Phylogenetic placement of a new hoplonemertean species commensal on ascidians
Juan Junoy A B , Sónia C. S. Andrade B and Gonzalo Giribet B C
+ Author Affiliations
- Author Affiliations
A Departamento de Zoología y Antropología Física, Universidad de Alcalá, E-28871 Alcalá de Henares, Spain.
B Museum of Comparative Zoology, Department of Organismic and Evolutionary Biology, Harvard University, 26 Oxford St, Cambridge, MA 02138, USA.
C Corresponding author. Email: ggiribet@oeb.harvard.edu
Invertebrate Systematics 24(6) 616-629 https://doi.org/10.1071/IS10036
Submitted: 2 November 2010 Accepted: 11 February 2011 Published: 29 April 2011
Abstract
The hoplonemertean Vieitezia luzmurubeae, gen. et sp. nov. is described from specimens collected in a national park on the north-west Iberian Peninsula, the Parque Nacional Marítimo-Terrestre das Illas Atlánticas de Galicia. The species, previously mistaken as the Mediterranean species Tetrastemma vittigerum (Bürger, 1904), is frequently associated with two common species of sea squirt, Phallusia mamillata (Cuvier, 1815) and Ciona intestinalis (Linnaeus, 1767), inside which the nemertean completes its life cycle. Some of the specimens examined were protandrous hermaphrodites. Data on morphology and anatomy are provided with illustrations. Sequences of the nuclear ribosomal gene 18S rRNA and the mitochondrial gene cytochrome c oxidase subunit I were compared with those of other hoplonemertean species and all phylogenetic analyses suggested that Vieitezia is sister to the genus Gononemertes, which parasitises ascidians, within a clade also containing the genera Oerstedia and Nemertellina. In contrast, the morphologically similar genus Tetrastemma appears in a separate clade. This study stresses the need for combining molecular and morphological data when studying nemertean biodiversity.
Additional keywords: COI, Galicia, 18S rRNA, phylogeny, Vieitezia luzmurubeae, gen. et sp. nov.
References
Akaike, H. (1974). A new look at the statistical model identification. IEEE Transactions on Automatic Control 19, 716–723.| A new look at the statistical model identification.Crossref | GoogleScholarGoogle Scholar |
Altschul, S., Madden, T., Schaffer, A., Zhang, J., Zhang, Z., Miller, W., and Lipman, D. (1997). Gapped Blast and Psi-blast: a new generation of protein database search programs. Nucleic Acids Research 25, 3389–3402.
| Gapped Blast and Psi-blast: a new generation of protein database search programs.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXlvFyhu7w%3D&md5=8ad95ecb1fd665273ec783b9d2afdba4CAS | 9254694PubMed |
Anadón, N., and Bitar, G. (1992). On the anatomy of Oerstedia vittata Hubrecht, 1879 (Nemertea, Enopla, Monostiliferoidea) from the Moroccan coast. Bulletin de la Société Zoologique de France 117, 383–391.
Bergendal, D. (1900). Über ein paar sehr eigenthümliche nordische Nemertinen. Zoologischer Anzeiger 23, 313–328.
Brinkmann, A. (1927). Gononemertes parasita und ihre stellung im system. Nyt Magazin for Naturvidenskaberne 65, 57–81.
Bürger, O. (1895). Die Nemertinen des Golfes von Neapel und der angrenzenden Meeres-Abschnitte. Fauna und Flora des Golfes von Neapel 22, 1–743.
Bürger, O. (1904). Nemertini. Das Tierreich 20, 1–151.
Chernyshev, A. V. (1999). Nemerteans of the genus Antarctonemertes (Enopla, Monostilifera). Zoologeski Zhournal 78, 939–948.
Coe, W. R. (1905). Nemerteans of the west and northwest coasts of America. Bulletin of the Museum of Comparative Zoology at Harvard College 47, 1–318.
Envall, M., and Sundberg, P. (1993). Intraspecific variation in nemerteans (Nemertea): synonymization of the genera Parorstedia and Oerstediella with Oerstedia. Journal of Zoology 230, 293–318.
| Intraspecific variation in nemerteans (Nemertea): synonymization of the genera Parorstedia and Oerstediella with Oerstedia.Crossref | GoogleScholarGoogle Scholar |
Envall, M., and Sundberg, P. (1998). Phylogenetic relationships and genetic distances between some monostiliferous interstitial nemerteans (Ototyphlonemertes, Hoplonemertea, Nemertea) indicated from the 16S rRNA gene. Zoological Journal of the Linnean Society 123, 105–115.
| Phylogenetic relationships and genetic distances between some monostiliferous interstitial nemerteans (Ototyphlonemertes, Hoplonemertea, Nemertea) indicated from the 16S rRNA gene.Crossref | GoogleScholarGoogle Scholar |
Farris, J. S., Albert, V. A., Källersjö, M., Lipscomb, D., and Kluge, A. G. (1996). Parsimony jackknifing outperforms neighbor-joining. Cladistics 12, 99–124.
| Parsimony jackknifing outperforms neighbor-joining.Crossref | GoogleScholarGoogle Scholar |
Felsenstein, J. (2004). ‘Inferring Phylogenies.’ (Sinauer Associates: Sunderland, MA.)
