets. In the present study we aimed at improving ‘taxonomic resolution’ in teredinids by combining morphological evidence with mitochondrial and nuclear DNA sequences, respectively Cytochrome c oxidase subunit I and small subunit rRNA 18S gene, to generate more rigorous and accessible identifications.

DNA barcodes of Atlantic and Mediterranean populations of Lyrodus pedicellatus diverged by ~20%, suggesting cryptic species in the morphospecies L. pedicellatus. The low intraspecific divergence found in barcodes of specimens of Nototeredo norvagica (0.78%) confirms that Atlantic and Mediterranean forms of N. norvagica, the latter sometimes reported as Teredo utriculus, are the same species. Teredothyra dominicensis was found for the first time in the Mediterranean. A match was obtained between our 18S sequences and sequences of T. dominicensis from Netherlands Antilles, confirming that T. dominicensis in the Mediterranean is the same species that occurs in the Caribbean. There were differences in 18S sequences between Bankia carinata from the Mediterranean and Caribbean, which may indicate cryptic species.


References

Ballast Water Convention (2004). Available at http://www.bsh.de/en/Marine_data/Environmental_protection/Ballastwater/index.jsp (accessed 14 April 2012).

Bartsch, P. (1921). A new classification of the shipworms and descriptions of some new wood boring mollusks. Proceedings of the Biological Society of Washington 34, 25–32. open url image1

Blaxter, M. L., Ley, P., Garey, J. R., Liu, L. X., Scheldeman, P., Vierstraete, A., Vanfleteren, J. R., Mackey, L. Y., Dorris, M., Frisse, L. M., Vida, J. T., and Thomas, W. K. (1998). A molecular evolutionary framework for the phylum Nematoda. Nature 392, 71–75.
A molecular evolutionary framework for the phylum Nematoda.CrossRef | 1:CAS:528:DyaK1cXhvVOgtb4%3D&md5=571f4f1c43fe354bb98ea068475bb165CAS | open url image1

Borges, L. M. S. (2007). Biogeography of wood boring organisms in European Coastal waters and new approaches to controlling borer attack. Ph.D. thesis, Portsmouth University, Portsmouth, UK.

Borges, L. M. S., Valente, A. A., Palma, P., and Nunes, L. (2010). Changes in the wood boring community in the Tagus estuary: a case study. Marine Biodiversity Records. 3, e41.
Changes in the wood boring community in the Tagus estuary: a case study.CrossRef | open url image1

Bucklin, A., Steinke, D., and Blanco-Bercial, L. (2011). DNA barcoding of marine Metazoa. Annual Review of Marine Science 3, 471–508.
DNA barcoding of marine Metazoa.CrossRef | open url image1

Calloway, C. B., and Turner, R. D. (1983). Documentation and implications of rapid successive gametogenic cycles and broods in the shipworm Lyrodus floridanus (Bartsch) (Bivalvia, Teredinidae). Journal of Shellfish Research 3, 65–69. open url image1

Calloway, C. B., and Turner, R. D (1987). Species pairs in the Teredinidae. International research group on wood preservation. IRG/WP/4142, 1–2.

Carlton, J. T. (1999). Molluscan invasions in marine and estuarine communities. Malacologia 41, 439–454. open url image1

Chessman, B., Williams, S., and Besley, C. (2007). Bioassessment of streams with macroinvertebrates: effect of sampled habitat and taxonomic resolution. Journal of the North American Benthological Society 26, 546–565.
Bioassessment of streams with macroinvertebrates: effect of sampled habitat and taxonomic resolution.CrossRef | open url image1

Clapp, W. F., and Kenk, R. (1963). ‘Marine Borers. An Annotated Bibliography’. (Office of Naval Research Department of the Navy. Washington, DC.)

