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

New insights into the phylogeny, systematics and DNA barcoding of Nemertea

Sebastian Kvist A C , Christopher E. Laumer A , Juan Junoy B and Gonzalo Giribet A

A Museum of Comparative Zoology, Department of Organismic and Evolutionary Biology, Harvard University, 26 Oxford Street, Cambridge, MA 02138, USA.

B EU_US Marine Biodiversity Research Group, Dpto de Ciencias de la Vida and Instituto Franklin, Universidad de Alcalá, E-28871 Alcalá de Henares, Spain.

C Corresponding author. Email: skvist@fas.harvard.edu

Invertebrate Systematics 28(3) 287-308 https://doi.org/10.1071/IS13061
Submitted: 6 December 2013  Accepted: 5 February 2014   Published: 30 June 2014

Abstract

Although some clades of ribbon worms (phylum Nemertea) are consistently recovered with high support in molecular phylogenies, the placement and inter-relationships of some taxa have proven problematic. Herein, we performed molecular phylogenetic analyses aimed at resolving these recalcitrant splits, using six loci (nuclear 18S rRNA, 28S rRNA, histones H3 and H4, and mitochondrial 16S rRNA and COI) for 133 terminals, with particular emphasis on the problematic families Hubrechtidae and Plectonemertidae. Three different datasets were used for phylogenetic analyses and both maximum likelihood and maximum parsimony methodologies were applied. All but one of the resulting tree topologies agree on the paraphyly of the class Palaeonemertea, whereas Heteronemertea, Hoplonemertea, Polystilifera, Monostilifera and Hubrechtidae are always recovered as reciprocally monophyletic. Hubrechtidae is sister group to Heteronemertea (the Pilidiophora hypothesis) only when length variable regions of 18S rRNA and 28S rRNA are excluded. Moreover, the terrestrial and freshwater family Plectonemertidae is recovered with high support and the implications of this finding are further discussed. Finally, we evaluate the utility of DNA barcoding for specimen identification within Nemertea using an extended dataset containing 394 COI sequences. Results suggest that DNA barcoding may work for Nemertea, insofar as a distinct barcoding gap (the gap between the maximum intraspecific variation and the minimum interspecific divergence) may exist, but its recognition is regularly hampered by low accuracy in species level identifications.

Additional keywords: cytochrome c oxidase subunit I, Hubrechtidae, Plectonemertidae, Pilidiophora.


References

Andrade, S. C. S., Strand, M., Schwartz, M., Chen, H., Kajihara, H., von Döhren, J., Sun, S., Junoy, J., Thiel, M., Norenburg, J. L., Turbeville, J. M., Giribet, G., and Sundberg, P. (2012). Disentangling ribbon worm relationships: multi-locus analysis supports traditional classification of the phylum Nemertea. Cladistics 28, 141–159.
Disentangling ribbon worm relationships: multi-locus analysis supports traditional classification of the phylum Nemertea.CrossRef | open url image1

Appeltans, W., Ahyong, S. T., Anderson, G., Angel, M. V., Artois, T., Bailly, N., Bamber, R., Barber, A., Bartsch, I., Berta, A., Blazewicz-Paszkowycz, M., Bock, P., Boxshall, G., Boyko, C. B., Brandao, S. N., Bray, R. A., Bruce, N. L., Cairns, S. D., Chan, T. Y., Cheng, L., Collins, A. G., Cribb, T., Curini-Galletti, M., Dahdouh-Guebas, F., Davie, P. J., Dawson, M. N., De Clerck, O., Decock, W., De Grave, S., de Voogd, N. J., Domning, D. P., Emig, C. C., Erséus, C., Eschmeyer, W., Fauchald, K., Fautin, D. G., Feist, S. W., Fransen, C. H., Furuya, H., Garcia-Alvarez, O., Gerken, S., Gibson, D., Gittenberger, A., Gofas, S., Gomez-Daglio, L., Gordon, D. P., Guiry, M. D., Hernandez, F., Hoeksema, B. W., Hopcroft, R. R., Jaume, D., Kirk, P., Koedam, N., Koenemann, S., Kolb, J. B., Kristensen, R. M., Kroh, A., Lambert, G., Lazarus, D. B., Lemaitre, R., Longshaw, M., Lowry, J., Macpherson, E., Madin, L. P., Mah, C., Mapstone, G., McLaughlin, P. A., Mees, J., Meland, K., Messing, C. G., Mills, C. E., Molodtsova, T. N., Mooi, R., Neuhaus, B., Ng, P. K., Nielsen, C., Norenburg, J., Opresko, D. M., Osawa, M., Paulay, G., Perrin, W., Pilger, J. F., Poore, G. C., Pugh, P., Read, G. B., Reimer, J. D., Rius, M., Rocha, R. M., Saiz-Salinas, J. I., Scarabino, V., Schierwater, B., Schmidt-Rhaesa, A., Schnabel, K. E., Schotte, M., Schuchert, P., Schwabe, E., Segers, H., Self-Sullivan, C., Shenkar, N., Siegel, V., Sterrer, W., Stöhr, S., Swalla, B., Tasker, M. L., Thuesen, E. V., Timm, T., Todaro, M. A., Turon, X., Tyler, S., Uetz, P., van der Land, J., Vanhoorne, B., van Ofwegen, L. P., van Soest, R. W. M., Vanaverbeke, J., Walker-Smith, G., Walter, T. C., Warren, A., Williams, G. C., Wilson, S. P., and Costello, M. J. (2012). The magnitude of global marine species diversity. Current Biology 22, 2189–2202.
The magnitude of global marine species diversity.CrossRef | 1:CAS:528:DC%2BC38Xhs12gtb7K&md5=1dc243389107e379b7ac46b6d2cd8621CAS | 23159596PubMed | open url image1