Folmer, O., Black, M., Hoeh, W., Lutz, R., and Vrijenhoek, R. C. (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=002ef50a594fc86f823ca8ae866828c6CAS | 7881515PubMed |
Friedrich, H. (1936). ‘Nemertini.’ Tierwelt der Nord- und Ostsee. IV. d, 1–69.
Gibson, R. (1972). ‘Nemerteans.’ (Hutchinson & Co.: London.)
Gibson, R. (1974). A new species of commensal hoplonemertean from Australia. Zoological Journal of the Linnean Society 55, 247–266.
| A new species of commensal hoplonemertean from Australia.Crossref | GoogleScholarGoogle Scholar |
Gibson, R. (1982). Nemertea. In: ‘Synopsis and Classification of Living Organisms. Vol. 1’. (Ed. S. P. Parker.) pp. 823–846. (McGraw-Hill: New York, NY.)
Gibson, R. (1994). ‘Nemerteans: Keys and Notes for Identification of the Species.’ (The Linnean Society of London and The Estuarine and Coastal Sciences Association, Field Studies Council: Shrewsbury, UK.)
Gibson, R. (1995). Nemertean genera and species of the world: an annotated checklist of original names and description citations, synonyms, current taxonomic status, habitats and recorded zoogeographic distribution. Journal of Natural History 29, 271–561.
| Nemertean genera and species of the world: an annotated checklist of original names and description citations, synonyms, current taxonomic status, habitats and recorded zoogeographic distribution.Crossref | GoogleScholarGoogle Scholar |
Gibson, R., and Sundberg, P. (2002). Some heteronemerteans (Nemertea) from the Solomon Islands. Journal of Natural History 36, 1785–1804.
| Some heteronemerteans (Nemertea) from the Solomon Islands.Crossref | GoogleScholarGoogle Scholar |
Giribet, G., Carranza, S., Baguñà, J., Riutort, M., and Ribera, C. (1996). First molecular evidence for the existence of a Tardigrada + Arthropoda clade. Molecular Biology and Evolution 13, 76–84.
| 1:CAS:528:DyaK28XhtVylur8%3D&md5=282d2668a431c326241b8fe131f8becaCAS | 8583909PubMed |
Gontcharoff, M. (1955). Nemertes. Inventaire de la Faune Marine de Roscoff , 3–15.
Harant, H. (1931). Les ascidies et leurs parasites. Annales de l’Institut Océanographique de Monaco 8, 231–389.
Hubrecht, A. A. W. (1879). The genera of European nemerteans critically revised, with description of several new species. Notes from the Leyden Museum 1, 193–232.
Joubin, L. (1890). Recherches sur les Turbellariés des côtes de France (Némertes). Archives de Zoologie Experimentale et Generale, Serie 2 8, 461–602.
Joubin, L. (1894). ‘Les Némertiens: Faune Française.’ (Eds R. Blanchard and J. de Guerne.) (Societé d’Editions Scientifiques: Paris.)
Junoy, J., and Herrera-Bachiller, A. (2010). Los Nemertinos del Parque Nacional Marítimo-Terrestre de las Islas Atlánticas de Galicia. In ‘Proyectos de Investigación en Parques Nacionales: 2006–2009’. (Eds L. Ramírez and B. Asensio.) pp. 311–325. (Organismo Autónomo Parques Nacionales: Madrid.)
Katoh, K., Kuma, K., Toh, H., and Miyata, T. (2005). MAFFT version 5: improvement in accuracy of multiple sequence alignment. Nucleic Acids Research 33, 511–518.
| MAFFT version 5: improvement in accuracy of multiple sequence alignment.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtV2qsbc%3D&md5=b41a068be746c1713b8929ff668957a4CAS | 15661851PubMed |
Kirsteuer, E. (1963). Beitrag zur kenntnis der systematik und anatomie der adriatischen nemertinen (genera Tetrastemma, Oerstedia, Oerstediella). Zoologische Jahrbiicher. Abteilungen Anatomie und Ontogenie der Tiere 80, 555–616.