Cobb, K. (2002). Return of castaway: the gripping story of a boring clam. Science News 162, 72–74.
Return of castaway: the gripping story of a boring clam.CrossRef | open url image1

Colborn, J., Crabtree, R. E., Shaklee, J. B., Pfeiler, E., and Bowen, B. W. (2001). The evolutionary enigma of bonefishes (Albula spp.): cryptic species and ancient separations in a globally distributed shorefish. Evolution 55, 807–820.
The evolutionary enigma of bonefishes (Albula spp.): cryptic species and ancient separations in a globally distributed shorefish.CrossRef | 1:CAS:528:DC%2BD3MXktleqtLk%3D&md5=c97f3258eed2acd817167b306ee301f8CAS | open url image1

Cole, T. J., and Turner, R. D. (1977). Genetic similarities of wood-boring bivalves (Pholadidae and Teredinidae) based on comparison of allozymes. The Biological Bulletin 153, 420. open url image1

Costa, F. O., and Antunes, P. M. (2012). The contribution of the Barcode of Life initiative to the discovery and monitoring of biodiversity. In ‘Natural Resources, Sustainability and Humanity – A Comprehensive View’. (Eds A. Mendonça, A. Cunha and R. Chakrabarti.) pp. 37–68. (Springer: Dordrecht.)

Costa, F. O., deWaard, J. R., Boutilier, J., Ratnasingham, S., Dooh, R. T., Hajibabaei, M., and Hebert, P. D. N. (2007). Biological inetifications through DNA barcodes: the case of the crustacean. Canadian Journal of Fisheries and Aquatic Sciences 64, 272–295.
| 1:CAS:528:DC%2BD2sXlt1Gqsbo%3D&md5=9d89bca9b399145dd7ed76fef409ae66CAS | open url image1

Costa, F. O., Henzler, C. M., Lunt, D. H., Whiteley, N., and Rock, J. (2009). Probing marine Gammarus (Amphipoda) taxonomy with DNA barcodes. Systematics and Biodiversity 7, 365–379.
Probing marine Gammarus (Amphipoda) taxonomy with DNA barcodes.CrossRef | open url image1

Cragg, S. M., Jumel, M.-C., Al-Horani, F. A., and Hendi, I. W. (2009). The life history characteristics of the wood-boring Teredo bartschi are suited to the elevated salinity, oligotrophic circulation in the Gulf of Aqaba, Red Sea. Journal of Experimental Marine Biology and Ecology 375, 99–105.
The life history characteristics of the wood-boring Teredo bartschi are suited to the elevated salinity, oligotrophic circulation in the Gulf of Aqaba, Red Sea.CrossRef | open url image1

Demir, M. (2003). Shells of Mollusca collected from the seas of Turkey. Turkish Journal of Zoology 27, 101–140. open url image1

Distel, D. L., Amim, M., Burgoyne, A., Linton, E., Mamangkey, G., Morrill, W., Nove, J., Wood, N., and Yang, J. (2011). Molecular phylogeny of Pholadoidea Lamarck, 1809 supports a single origin for xylotrophy (wood feeding) and xylotrophic bacterial endosymbiosis in Bivalvia. Molecular Phylogenetics and Evolution 61, 245–254.
Molecular phylogeny of Pholadoidea Lamarck, 1809 supports a single origin for xylotrophy (wood feeding) and xylotrophic bacterial endosymbiosis in Bivalvia.CrossRef | open url image1

Edmondson, C. H. (1955). Resistance of woods to marine borers in Hawaiian waters. Bernice P. Bishop Museum occasional papers 217, 1–91. open url image1

Espiñeira, M., González-Lavín, N., Vieites, J. M., and Santaclara, F. J. (2009). Development of a method for the genetic identification of commercial bivalve species based on mitochondrial 18S rRNA sequences. Journal of Agricultural and Food Chemistry 57, 495–502.
Development of a method for the genetic identification of commercial bivalve species based on mitochondrial 18S rRNA sequences.CrossRef | open url image1

Feng, Y., Li, Q., Kong, L., and Zheng, X. (2011). DNA barcoding and phylogenetic analysis of Pectinidae (Mollusca: Bivalvia) based on mitochondrial COI and 16S rRNA genes. Molecular Biology Reports 38, 291–299.
DNA barcoding and phylogenetic analysis of Pectinidae (Mollusca: Bivalvia) based on mitochondrial COI and 16S rRNA genes.CrossRef | 1:CAS:528:DC%2BC3cXhsFSmtL%2FJ&md5=d3cab13c4719e0d33cc639b222e829ceCAS | open url image1