Bartolomaeus, T., and von Döhren, J. (2010). Comparative morphology and evolution of the nephridia in Nemertea. Journal of Natural History 44, 2255–2286.
Comparative morphology and evolution of the nephridia in Nemertea.CrossRef | open url image1

Bell, P. J., and Hickman, J. L. (1985). Observations on Carcinonemertes (Nemertea: Carcinonemertidae) associated with the smooth pebble crab, Philyra laevis. Papers and Proceedings of the Royal Society of Tasmania 119, 65–68. open url image1

Berg, G. (1985). Annulonemertes gen. nov., a new segmented hoplonemertean. In ‘The Origins and Relationships of Lower Invertebrates’. (Eds S. Conway Morris, J. D. George, R. Gibson and H. Platt.) pp. 200–209. (Clarendon Press, UK.)

Boyer, S. L., Baker, J. M., and Giribet, G. (2007). Deep genetic divergences in Aoraki denticulata (Arachnida, Opiliones, Cyphophthalmi): a widespread ‘mite harvestman’ defies DNA taxonomy. Molecular Ecology 16, 4999–5016.
Deep genetic divergences in Aoraki denticulata (Arachnida, Opiliones, Cyphophthalmi): a widespread ‘mite harvestman’ defies DNA taxonomy.CrossRef | 17944852PubMed | open url image1

Bürger, O. (1895). Die Nemertinen des Golfes von Neapel und der angrenzenden Meeres-Abschnitte. Fauna und Flora des Golfes von Neapel 22, 1–743. open url image1

Cantell, C.-E. (1969). Morphology, development, and biology of the pilidium larvae (Nemertini) from the Swedish west coast. Zoologiska Bidrag från Uppsala 38, 61–111. open url image1

Caplins, S., Penna-Diaz, M. A., Godoy, E., Valdivia, N., Turbeville, J. M., and Thiel, M. (2012). Activity patterns and predatory behaviour of an intertidal nemertean from rocky shores: Prosorhochmus nelsoni (Hoplonemertea) from the Southeast Pacific. Marine Biology 159, 1363–1374.
Activity patterns and predatory behaviour of an intertidal nemertean from rocky shores: Prosorhochmus nelsoni (Hoplonemertea) from the Southeast Pacific.CrossRef | open url image1

Castresana, J. (2000). Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Molecular Biology and Evolution 17, 540–552.
Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis.CrossRef | 1:CAS:528:DC%2BD3cXisVSgt7g%3D&md5=b9e72f4f43e92e5aaa6c2696c6b069dbCAS | 10742046PubMed | open url image1

Chen, H., Strand, M., Norenburg, J. L., Sun, S., Kajihara, H., Chernyshev, A. V., Maslakova, S. A., and Sundberg, P. (2010). Statistical parsimony networks and species assemblages in cephalothricid nemerteans (Nemertea). PLoS ONE 5, e12885.
Statistical parsimony networks and species assemblages in cephalothricid nemerteans (Nemertea).CrossRef | 20877627PubMed | open url image1

Chernyshev, A. V. (2003). Classification system for the higher taxa of enoplan nemerteans (Nemertea: Enopla). Russian Journal of Marine Biology 29, S57–S65.
Classification system for the higher taxa of enoplan nemerteans (Nemertea: Enopla).CrossRef | open url image1

Chernyshev, A. V. (2005). System of families of enoplan nemerteans of the order Eumonostilifera (Nemertea: Enopla). Russian Journal of Marine Biology 31, S27–S33.
System of families of enoplan nemerteans of the order Eumonostilifera (Nemertea: Enopla).CrossRef | open url image1

Chernyshev, A. V., Magarlamov, T. Y., and Turbeville, J. M. (2013). Morphology of the proboscis of Hubrechtella juliae (Nemertea, Pilidiophora): implications for pilidiophoran monophyly. Journal of Morphology 274, 1397–1414.
Morphology of the proboscis of Hubrechtella juliae (Nemertea, Pilidiophora): implications for pilidiophoran monophyly.CrossRef | 24105877PubMed | open url image1

