Phylogeny of Nemertea with special interest in the placement of diversity from Far East Russia and northeast Asia


Recent investigations, based mostly on molecular data, have unraveled the evolutionary history of several common ribbon worm (phylum Nemertea) species and solidified the taxonomic status of many higher taxa within the group. However, a large proportion of enigmatic species have yet to be placed in a phylogenetic framework. We investigated the phylogenetic positions of 26 novel and/or perplexing nemertean species from the Sea of Okhotsk, the Sea of Japan, the Kuril–Kamchatka Trench, and Vietnam (including the first record of a reptant nemertean from the Far East seas of Russia). We conducted both maximum likelihood and parsimony analyses, utilizing four molecular loci—mitochondrial COI and 16S rRNA, as well as nuclear 18S rRNA and 28S rRNA—finding that the current classification for most of these species is corroborated by their phylogenetic placement. We then discuss the evolution of some unique morphological traits possessed by some of these species, using the molecular phylogeny as a backbone for our general conclusions.

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

  2. Andrade, S. C., H. Montenegro, M. Strand, M. Schwartz, H. Kajihara, J. L. Norenburg, J. M. Turbeville, P. Sundberg & G. Giribet, 2014. A transcriptomic approach to ribbon worm systematics (Nemertea): resolving the Pilidiophora problem. Molecular Biology and Evolution 31: 3206–3215.

  3. Blaxter, M., 2003. Counting angels with DNA. Nature 421: 122–124.

  4. Chernyshev, A. V., 2000. Nemertean larvae of the Ototyphlonemertidae family in the plankton of Peter the Great Bay, Sea of Japan. Russian Journal of Marine Biology 26: 48–50.

  5. Chernyshev, A. V., 2002. Description of a new species of the genus Poseidonemertes (Nemertea; Monostilifera) with establishment of the family Poseidonemertidae. Zoologicheskii Zhurnal 81: 909–916. [In Russian].

  6. Chernyshev, A. V., 2003. New species of the genus Hubrechtella (Nemertea, Anopla) from the Sea of Japan and validation of the family Hubrechtellidae. Russian Journal of Marine Biology 29: 333–336.

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

  8. Chernyshev, A. V., 2010. Confocal laser scanning microscopy analysis of the phalloidin-labelled musculature in nemerteans. Journal of Natural History 44: 37–40.

  9. Chernyshev, A. V., 2011a. Comparative Morphology, Systematics and Phylogeny of the Nemerteans. Dalnauka, Vladivostok. [In Russian].

  10. Chernyshev, A. V., 2011b. Nemertean worms (Nemertea) of the Vietnamese coastal waters. In Lutaenko K. A. (ed) Proceedings of the Workshop Coastal Marine Biodiversity and Bioresources of Vietnam and Adjacent Areas of the South China Sea, Nha Trang, Vietnam, November 24–25, 2011 Vladivostok-Nha Trang: Dalnauka: 21–25.

  11. Chernyshev, A. V., 2013. Two new species of deep-sea nemerteans from the SoJaBio expedition in the Sea of Japan. Deep Sea research Part II: Topical Studies in Oceanography 86–87: 148–155.

  12. Chernyshev, A. V., 2014. Nemertean biodiversity in the Sea of Japan and adjacent areas. In Sun, S., et al. (eds), Marine Biodiversity and Ecosystem Dynamics of the North-Western Pacific Ocean. Publishing House of Science, Beijing: 119–135.

  13. Chernyshev, A. V., S. Abukawa & H. Kajihara, 2015. Sonnenemertes cantelli gen. et sp. nov. (Heteronemertea)—a new Oxypolella-like nemertean from the abyssal plain adjacent to the Kuril–Kamchatka Trench. Deep Sea research Part II: Topical Studies in Oceanography 111: 119–127.

  14. Crandall, F. B., 1993. Major characters and enoplan systematics. Hydrobiologia 266: 115–140.

  15. Crandall, F. B., 2001. A cladistic view of the Monostilifera (Hoplonemertea) with interwoven rhynchocoel musculature: a preliminary assessment. Hydrobiologia 456: 87–110.

  16. Crandall, F. B., J. L. Norenburg, A. V. Chernyshev, S. A. Maslakova, M. L. Schwartz & H. Kajihara, 2002. Checklist of the nemertean fauna of Japan and northeastern Asia. Smithsonian Institution, Washington D.C: 1–44. Available from

  17. Gibson, R., 1972. Nemerteans. Hutchinson, London.

  18. Gibson, R., 1988. Evolutionary relationships between mono- and polystiliferous hoplonemerteans: Nipponnemertes (Cratenemertidae), a “missing link” genus? Hydrobiologia 156: 61–74.