Fernandes, J. N., Cruz, T., and van Syoc, R. (2010). Pollicipes caboverdensis sp. nov. (Crustacea: Cirripedia: Scalpelliformes) an intertidal barnacle from the Cape Verde Islands. Zootaxa 2557, 29–38. open url image1

Folmer, O., Black, M., Hoeh, W., Lutz, R., and Vrijenhoek, R. (1994). DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology 3, 294–299.
| 1:CAS:528:DyaK2MXjt12gtLs%3D&md5=0a6e1d841a9ef8fafdf936427c59141bCAS | open url image1

Fonseca, V. G., Carvalho, G. R., Sung, W., Johnson, H. F., Power, D. M., Neill, S. P., Packer, M., Blaxter, M. L., Lambshead, P. J., Thomas, W. K., and Creer, S. (2010). Second-generation environmental sequencing unmasks marine metazoan biodiversity. Nature communications , 1–98.
Second-generation environmental sequencing unmasks marine metazoan biodiversity.CrossRef | open url image1

Fougerousse, M. (1971). Resistance naturelle des bois tropicaux aux attaques des organismes xylophages marins. In ‘Les Perforants, les Champignons et les Salissures du Bois en Millieu Marin’. (Eds E. B. G. Jones and S. K. Eltringham.) pp. 347–358. (OECD: Paris.)

Giribet, G., and Wheeler, W. C. (2002). On bivalve phylogeny: a high-level analysis of the Bivalvia (Mollusca) based on combined morphology and DNA sequence data. Invertebrate Biology 121, 271–324.
On bivalve phylogeny: a high-level analysis of the Bivalvia (Mollusca) based on combined morphology and DNA sequence data.CrossRef | open url image1

Gollasch, S. (2002). The importance of ship hull fouling as a vector of species introduction into the North Sea. Biofouling 18, 105–121.
The importance of ship hull fouling as a vector of species introduction into the North Sea.CrossRef | open url image1

Graeffe, P. (1900). Üebersicht über die Fauna des Golfes von Triest nebst Notizen über Vorkommen, Lebenweise, Erscheinungs- und Laichzeit der einzelen Arten. Vol. V. Crustacea. Arb. aus den Zool. Inst. Univ. Wien und Zool. Stat. Triest 13, 33–80. open url image1

Gray, J. E. (1827). A monograph of the genus Teredo Linné, with descriptive characters of the species in the British Museum. Philosophical Magazine 2, 409–411. open url image1

Guindon, S., and Gascuel, O. (2003). PhyML – a simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Systematic Biology 52, 696–704.
PhyML – a simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood.CrossRef | open url image1

Guindon, S., Delsuc, F., Dufayard, J. F., and Gascuel, O. (2009). Estimating Maximum Likelihood Phylogenies with PhyML. In ‘Bioinformatics for DNA Sequence Analysis’. (Ed. D. Posada.) pp. 113–139. (Humana Press: New York.)

Hebert, P. D. N., Cywinska, A. A., Ball, S. L., and deWaard, J. R. (2003). Biological identifications through DNA barcodes. Proceedings of the Royal Society of London. Series B – Biological Sciences 270, 313–321.
| 1:CAS:528:DC%2BD3sXktVWiu7g%3D&md5=bacde07336013937477a1e8839a85156CAS | open url image1

Hoagland, K. E., and Turner, R. D. (1981). Evolution and adaptative radiation of wood-boring bivalves (Pholadacea). Malacologia 21, 111–148.
| 1:CAS:528:DyaL38Xjt1SjsQ%3D%3D&md5=2fb433b6fc5064f089eae0ab1a499d14CAS | open url image1

Jones, D. T., Taylor, W. R., and Thornton, J. M. (1992). The rapid generation of mutation data matrices from protein sequences. Computer Applications in the Biosciences 8, 275–282.
| 1:CAS:528:DyaK38Xlt1Okt7w%3D&md5=7000da0b2d11826f6b758942c8fb79cdCAS | open url image1

Kofoid, C. A., and Miller, R. C. (1927). Marine borers and their relation to marine construction on the Pacific coast. Final report of the San Francisco Bay Marine Piling Committee. Committee of the San Francisco Bay, California. pp. 188–295.