Langerhans, P. (1880). Die wurmfauna von Madeira III. Zeitschrift fur Wissenschartliche Zoologie 34, 87–143.
Levitan, D. R. (1995). The ecology of fertilization in free-spawning invertebrates. In ‘Ecology of Marine Invertebrate Larvae’. (Ed. L. McEdward.) pp. 123–156. (CRC Press: Boca Raton, FL.)
Maslakova, S. A., and Norenburg, J. L. (2008a). Revision of the smiling worms, genus Prosorhochmus Keferstein, 1862, and description of a new species, Prosorhochmus belizeanus sp. nov. (Prosorhochmidae, Hoplonemertea, Nemertea) from Florida and Belize. Journal of Natural History 42, 1219–1260.
| Revision of the smiling worms, genus Prosorhochmus Keferstein, 1862, and description of a new species, Prosorhochmus belizeanus sp. nov. (Prosorhochmidae, Hoplonemertea, Nemertea) from Florida and Belize.Crossref | GoogleScholarGoogle Scholar |
Maslakova, S. A., and Norenburg, J. L. (2008b). Revision of the smiling worms, genera Prosadenoporus Bürger, 1890 and Pantinonemertes Moore and Gibson, 1981 and description of a new species Prosadenoporus floridensis sp. nov. (Prosorhochmidae; Hoplonemertea; Nemertea) from Florida and Belize. Journal of Natural History 42, 1689–1727.
| Revision of the smiling worms, genera Prosadenoporus Bürger, 1890 and Pantinonemertes Moore and Gibson, 1981 and description of a new species Prosadenoporus floridensis sp. nov. (Prosorhochmidae; Hoplonemertea; Nemertea) from Florida and Belize.Crossref | GoogleScholarGoogle Scholar |
Monniot, C. (1990). Diseases of Urochordata. In ‘Diseases of Marine Animals. Vol 3’. (Ed. O. Kinne.) pp. 569–636. (Biologische Anstalt Helgoland: Hamburg.)
Oxner, M. (1907). Quelques observations sur les Nemertes de Roscoff et de Villefranche-sur-Mer. Archives de Zoologie Experimentale et Generale, Série 4 6, 82–92.
Pond, S. L. K., Frost, S. D. W., and Muse, S. V. (2005). HyPhy: hypothesis testing using phylogenies. Bioinformatics 21, 676–679.
| HyPhy: hypothesis testing using phylogenies.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhslSlurs%3D&md5=1f467b717adf620b1d27d5fb34fb4635CAS | 15509596PubMed |
Posada, D., and Crandall, K. A. (1998). Modeltest: testing the model of DNA substitution. Bioinformatics 14, 817–818.
| Modeltest: testing the model of DNA substitution.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXktlCltw%3D%3D&md5=d2bcfda7a0dd43b2a56458d7a5084483CAS | 9918953PubMed |
Puerta, P., Andrade, S. C. S., and Junoy, J. (2010). Redescription of Lineus acutifrons Southern, 1913 (Nemertea : Pilidiophora) and comments on its phylogenetic position. Journal of Natural History 44, 2363–2378.
| Redescription of Lineus acutifrons Southern, 1913 (Nemertea : Pilidiophora) and comments on its phylogenetic position.Crossref | GoogleScholarGoogle Scholar |
Ramírez, M. J., Coddington, J. A., Maddison, W. P., Midford, P. E., Prendini, L., Miller, J., Griswold, C. E., Hormiga, G., Sierwald, P., Scharff, N., Benjamin, S. P., and Wheeler, W. C. (2007). Linking of digital images to phylogenetic data matrices using a morphological ontology. Systematic Biology 56, 283–294.
| Linking of digital images to phylogenetic data matrices using a morphological ontology.Crossref | GoogleScholarGoogle Scholar | 17464883PubMed |
Riser, N. W. (1985). Epilogue: Nemertinea, a successful phylum. American Zoologist 25, 145–151.
Riser, N. W. (1988). Notogaeanemertes folzae gen. n., sp. n., an additional ecologically restricted hoplonemertean from New Zealand. Hydrobiologia 156, 125–133.
| Notogaeanemertes folzae gen. n., sp. n., an additional ecologically restricted hoplonemertean from New Zealand.Crossref | GoogleScholarGoogle Scholar |
Schwartz, M. L. (2009). Untying a Gordian knot of worms: systematics and taxonomy of the Pilidiophora (phylum Nemertea) from multiple data sets. Ph.D. Thesis, The George Washington University, Washington, D.C.