Colgan, D. J., McLauchlan, A., Wilson, G. D. F., Livingston, S. P., Edgecombe, G. D., Macaranas, J., Cassis, G., and Gray, M. R. (1998). Histone H3 and U2 snRNA DNA sequences and arthropod molecular evolution. Australian Journal of Zoology 46, 419–437.
Histone H3 and U2 snRNA DNA sequences and arthropod molecular evolution.CrossRef | open url image1

Crandall, F. B. (2001). A cladistics view of the Monostilifera (Hoplonemertea) with interwoven rhynchocoel musculature: a preliminary assessment. Hydrobiologia 456, 87–110.
A cladistics view of the Monostilifera (Hoplonemertea) with interwoven rhynchocoel musculature: a preliminary assessment.CrossRef | open url image1

DeSalle, R., Egan, M. G., and Siddall, M. (2005). The unholy trinity: taxonomy, species delimitation and DNA barcoding. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 360, 1905–1916.
The unholy trinity: taxonomy, species delimitation and DNA barcoding.CrossRef | 1:CAS:528:DC%2BD2MXhtlSjsrnE&md5=1153e24be084fafe008a91ce469d29f0CAS | 16214748PubMed | open url image1

Dunn, C. W., Hejnol, A., Matus, D. Q., Pang, K., Browne, W. E., Smith, S. A., Seaver, E. C., Rouse, G. W., Obst, M., Edgecombe, G. D., Sørensen, M. V., Haddock, S. H. D., Schmidt-Rhaesa, A., Okusu, A., Kristensen, R. M., Wheeler, W. C., Martindale, M. Q., and Giribet, G. (2008). Broad taxon sampling improves resolution of the Animal Tree of Life. Nature 452, 745–749.
Broad taxon sampling improves resolution of the Animal Tree of Life.CrossRef | 1:CAS:528:DC%2BD1cXksFSju7k%3D&md5=16e210f3588dd00d1cbee1b9b9d1bb83CAS | 18322464PubMed | open url image1

Ebach, M. C., and Holdredge, C. (2005). DNA barcoding is no substitute for taxonomy. Nature 434, 697.
DNA barcoding is no substitute for taxonomy.CrossRef | 1:CAS:528:DC%2BD2MXivFCgt74%3D&md5=e81b8eb53b2d024405fc38166b6ba34aCAS | 15815602PubMed | open url image1

Edgecombe, G. D., and Giribet, G. (2006). A century later – a total evidence re-evaluation of the phylogeny of scutigeromorph centipedes (Myriapoda: Chilopoda). Invertebrate Systematics 20, 503–525.
A century later – a total evidence re-evaluation of the phylogeny of scutigeromorph centipedes (Myriapoda: Chilopoda).CrossRef | open url image1

Fernández-Álvarez, F. Á., and Machordom, A. (2013). DNA barcoding reveals a cryptic nemertean invasion in Atlantic and Mediterranean waters. Helgoland Marine Research 67, 599–605.
DNA barcoding reveals a cryptic nemertean invasion in Atlantic and Mediterranean waters.CrossRef | open url image1

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=41891c10f444b637826cbf6001a4954cCAS | 7881515PubMed | open url image1

Gibson, R. (1967). Occurrence of the entocommensal rhynchocoelan, Malacobdella grossa, in the oval piddock, Zirfaea crispata, on the Yorkshire coast. Journal of the Marine Biological Association of the United Kingdom 47, 301–317.
Occurrence of the entocommensal rhynchocoelan, Malacobdella grossa, in the oval piddock, Zirfaea crispata, on the Yorkshire coast.CrossRef | open url image1

Gibson, R. (1985). The need for a standard approach to taxonomic descriptions of Nemertea. American Zoologist 25, 5–14. open url image1

Gibson, R. (1990). The macrobenthic nemertean fauna of Hong Kong. In ‘Proceedings of the Second International Marine Biological Workshop: the Marine Flora and Fauna of Hong Kong and Southern China 1’. (Ed. B. S. Morton.) (University Press: Hong Kong.)

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 | open url image1

Giribet, G., and Edgecombe, G. D. (2013). Stable phylogenetic patterns in scutigeromorph centipedes (Myriapoda: Chilopoda: Scutigeromorpha): dating the diversification of an ancient lineage of terrestrial arthropods. Invertebrate Systematics 27, 485–501.
Stable phylogenetic patterns in scutigeromorph centipedes (Myriapoda: Chilopoda: Scutigeromorpha): dating the diversification of an ancient lineage of terrestrial arthropods.CrossRef | open url image1

Giribet, G., Carranza, S., Baguñá, 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.
First molecular evidence for the existence of a Tardigrada + Arthropoda clade.CrossRef | 1:CAS:528:DyaK28XhtVylur8%3D&md5=12d70fb007b406aad2b3d1737a48a9adCAS | 8583909PubMed | open url image1

Giribet, G., Dunn, C. W., Edgecombe, G. D., Hejnol, A., Martindale, M. Q., and Rouse, G. W. (2009). Assembling the spiralian tree of life. In ‘Animal Evolution: Genomes, Fossils and Trees’. (Eds M. J. Telford and D. T. J. Littlewood.) pp. 52–64. (Oxford University Press: Oxford, UK.)