Lebour, M. V. (1946). The species of Teredo from Plymouth waters. Journal of the Marine Biological Association of the United Kingdom 26, 381–389.
The species of Teredo from Plymouth waters.CrossRef | open url image1

Macintosh, H. (2012). Lyrodus turnerae, a new teredinid from eastern Australia and the Coral Sea (Bivalvia: Teredinidae). Molluscan Research 32, 36–42. open url image1

Miloslavich, P., Díaz, J. M., Klein, E., Alvarado, J. J., Díaz, C., Gobin, J., Escobar-Briones, E., Cruz-Motta, J. J., Weile, E., Cortés, J., Bastidas, A. C., Robertson, R., Zapata, F., Martín, A., Castillo, J., Kazandjian, A., and Ortiz, M. (2010). Marine biodiversity in the Caribbean: regional estimates and distribution patterns. PLoS ONE 5, e11916.
Marine biodiversity in the Caribbean: regional estimates and distribution patterns.CrossRef | open url image1

Paalvast, P., and van der Velde, G. (2011). New threats of an old enemy: the distribution of the shipworm Teredo navalis L. (Bivalvia: Teredinidae) related to climate change in the Port of Rotterdam area, the Netherlands. Marine Pollution Bulletin 62, 1822–1829.
New threats of an old enemy: the distribution of the shipworm Teredo navalis L. (Bivalvia: Teredinidae) related to climate change in the Port of Rotterdam area, the Netherlands.CrossRef | 1:CAS:528:DC%2BC3MXovFKqsr4%3D&md5=061b3f92d2c6996a51b15d8e2ad93aaaCAS | open url image1

Posada, D. A., and Crandall, K. A. (1998). ModelTest: testing the model of DNA substitution. Bioinformatics (Oxford, England) 14, 817–818.
ModelTest: testing the model of DNA substitution.CrossRef | 1:CAS:528:DyaK1MXktlCltw%3D%3D&md5=96deade1c75c4e555f1a98ea1a9c9435CAS | open url image1

Radulovici, A., Saint-Marie, B., and Dufresne, F. (2009). DNA barcoding of marine crustaceans from the Estuary and Gulf of St Lawrence: a regional-scale approach. Molecular Ecology Resources 9, 181–187.
DNA barcoding of marine crustaceans from the Estuary and Gulf of St Lawrence: a regional-scale approach.CrossRef | 1:CAS:528:DC%2BD1MXlslOjtrs%3D&md5=46e77ca2e6e692b0e7ab05323b022058CAS | open url image1

Radulovici, A., Archambault, P., and Dufresne, F. (2010). DNA barcodes for marine biodiversity: moving fast forward. Diversity 2, 450–472.
DNA barcodes for marine biodiversity: moving fast forward.CrossRef | 1:CAS:528:DC%2BC3cXkslems7w%3D&md5=ba6ef5bff7bf6eac2f2d110deaaf9a9aCAS | open url image1

Ratnasingham, S., and Hebert, P. D. N. (2007). BOLD: The Barcode of Life Data System (www.barcodinglife.org). Molecular Ecology Notes 7, 355–364.
BOLD: The Barcode of Life Data System (www.barcodinglife.org).CrossRef | 1:CAS:528:DC%2BD2sXntVyksbc%3D&md5=53cd40598900a88b3cc1c91ad7b9427cCAS | open url image1

Raupach, M. J., and Wägele, J.-W. (2006). Distinguish cryptic species in Antarctic Asellota (Crustacea: Isopoda) – a preliminary study of mitochondrial DNA in Acanthaspidia drygalskii. Antarctic Science 18, 191–198.
Distinguish cryptic species in Antarctic Asellota (Crustacea: Isopoda) – a preliminary study of mitochondrial DNA in Acanthaspidia drygalskii.CrossRef | open url image1

Rayner, S. M. (1983). Distribution of teredinids (Mollusca: Teredinidae) in Papua New Guinea. Records of the Australian Museum 35, 61–76.
Distribution of teredinids (Mollusca: Teredinidae) in Papua New Guinea.CrossRef | open url image1