Schwartz, M. L., and Norenburg, J. L. (2001). Can we infer heteronemertean phylogeny from available morphological data? Hydrobiologia 456, 165–174.
| Can we infer heteronemertean phylogeny from available morphological data?Crossref | GoogleScholarGoogle Scholar |
Stamatakis, A. (2006). RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22, 2688–2690.
| RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtFKlsbfI&md5=06d9041d7f874751d1cf289adbd4caf9CAS | 16928733PubMed |
Stamatakis, A., Hoover, P., and Rougemont, J. (2008). A fast bootstrapping algorithm for the RaxML web-servers. Systematic Biology 57, 758–771.
| A fast bootstrapping algorithm for the RaxML web-servers.Crossref | GoogleScholarGoogle Scholar | 18853362PubMed |
Stiasny-Winjhoff, G. (1930). Die Gattung Oerstedia. Zöologische Mededelingen, Leiden 13, 226–240.
Strand, M., and Sundberg, P. (2005). Delimiting species in the hoplonemertean genus Tetrastemma (phylum Nemertea): morphology is not concordant with phylogeny as evidenced from mtDNA sequences. Biological Journal of the Linnean Society. Linnean Society of London 86, 201–212.
| Delimiting species in the hoplonemertean genus Tetrastemma (phylum Nemertea): morphology is not concordant with phylogeny as evidenced from mtDNA sequences.Crossref | GoogleScholarGoogle Scholar |
Strand, M., and Sundberg, P. (2011). A DNA-based description of a new nemertean (phylum Nemertea) species. Marine Biology Research 7, 63–70.
| A DNA-based description of a new nemertean (phylum Nemertea) species.Crossref | GoogleScholarGoogle Scholar |
Sundberg, P., and Strand, M. (2010). Nemertean taxonomy – time to change lane? Journal of Zoolology Systematics and Evolutionary Research 48, 283–284.
Sundberg, P., Turbeville, J. M., and Lindh, S. (2001). Phylogenetic relationships among higher nemertean taxa inferred from 18S rDNA sequences. Molecular Phylogenetics and Evolution 20, 327–334.
| Phylogenetic relationships among higher nemertean taxa inferred from 18S rDNA sequences.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXmtleis7g%3D&md5=2837e7f0f3c099518dca368a69ebad59CAS | 11527461PubMed |
Sundberg, P., Gibson, R., and Strand, M. (2007). Swedish nemerteans (phylum Nemertea), with description of a new hoplonemertean genus and species. Journal of Natural History 41, 2287–2299.
| Swedish nemerteans (phylum Nemertea), with description of a new hoplonemertean genus and species.Crossref | GoogleScholarGoogle Scholar |
Sundberg, P., Chernyshev, A. V., Kajihara, H., Kånneby, T., and Strand, M. (2009). Character-matrix based descriptions of two new nemertean (Nemertea) species. Zoological Journal of the Linnean Society 157, 264–294.
| Character-matrix based descriptions of two new nemertean (Nemertea) species.Crossref | GoogleScholarGoogle Scholar |
Thiel, M., and Junoy, J. (2006). Mating behavior of nemerteans: present knowledge and future directions. Journal of Natural History 40, 1021–1034.
| Mating behavior of nemerteans: present knowledge and future directions.Crossref | GoogleScholarGoogle Scholar |
Thollesson, M., and Norenburg, J. L. (2003). Ribbon worms relationship: a phylogeny of the phylum Nemertea. Proceedings. Biological Sciences 270, 407–415.
| Ribbon worms relationship: a phylogeny of the phylum Nemertea.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXktVWiu70%3D&md5=cb2b5edcd4e483d2f92c71b1a1bc6293CAS |
Varón, A., Sy Vinh, L., and Wheeler, W. C. (2010). POY version 4: phylogenetic analysis using dynamic homologies. Cladistics 26, 72–85.
| POY version 4: phylogenetic analysis using dynamic homologies.Crossref | GoogleScholarGoogle Scholar |
Verrill, A. E. (1874). Brief contributions to Zoology from the Museum of Yale College. No. 26. Results of recent dredging expeditions on the coast of New England. American Journal of Science, Series 3 7, 38–46.
Wheeler, W. C. (1996). Optimization alignment: the end of multiple sequence alignment in phylogenetics? Cladistics 12, 1–9.
| Optimization alignment: the end of multiple sequence alignment in phylogenetics?Crossref | GoogleScholarGoogle Scholar |
Whiting, M. F., Carpenter, J. M., Wheeler, Q. D., and Wheeler, W. C. (1997). The Strepsiptera problem: phylogeny of the holometabolous insect orders inferred from 18S and 28S ribosomal DNA sequences and morphology. Systematic Biology 46, 1–68.
| 1:STN:280:DC%2BD383js1yqtQ%3D%3D&md5=0f7617b7c2a71160c61603d215d15751CAS | 11975347PubMed |