Giribet, G., Vogt, L., Pérez González, A., Sharma, P., and Kury, A. B. (2010). A multilocus approach to harvestman (Arachnida: Opiliones) phylogeny with emphasis on biogeography and the systematics of Laniatores. Cladistics 26, 408–437. open url image1

Goloboff, P. A., Farris, J. S., and Nixon, K. C. (2008). TNT, a free program for phylogenetic analysis. Cladistics 24, 774–786.
TNT, a free program for phylogenetic analysis.CrossRef | open url image1

Guzik, M. T., Austain, A. D., Cooper, S. J., Harvey, M. S., Humphreys, W. F., Bradford, T., Eberhard, S. M., King, R. A., Leys, R., Muirhead, K. A., and Tomlinson, M. (2011). Is the Australian fauna uniquely diverse? Invertebrate Systematics 24, 407–418.
Is the Australian fauna uniquely diverse?CrossRef | open url image1

Härlin, M. S., and Sundberg, P. (1995). Cladistic analysis of the eureptantic nemerteans (Nemertea: Hoplonemertea). Invertebrate Taxonomy 9, 1211–1229.
Cladistic analysis of the eureptantic nemerteans (Nemertea: Hoplonemertea).CrossRef | open url image1

Hebert, P. D. N., Cywinska, A., Ball, S. L., and deWaard, J. R. (2003a). Biological identifications through DNA barcodes. Proceedings of the Royal Society of London. Series B, Biological Sciences 270, 313–321.
Biological identifications through DNA barcodes.CrossRef | 1:CAS:528:DC%2BD3sXktVWiu7g%3D&md5=6937f93aeb832a9058d1fe8b082d2953CAS | open url image1

Hebert, P. D. N., Ratnasingham, S., and deWaard, J. R. (2003b). Barcoding animal life: cytochrome c oxidase subunit 1 divergences among closely related species . Proceedings of the Royal Society of London B: Biological Sciences 270, S96–S99.
| 1:CAS:528:DC%2BD3sXns1Smsbo%3D&md5=cc30dfe67bf89e0a3f52f8dc648ad826CAS | open url image1

Hejnol, A., Obst, M., Stamatakis, A., Ott, M., Rouse, G. W., Edgecombe, G. D., Martinez, P., Baguña, J., Bailly, X., Jondelius, U., Wiens, M., Müller, W. E. G., Seaver, E., Wheeler, W. C., Martindale, M. Q., Giribet, G., and Dunn, C. W. (2009). Assessing the root of bilaterian animals with scalable phylogenomic methods. Proceedings of the Royal Society of London. Series B, Biological Sciences 276, 4261–4270.
Assessing the root of bilaterian animals with scalable phylogenomic methods.CrossRef | open url image1

Humphreys, W. F. (2008). Rising from Down Under: developments in subterranean biodiversity in Australia from a groundwater fauna perspective. Invertebrate Systematics 22, 85–101.
Rising from Down Under: developments in subterranean biodiversity in Australia from a groundwater fauna perspective.CrossRef | open url image1

Junoy, J., Andrade, S. C. S., and Giribet, G. (2011). Phylogenetic placement of a new hoplonemertean species commensal of ascidians. Invertebrate Systematics 24, 616–629.
Phylogenetic placement of a new hoplonemertean species commensal of ascidians.CrossRef | open url image1

Kajihara, H., Gibson, R., and Mawatari, S. F. (2000). Redescription and taxonomic reassessment of Nemertellina minuta Friedrich, 1935 sensu Yamoaka, 1940 (Nemertea, Hoplonemertea, Monostilifera). Zoological Science 17, 265–276.
Redescription and taxonomic reassessment of Nemertellina minuta Friedrich, 1935 sensu Yamoaka, 1940 (Nemertea, Hoplonemertea, Monostilifera).CrossRef | open url image1

Kajihara, H., Chernyshev, A. V., Sun, S.-C., Sundberg, P., and Crandall, F. B. (2008). Checklist of nemertean genera and species published between 1995 and 2007. Species Diversity 13, 245–274. open url image1

Kajihara, H., Yamasaki, H., and Andrade, S. C. S. (2011). Carinoma hamanako sp. nov. (Nemertea: Palaeonemertea), the first representative of the genus from the Northwest Pacific. Species Diversity 16, 149–165. open url image1