Roch, F. (1931). Die Terediniden der skandinavischen Museumssammlunen (Stockholm, Gothenburg, Kopenhagen, Oslo, Nidaros und Tromsø). Ark. för Zool 22, 1–29. open url image1

Santos, S. M. L., Tagliaro, C. H., Beasley, C. R., Schneider, H., Sampaio, I., Filho, C. S., and Müller, A. C. P. (2005). Taxonomic implications of molecular studies on northern Brazilian Teredinidae (Mollusca: Bivalvia) specimens. Genetics and Molecular Biology 28, 175–179.
Taxonomic implications of molecular studies on northern Brazilian Teredinidae (Mollusca: Bivalvia) specimens.CrossRef | 1:CAS:528:DC%2BD2MXkt1Gisb0%3D&md5=7c18c0aa5b0379749c7121363b96d83aCAS | open url image1

Sivrikaya, H., Cragg, S. M., and Borges, L. M. S. (2009). Variation in resistance to marine borers in commercial timbers from Turkey, as assessed by marine trial and laboratory screening. Turkish Journal of Agriculture and Forestry 33, 569–576. open url image1

Spengler, L. (1792). Betragtninger og Anmaerkniger ved den Linneiske Slaegt Pholas blantde mangeskallede Muskeler, med dens hidindtil bekiendte gamle og nye Arter, samt den dermed i Forbindelse staaende Slaegt Teredo Linn. Skrivter af Naturhistorie-Selskabet (Kiøenhavn) 2, 72–106. open url image1

Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M., and Kumar, S. (2011). MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution 28, 2731–2739.
MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods.CrossRef | 1:CAS:528:DC%2BC3MXht1eiu73K&md5=ff48f25899fc988f16ef1534cf14445fCAS | open url image1

Taylor, J. D., Williams, S. T., Glover, E., and Dyal, P. (2007). A molecular phylogeny of heterodont bivalves (Mollusca: Bivalvia: Heterodonta): new analyses of 18S and 28S rRNA genes. Zoologica Scripta 36, 587–606.
A molecular phylogeny of heterodont bivalves (Mollusca: Bivalvia: Heterodonta): new analyses of 18S and 28S rRNA genes.CrossRef | open url image1

Teletchea, F. (2010). After 7 years and 1000 citations: comparative assessment of the DNA barcoding and the DNA taxonomy proposals for taxonomists and non-taxonomists. Mitochondrial DNA 21, 206–226.
After 7 years and 1000 citations: comparative assessment of the DNA barcoding and the DNA taxonomy proposals for taxonomists and non-taxonomists.CrossRef | 1:CAS:528:DC%2BC3cXhsFyksr7P&md5=d5601c42f89c81e26ea46e0b60bfa064CAS | open url image1

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. Nucleic Acids Research 22, 4673–4680.
CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice.CrossRef | 1:CAS:528:DyaK2MXitlSgu74%3D&md5=30ced7c55989028a0f69fafe641cd83eCAS | open url image1

Turgeon, D. D., Lyons, W. G., Mikkelsen, P. G., Rosenberg, G., and Moretzsohn, F. (2009). Bivalvia (Mollusca) of the Gulf of Mexico. In ‘Gulf of Mexico. Origins, Waters, and Biota. Vol. 1: Biodiversity’. (Eds D. L. Felder and D. K. Camp.) pp. 711–744. (Texas A&M Press: College Station, TX.)

Turner, R. D. (1966). ‘A Survey and Illustrated Catalogue of the Teredinidae.’ (Harvard University: Cambridge, MA.).

Turner, R. D. (1971). Identification of marine wood-boring molluscs. In ‘Marine Borers, Fungi and Fouling Organisms’. (Eds E. B. G. Jones and S. K. Eltringham.) pp. 17–62. (Organisation for Economic Cooperation and Development: Paris.)

Wake, D. B. (1991). Homoplasy: the result of natural selection, or evidence of design limitations? American Naturalist 138, 543–567.
Homoplasy: the result of natural selection, or evidence of design limitations?CrossRef | open url image1



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