  19. 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: 271–562.

  20. Gibson, R. & P. Sundberg, 1992. Three new nemerteans from Hong Kong. In Morton, B. (ed.), The Marine Flora and Fauna of Hong Kong and Southern China III, Vol. 1. University Press, Hong Kong: 97–129.

  21. Gibson, R. & P. Sundberg, 1999. Six new species of palaeonemerteans (Nemertea) from Hong Kong. Zoological Journal of Linnean Society 125: 151–196.

  22. Goloboff, P. A., J. S. Farris & K. C. Nixon, 2008. TNT, a free program for phylogenetic analysis. Cladistics 24: 774–786.

  23. Hidaka, K., 1966. Japan Sea. In Fairbridge, R. W. (ed.), Encyclopedia of Oceanography. Reinhold Publisher, New York: 417–424.

  24. Kajihara, H., 2006. Four palaeonemerteans (Nemertea: Anopla) from a tidal flat in middle Honshu, Japan. Zootaxa 1163: 1–47.

  25. Kajihara, H., A. V. Chernyshev, S. C. Sun, P. Sundberg & F. B. Crandall, 2008. Checklist of nemertean genera and species published between 1995 and 2007. Species Diversity 13: 245–274.

  26. Kajihara, H., M. Olympia, N. Kobayashi, T. Katoh, H.-X. Chen, M. Strand & P. Sundberg, 2011. Systematics and phylogeny of the hoplonemertean genus Diplomma (Nemertea) based on molecular and morphological evidence. Zoological Journal of the Linnean Society 161: 695–722.

  27. Katoh, K. & D. M. Standley, 2013. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Molecular Biology and Evolution 30: 772–780.

  28. Kitamura, A., O. Takano, H. Takata & H. Omote, 2001. Late Pliocene-early Pleistocene paleogeographic evolution of the Sea of Japan. Paleogeography, Paleoclimatology, Paleoecology 172: 81–98.

  29. Kojima, S., 2002. Deep-sea chemoautosynthesis-based communities in the Northwestern Pacific. Journal of Oceanography 58: 343–363.

  30. Korotkevich, V. S., 1971. On the ecology and systematics of the nemerteans of the Possjet Bay of the Sea of Japan. Issledovaniya Fauny Morei 8: 109–122. (In Russian).

  31. Kvist, S., C. E. Laumer, J. Junoy & G. Giribet, 2014. New insights into the phylogeny, systematics and DNA barcoding of Nemertea. Invertebrate Systematics 28: 287–308.

  32. 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.

  33. Leasi, F. & J. L. Norenburg, 2014. The necessity of DNA taxonomy to reveal cryptic diversity and spatial distribution of meiofauna, with a focus on Nemertea. PLoS one 9: e104385.

  34. Maddison, W. P. & D. R. Maddison, 2010. Mesquite: a modular system for evolutionary analysis version 2.5. Available from

  35. Mahon, A. R., D. J. Thornhill, J. L. Norenburg & K. M. Halanych, 2010. DNA uncovers Antarctic nemertean biodiversity and exposes a decades-old cold case of asymmetric inventory. Polar Biology 33: 193–202.

  36. May, R. M., 1988. How many species are there on earth? Science 241: 1441–1449.

  37. Miller, M. A., W. Pfeiffer & T. Schwartz, 2010. Creating the CIPRES Science Gateway for inference of large phylogenetic trees. Proceedings of the Gateway Computing Environments Workshop (GCE), New Orleans, LA: 1–8.

  38. Moore, J. & R. Gibson, 1981. The Geonemertes problem (Nemertea). Journal of Zoology (London) 194: 175–201.

  39. Olson, D. M. E. & E. D. Dinerstein, 1998. The global 200: a representation approach to conserving the Earth’s most biologically valuable ecoregions. Conservation Biology 12: 502–515.

  40. Preller, R. H. & P. J. Hogan, 1998. Oceanography of the Sea of Okhotsk and the Japan/East Sea. In Brink, K. H. & A. R. Robinson (eds), the Sea. Wiley, New York: 429–481.