Katoh, K., and Standley, D. M. (2013). MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Molecular Biology and Evolution 30, 772–780.
MAFFT multiple sequence alignment software version 7: improvements in performance and usability.CrossRef | 1:CAS:528:DC%2BC3sXksFWisLc%3D&md5=14a6e5bc04e61af99a92f9a397a54c77CAS | 23329690PubMed | open url image1

Kocot, K. M., Cannon, J. T., Todt, C., Citarella, M. R., Kohn, A. B., Meyer, A., Santos, S. R., Schander, C., Moroz, L. L., Lieb, B., and Halanych, K. M. (2011). Phylogenomics reveals deep molluscan relationships. Nature 477, 452–456.
Phylogenomics reveals deep molluscan relationships.CrossRef | 1:CAS:528:DC%2BC3MXhtFers7fE&md5=ed483a49693e0582006f0b202c9109c0CAS | 21892190PubMed | open url image1

Kvist, S. (2013). Barcoding in the dark?: a critical view of the sufficiency of zoological DNA barcoding databases and a plea for broader integration of taxonomic knowledge. Molecular Phylogenetics and Evolution 69, 39–45.
Barcoding in the dark?: a critical view of the sufficiency of zoological DNA barcoding databases and a plea for broader integration of taxonomic knowledge.CrossRef | 1:CAS:528:DC%2BC3sXhtFShtbbM&md5=13f6be9fcf90aca3ec4f9f03be802d96CAS | 23721749PubMed | open url image1

Kvist, S., Oceguera-Figueroa, A., Siddall, M. E., and Erséus, C. (2010). Barcoding, types and the Hirudo files: using information content to critically evaluate the identity of DNA barcodes. Mitochondrial DNA 21, 198–205.
Barcoding, types and the Hirudo files: using information content to critically evaluate the identity of DNA barcodes.CrossRef | 1:CAS:528:DC%2BC3cXhsFyksr7J&md5=02be347995587d8cbda46812dd706c0cCAS | 21171864PubMed | open url image1

Lanfear, R., Calcott, B., Ho, S. Y. W., and Guindon, S. (2012). PartitionFinder: combined selection of partitioning schemes and substitution models for phylogenetic analyses. Molecular Biology and Evolution 29, 1695–1701.
PartitionFinder: combined selection of partitioning schemes and substitution models for phylogenetic analyses.CrossRef | 1:CAS:528:DC%2BC38Xnt1ehsbg%3D&md5=6252e96674fb862520ea0b491079d71fCAS | 22319168PubMed | open url image1

Lindgren, A. R., and Daly, M. (2007). The impact of length-variable data and alignment criterion on the phylogeny of Decapodiformes (Mollusca: Cephalopoda). Cladistics 23, 464–476.
The impact of length-variable data and alignment criterion on the phylogeny of Decapodiformes (Mollusca: Cephalopoda).CrossRef | open url image1

Lipscomb, D., Platnick, N., and Wheeler, Q. (2003). The intellectual content of taxonomy: a comment on DNA taxonomy. Trends in Ecology & Evolution 18, 65–66.
The intellectual content of taxonomy: a comment on DNA taxonomy.CrossRef | open url image1

Maddison, W. P., and Maddison, D. R. (2010). Mesquite: a modular system for evolutionary analysis version 2.5. Available from http://mesquiteproject.org. [verified 4 June 2014]

Mahon, A. R., Thornhill, D. J., Norenburg, J. L., and Halanych, K. M. (2010). DNA uncovers Antarctic nemertean biodiversity and exposes a decades-old cold case of asymmetric inventory. Polar Biology 33, 193–202.
DNA uncovers Antarctic nemertean biodiversity and exposes a decades-old cold case of asymmetric inventory.CrossRef | open url image1

Maslakova, S. A. (2010). Development to metamorphosis of the nemertean pilidium larva. Frontiers in Zoology 7, 30.
Development to metamorphosis of the nemertean pilidium larva.CrossRef | 21126367PubMed | open url image1

Mateos, E., and Giribet, G. (2008). Exploring the molecular diversity of terrestrial nemerteans (Hoplonemertea, Monostilifera, Acteonemertidae) in a continental landmass. Zoologica Scripta 37, 235–243.
Exploring the molecular diversity of terrestrial nemerteans (Hoplonemertea, Monostilifera, Acteonemertidae) in a continental landmass.CrossRef | open url image1

McDermott, J. J., and Roe, P. (1985). Food, feeding behavior and feeding ecology of nemerteans. American Zoologist 25, 113–125. open url image1

McIntosh, W. C. (1873). ‘A Monograph of the British Annelids. Part 1. The Nemerteans.’ (Ray Society, London.)

Miller, M. A., Pfeiffer, W., and Schwartz, T. (2010). Creating the CIPRES Science Gateway for inference of large phylogenetic trees. In ‘Proceedings of the Gateway Computing Environments Workshop (GCE), New Orleans, LA’. pp. 1–8.

Moore, J., and Gibson, R. (1981). The Geonemertes problem (Nemertea). Journal of Zoology 194, 175–201.
The Geonemertes problem (Nemertea).CrossRef | open url image1

Moore, J., and Gibson, R. (1985). The evolution and comparative physiology of terrestrial and freshwater nemerteans. Biological Reviews of the Cambridge Philosophical Society 60, 257–312.
The evolution and comparative physiology of terrestrial and freshwater nemerteans.CrossRef | open url image1

Moore, J., and Gibson, R. (1988). Further studies on the evolution of land and freshwater nemerteans: generic relationships among the paramonostiliferous taxa. Journal of Zoology 216, 1–20.
Further studies on the evolution of land and freshwater nemerteans: generic relationships among the paramonostiliferous taxa.CrossRef | open url image1

Moore, J., Gibson, R., and Jones, H. D. (2001). Terrestrial nemerteans thirty years on. Hydrobiologia 456, 1–6.
Terrestrial nemerteans thirty years on.CrossRef | open url image1

Moritz, C., and Cicero, C. (2004). DNA barcoding: promise and pitfalls. PLoS Biology 2, e354.
DNA barcoding: promise and pitfalls.CrossRef | 15486587PubMed | open url image1

Norenburg, J. L. (1993). Riserius pugetensis gen. n., sp. n. (Nemertina: Anopla), a new mesopsammic species, and comments onphylogenetics of some anoplan characters. Hydrobiologia 266, 203–218.
Riserius pugetensis gen. n., sp. n. (Nemertina: Anopla), a new mesopsammic species, and comments onphylogenetics of some anoplan characters.CrossRef | open url image1

Palumbi, S., Martin, A., Romano, S., McMillan, W. O., Stice, L., and Grabowski, G. (1991). ‘The Simple Fools Guide to PCR, ver. 2.0.’ (Department of Zoology and Kewalo Marine Laboratory, University of Hawaii: Honolulu, HI.)

Pennak, R. W. (1963). Ecological affinities and origins of free-living acelomate freshwater invertebrates. In ‘The Lower Metazoa’. (Eds E. C. Dougherty, Z. N. Brown, E. D. Hanson and W. D. Hartman.) pp. 435–451. (University of California Press: Berkeley, CA.)

Pineau, P., Henry, M., Suspène, R., Marchio, A. S., Dettai, A., Debruyne, R., Petit, T., Lécu, A., Moisson, P., Dejean, A., Wain-Hobson, S., and Vartanian, J. P. (2005). A universal primer set for PCR amplification of nuclear histone H4 genes from all animal species. Molecular Biology and Evolution 22, 582–588.
A universal primer set for PCR amplification of nuclear histone H4 genes from all animal species.CrossRef | 1:CAS:528:DC%2BD2MXhs1Kru7w%3D&md5=468b3c3fe65ee8862abb24e073be5c51CAS | 15601889PubMed | open url image1

Puillandre, N., Lambert, A., Brouillet, S., and Achaz, G. (2012). ABGD, automatic barcode gap discovery for primary species delimitation. Molecular Ecology 21, 1864–1877.
ABGD, automatic barcode gap discovery for primary species delimitation.CrossRef | 1:STN:280:DC%2BC38zlsFeltQ%3D%3D&md5=6a988792b76cb4958ac97b6ceacba539CAS | 21883587PubMed | open url image1

Ratnasingham, S., and Hebert, P. D. N. (2007). BOLD: the Barcode of Life Data System. Available at: http://www.barcodinglife.org. Molecular Ecology Resources 7, 355–364. [Verified 4 June 2014]

Riser, N. W. (1994). The morphology and generic relationships of some fissiparous heteronemertines. Proceedings of the Biological Society of Washington 107, 548–556. open url image1

Rogers, A. D., Thorpe, J. P., and Gibson, R. (1995). Genetic evidence for the occurrence of a cryptic species with the littoral nemerteans Lineus ruber and L. viridis (Nemertea: Anopla). Marine Biology 1995, 305–316. open url image1

Rubinoff, D., Cameron, S., and Will, K. (2006). A genomic perspective on the shortcomings of mitochondrial DNA for “barcoding” identification. The Journal of Heredity 97, 581–594.
A genomic perspective on the shortcomings of mitochondrial DNA for “barcoding” identification.CrossRef | 1:CAS:528:DC%2BD28XhtlCru7jL&md5=7af0f81d3d7199d0dc7ecb6ce29eb84aCAS | 17135463PubMed | open url image1

Schander, C., and Willassen, E. (2005). What can biological barcoding do for marine biology? Marine Biology Research 1, 79–83.
What can biological barcoding do for marine biology?CrossRef | open url image1

Schultze, M. S. (1851). ‘Beiträge zur Naturgeschichte den Turbellarien.’ (C.A. Koch: Greifswald, Germany.)