  41. Ritger, R. K. & J. L. Norenburg, 2006. Tubulanus riceae new species (Nemertea: Anopla: Palaeonemertea: Tubulanidae), from South Florida, Belize and Panama. Journal of Natural History 40: 931–942.

  42. Ryu, E., S. Yi & S.-J. Lee, 2005. Late Pleistocene-Holocene paleoenvironmental changes inferred from the diatom record of the Ulleung basin, East Sea (Sea of Japan). Marine Micropaleontology 55: 157–182.

  43. Sahling, H., S. V. Galkin, A. Salyuk, J. Greinert, H. Foerstel, D. Piepenburg & E. Suess, 2003. Depth-related structure and ecological significance of cold-seep communities—a case study from the Sea of Okhotsk. Deep Sea Research Part I: Oceanographic Research Papers 50: 1391–1409.

  44. Schwartz, M. L., 2009. Untying a Gordian knot of worms: systematics and taxonomy of the Pilidiophora (phylum Nemertea). Ph.D. thesis. Washington DC: George Washington University.

  45. Schwartz, M. L. & J. L. Norenburg, 2001. Can we infer heteronemertean phylogeny from available morphological data? Hydrobiologia 456: 165–174.

  46. Stamatakis, A., 2006. RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22: 2688–2690.

  47. Strand, M. & P. Sundberg, 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 86: 201–212.

  48. Strand, M. & P. Sundberg, 2005b. Genus Tetrastemma Ehrenberg, 1831 (phylum Nemertea)—a natural group? Phylogenetic relationships inferred from partial 18S rRNA sequences. Molecular Phylogenetics and Evolution 37: 144–152.

  49. Strand, M., A. Herrera-Bachiller, A. Nygren & T. Kånneby, 2014. A new nemertean species: what are useful characters for ribbon worm descriptions? Journal of the Marine Biological Association of the UK 94: 317–330.

  50. Sundberg, P., 1991. A proposal for renaming higher taxonomic categories in the phylum Nemertea. Journal of Natural History 25: 45–48.

  51. Sundberg, P., 1993. Phylogeny, natural groups and nemertean classification. Hydrobiologia 266: 103–113.

  52. Sundberg, P., R. Gibson & U. Olsson, 2003. Phylogenetic analysis of a group of palaeonemerteans (Nemertea) including two new species from Queensland and the Great Barrier Reef, Australia. Zoologica Scripta 32: 279–296.

  53. Sundberg, P. & R. Hylbom, 1994. Phylogeny of the nemertean subclass Palaeonemertea (Anopla, Nemertea). Cladistics, 10: 347–402.

  54. Sundberg, P. & M. Strand, 2010. Nemertean taxonomy—time to change lane? Journal of Zoological Systematics and Evolutionary Research 48: 283–284.

  55. Sundberg, P., E. Thuroczy Vodoti & M. Strand, 2010. DNA barcoding should accompany taxonomy—the case of Cerebratulus spp (Nemertea). Molecular Ecology Resources 10: 274–281.

  56. Sundberg, P., J. M. Turbeville & S. Lindh, 2001. Phylogenetic relationships among higher nemertean (Nemertea) taxa inferred from 18S rDNA sequences. Molecular Phylogenetics and Evolution 20: 327–334.

  57. Thollesson, M. & J. L. Norenburg, 2003. Ribbon worm relationships: a phylogeny of the phylum Nemertea. Proceedings of the Royal Society of London B: Biological Sciences 270: 407–415.

  58. Turbeville, J. M., 2002. Progress in nemertean biology: development and phylogeny. Integrative and Comparative Biology 42: 692–703.

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This study was supported in part by a Russian Foundation for Basic Research grants (14-04-01067 and 15-04-01933) to A.V.C. It was also supported by funding from the Wenner-Gren Foundations, Helge Ax:son and Olle Engkvist Byggmästare’s Foundation to S.K., as well as by internal funds from the Museum of Comparative Zoology to G.G. We thank the Harvard FAS Center for Systems Biology for providing sequencing support and the Willi Hennig Society for making TNT freely available. Three anonymous reviewers provided comments and ideas that greatly improved earlier versions of the paper.

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Kvist, S., Chernyshev, A.V. & Giribet, G. Phylogeny of Nemertea with special interest in the placement of diversity from Far East Russia and northeast Asia. Hydrobiologia 760, 105–119 (2015).

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  • Nemertea
  • Phylogeny
  • Sea of Okhotsk
  • Sea of Japan
  • Vietnam
  • Kuril–Kamchatka Trench