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 | open url image1

Schwartz, M. L., and Norenburg, J. L. (2005). Three new species of Micrura (Nemertea: Heteronemertea) and a new type of heteronemertean larva from the Caribbean Sea. Caribbean Journal of Science 41, 528–543. open url image1

Schwendinger, P. J., and Giribet, G. (2005). The systematics of the southeast Asian genus Fangensis Rambla (Opiliones: Cyphophthalmi: Stylocellidae). Invertebrate Systematics 19, 297–323.
The systematics of the southeast Asian genus Fangensis Rambla (Opiliones: Cyphophthalmi: Stylocellidae).CrossRef | open url image1

Shimodaira, H. (2002). An approximately unbiased test of phylogenetic tree selection. Systematic Biology 51, 492–508.
An approximately unbiased test of phylogenetic tree selection.CrossRef | 12079646PubMed | open url image1

Shimodaira, H., and Hasegawa, M. (1999). Multiple comparisons of log-likelihoods with applications to phylogenetic inference. Molecular Biology and Evolution 16, 1114–1116.
Multiple comparisons of log-likelihoods with applications to phylogenetic inference.CrossRef | 1:CAS:528:DyaK1MXltVyksrg%3D&md5=e26146dec84bc74dd41bbd568f11c0c2CAS | open url image1

Shimodaira, H., and Hasegawa, M. (2001). CONSEL: for assessing the confidence of phylogenetic tree selection. Bioinformatics 17, 1246–1247.
CONSEL: for assessing the confidence of phylogenetic tree selection.CrossRef | 1:STN:280:DC%2BD38%2FgtFOlsw%3D%3D&md5=2e6b69bf2a602aaab2c623f68e7e43d2CAS | 11751242PubMed | open url image1

Smith, M. A., Fisher, B. L., and Hebert, P. D. N. (2005). DNA barcoding for effective biodiversity assessment of a hyperdiverse arthropod group: the ants of Madagascar. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 360, 1825–1834.
DNA barcoding for effective biodiversity assessment of a hyperdiverse arthropod group: the ants of Madagascar.CrossRef | 1:CAS:528:DC%2BD2MXhtlSjsrjP&md5=9c4321a7c6164a446d768dffdf8fcabcCAS | 16214741PubMed | open url image1

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 | 1:CAS:528:DC%2BD28XhtFKlsbfI&md5=b0df768ad6679df0c2d42f77d14048ddCAS | 16928733PubMed | open url image1

Stothard, P. (2000). The sequence manipulation suite: JavaScript programs for analyzing and formatting protein and DNA sequences. BioTechniques 28, 1102–1104.
| 1:CAS:528:DC%2BD3cXktF2ks7w%3D&md5=7011f2908a4f3fa71b9d88865014c08bCAS | 10868275PubMed | open url image1

Strand, M., and Sundberg, P. (2005a). 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 | open url image1

Strand, M., and Sundberg, P. (2005b). Genus Tetrastemma Ehrenberg, 1831 (phylum Nemertea) – a natural group? Phylogenetic relationships inferred from partial 18SrRNA sequences. Molecular Phylogenetics and Evolution 37, 144–152.
Genus Tetrastemma Ehrenberg, 1831 (phylum Nemertea) – a natural group? Phylogenetic relationships inferred from partial 18SrRNA sequences.CrossRef | 1:CAS:528:DC%2BD2MXhtVart7vF&md5=45d58f74da8f282a92b74f27ff6053b5CAS | 16182152PubMed | open url image1

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 | open url image1

Strand, M., Hererra-Bachiller, A., Nygren, A., and Kånneby, T. (2013). A new nemertean species: what are the useful characters for ribbon worm descriptions? Journal of the Marine Biological Association of the United Kingdom , . open url image1

Sundberg, P. (1989a). Phylogeny and cladistic classification of the Paramonostiliferous family Plectonemertidae (phylum Nemertea). Cladistics 5, 87–100.
Phylogeny and cladistic classification of the Paramonostiliferous family Plectonemertidae (phylum Nemertea).CrossRef | open url image1

Sundberg, P. (1989b). Phylogeny and cladistics classification of terrestrial nemerteans: the genera Pantinonemertes Moore & Gibson and Geonemertes Semper. Zoological Journal of the Linnean Society 95, 363–372.
Phylogeny and cladistics classification of terrestrial nemerteans: the genera Pantinonemertes Moore & Gibson and Geonemertes Semper.CrossRef | open url image1

Sundberg, P., and Gibson, R. (2008). Global diversity of nemerteans (Nemertea) in freshwater. Hydrobiologia 595, 61–66.
Global diversity of nemerteans (Nemertea) in freshwater.CrossRef | open url image1

Sundberg, P., and Hylbom, R. (1994). Phylogeny of the nemertean subclass Palaeonemertea (Anopla, Nemertea). Cladistics 10, 347–402.
Phylogeny of the nemertean subclass Palaeonemertea (Anopla, Nemertea).CrossRef | open url image1

Sundberg, P., and Saur, M. (1998). Molecular phylogeny of some European heteronemertea (Nemertea) species and the monophyletic status of Riseriellus, Lineus, and Micrura. Molecular Phylogenetics and Evolution 10, 271–280.
Molecular phylogeny of some European heteronemertea (Nemertea) species and the monophyletic status of Riseriellus, Lineus, and Micrura.CrossRef | 1:CAS:528:DyaK1MXhtlKmtLY%3D&md5=b3c0403b675937767912ea21d0a3e442CAS | 10051380PubMed | open url image1

Sundberg, P., and Strand, M. (2007). Annulonemertes (phylum Nemertea): when segments do not count. Biology Letters 3, 570–573.
Annulonemertes (phylum Nemertea): when segments do not count.CrossRef | 17686756PubMed | open url image1

Sundberg, P., and Svensson, M. (1994). Homoplasy, character function, and nemertean systematics. Journal of Zoology 234, 253–263.
Homoplasy, character function, and nemertean systematics.CrossRef | open url image1

Sundberg, P., Turbeville, J. M., and Lindh, S. (2001). Phylogenetic relationships among higher nemertean (Nemertea) taxa inferred from 18S rRNA sequences. Molecular Phylogenetics and Evolution 20, 327–334.
Phylogenetic relationships among higher nemertean (Nemertea) taxa inferred from 18S rRNA sequences.CrossRef | 1:CAS:528:DC%2BD3MXmtleis7g%3D&md5=f5ade2889e4f4280e72c55453cdf838eCAS | 11527461PubMed | open url image1

Sundberg, P., Thuroczy Vodoti, E., and Strand, M. (2010). DNA barcoding should accompany taxonomy – the case of Cerebratulus spp. (Nemertea). Molecular Ecology Resources 10, 274–281.
DNA barcoding should accompany taxonomy – the case of Cerebratulus spp. (Nemertea).CrossRef | 1:CAS:528:DC%2BC3cXjvFCks7c%3D&md5=6bc331574461383b4ef513eb7b630f10CAS | 21565022PubMed | open url image1

Taboada, S., Junoy, J., Andrade, S. C. S., Giribet, G., Cristobo, J., and Avila, C. (2013). On the identity of two Antarctic brooding nemerteans: redescription of Antarctonemertes valida (Bürger, 1893) and description of a new species in the genus Antarctonemertes Friedrich, 1955 (Nemertea, Hoplonemertea). Polar Biology 36, 1415–1430.
On the identity of two Antarctic brooding nemerteans: redescription of Antarctonemertes valida (Bürger, 1893) and description of a new species in the genus Antarctonemertes Friedrich, 1955 (Nemertea, Hoplonemertea).CrossRef | 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=5ee5a71f721d24a7782516dc0ff5fcfcCAS | 21546353PubMed | open url image1

Tautz, D., Arctander, P., Minelli, A., Thomas, R. H., and Vogler, A. P. (2002). DNA points the way ahead in taxonomy. Nature 418, 479.
DNA points the way ahead in taxonomy.CrossRef | 1:CAS:528:DC%2BD38Xls12nt7c%3D&md5=0684c01eebaee80900de30c8214acc46CAS | 12152050PubMed | open url image1

Tautz, D., Arctander, P., Minelli, A., Thomas, R. H., and Vogler, A. P. (2003). A plea for DNA taxonomy. Trends in Ecology & Evolution 18, 70–74.
A plea for DNA taxonomy.CrossRef | open url image1

Thollesson, M., and Norenburg, J. L. (2003). Ribbon worm relationships: a phylogeny of the phylum Nemertea. Proceedings of the Royal Society of London. Series B, Biological Sciences 270, 407–415.
Ribbon worm relationships: a phylogeny of the phylum Nemertea.CrossRef | 1:CAS:528:DC%2BD3sXktVWiu70%3D&md5=545ab5feea4ecc5adeaeb9817754108cCAS | open url image1

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=86df74a7ce3b490b4da8ad4ca25d6b71CAS | 11975347PubMed | open url image1

Will, K., and Rubinoff, D. (2004). Myth of the molecule: DNA barcodes for species cannot replace morphology for identification and classification. Cladistics 20, 47–55.
Myth of the molecule: DNA barcodes for species cannot replace morphology for identification and classification.CrossRef | open url image1

Wilson, G. D. F. (2008). Gondwanan groundwater: subterranean connections of Australian phreatoicidean isopods (Crustacea) to India and New Zealand. Invertebrate Systematics 22, 301–310.
Gondwanan groundwater: subterranean connections of Australian phreatoicidean isopods (Crustacea) to India and New Zealand.CrossRef | open url image1

Zhang, Z.-Q. (2011). Animal biodiversity: an introduction to higher-level classification and taxonomic richness. Zootaxa 3148, 7–12. open url image1


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