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Systematics, phylogeny and biogeography
RESEARCH ARTICLE

A new nemertean with a branched proboscis, Gorgonorhynchus citrinus sp. nov. (Nemertea: Pilidiophora), with molecular systematics of the genus

Natsumi Hookabe https://orcid.org/0000-0002-3498-8614 A F , Cong-Mei Xu B , Aoi Tsuyuki https://orcid.org/0000-0002-6001-0679 C , Naoto Jimi https://orcid.org/0000-0001-8586-3320 D , Shi-Chun Sun B and Hiroshi Kajihara https://orcid.org/0000-0001-6510-9355 E
+ Author Affiliations
- Author Affiliations

A Misaki Marine Biological Station, The University of Tokyo, Miura, Kanagawa 238-0225, Japan.

B Institute of Evolution & Marine Biodiversity, Ocean University of China, Qingdao, 266003, PR China.

C Graduate School of Science, Hokkaido University, N10W8 Kita-ku, Sapporo, Hokkaido 060-0180, Japan.

D Bioscience Group, National Institute of Polar Research, Tachikawa 190-8518, Japan.

E Faculty of Science, Hokkaido University, N10W8 Kita-ku, Sapporo, Hokkaido 060-0180, Japan.

F Corresponding author. Email: sofeechan312@gmail.com

Invertebrate Systematics 35(3) 350-359 https://doi.org/10.1071/IS20057
Submitted: 23 July 2020  Accepted: 13 November 2020   Published: 24 March 2021

Abstract

Among ~1300 species of world nemerteans, seven species in five genera of lineid heteronemerteans have been known to possess a branched proboscis. In this paper, we describe the eighth branched-proboscis species: Gorgonorhynchus citrinus sp. nov. from Okinawa, Japan. We also report Gorgonorhynchus cf. repens Dakin & Fordham, 1931 with uniformly orange body, as a new member for the Japanese nemertean fauna. We infer the phylogenetic relationships between these forms and other members of Lineidae McIntosh, 1874 for which partial sequences of the mitochondrial 16S rRNA and cytochrome c oxidase subunit I, and the nuclear 18S rRNA, 28S rRNA, and histone H3 genes are available in public databases, along with newly sequenced data of another branched-proboscis heteronemertean, Polydendrorhynchus zhanjiangensis (Yin & Zheng, 1984) from China. In the resulting tree, Gorgonorhychus Dakin & Fordham, 1931 was sister group to non-branched-proboscis Dushia Corrêa, 1963, whereas P. zhanjiangensis was sister group to likewise non-branched-proboscis Cerebratulus lacteus (Leidy, 1851).

http://zoobank.org/urn:lsid:zoobank.org:pub:685992C5-F595-4C28-9178-256D945E595A

Keywords: DNA barcode, histology-free description, Pacific, ribbon worm, SCUBA, taxonomy.


References

Ament-Velásquez, S. L., Figuet, E., Ballenghien, M., Zattara, E. E., Norenburg, J. L., Fernández-Álvarez, F. A., Bierne, J., Bierne, N., and Galtier, N. (2016). Population genomics of sexual and asexual lineages in fissiparous ribbon worms (Lineus, Nemertea): hybridization, polyploidy and the Meselson effect. Molecular Ecology 25, 3356–3369.
Population genomics of sexual and asexual lineages in fissiparous ribbon worms (Lineus, Nemertea): hybridization, polyploidy and the Meselson effect.Crossref | GoogleScholarGoogle Scholar | 27286413PubMed |

Andrade, S. C. S., Strand, M., Schwartz, M. L., Chen, H.-X., Kajihara, H., von Döhren, J., Sun, S.-C., 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 | GoogleScholarGoogle Scholar |

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 | GoogleScholarGoogle Scholar | 10742046PubMed |

Cherneva, I. A., Chernyshev, A. V., Ekimova, I. A., Polyakova, N. E., Schepetov, D. M., Turanov, S. V., Neretina, T. V., Chaban, E. M., and Malakhov, V. V. (2019). Species identity and genetic structure of nemerteans of the “Lineus ruber–viridis” complex (Müller, 1774) from Arctic waters. Polar Biology 42, 497–506.
Species identity and genetic structure of nemerteans of the “Lineus ruber–viridis” complex (Müller, 1774) from Arctic waters.Crossref | GoogleScholarGoogle Scholar |

Chernyshev, A. V., Polyakova, N. E., Turanov, S. V., and Kajihara, H. (2018). Taxonomy and phylogeny of Lineus torquatus and allies (Nemertea, Lineidae) with descriptions of a new genus and a new cryptic species. Systematics and Biodiversity 16, 55–68.
Taxonomy and phylogeny of Lineus torquatus and allies (Nemertea, Lineidae) with descriptions of a new genus and a new cryptic species.Crossref | GoogleScholarGoogle Scholar |

Coe, W. R. (1943). Biology of the nemerteans of the Atlantic coast of North America. Transactions of the Connecticut Academy of Arts and Sciences 35, 129–328.

Coe, W. R. (1947). Nemerteans of the Hawaiian and Marshall Islands. Occasional Papers of the Bernice P. Bishop Museum 19, 101–106.

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 | GoogleScholarGoogle Scholar |

Dakin, W. J., and Fordham, M. G. C. (1931). A new and peculiar marine nemertean from the Australian coast. Nature 128, 796.
A new and peculiar marine nemertean from the Australian coast.Crossref | GoogleScholarGoogle Scholar |

Dakin, W. J., and Fordham, M. G. C. (1936). The anatomy and systematic position of Gorgonorhynchus repens, gen. n., sp. n.: a new genus of nemertines characterized by a multi-branched proboscis. Proceedings of the Zoological Society of London 50, 461–483.

Fernández-Álvarez, F. Á., and Anadón, N. (2012). Oligodendrorhynchus hesperides gen. et sp. n. (Heteronemertea) from the Bellingshausen Sea. Polish Polar Research 33, 81–98.
Oligodendrorhynchus hesperides gen. et sp. n. (Heteronemertea) from the Bellingshausen Sea.Crossref | GoogleScholarGoogle Scholar |

Gibson, R. (1974). Occurrence of the heteronemertean Gorgonorhynchus bermudensis Wheeler, 1940, in Floridan water. Bulletin of Marine Science 24, 473–492.

Gibson, R. (1977). A new genus and species of lineid heteronemertean from South Africa, Polybrachiorhynchus dayi (Nemertea: Anopla), possessing a multi-branched proboscis. Bulletin of Marine Science 27, 552–571.

Gibson, R. (1981). Nemerteans of the Great Barrier Reef 3. Anopla Heteronemertea (Lineidae). Zoological Journal of the Linnean Society 71, 171–235.
Nemerteans of the Great Barrier Reef 3. Anopla Heteronemertea (Lineidae).Crossref | GoogleScholarGoogle Scholar |

Gibson, R. (1985). The need for a standard approach to taxonomic descriptions of nemerteans. American Zoologist 25, 5–14.
The need for a standard approach to taxonomic descriptions of nemerteans.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.
First molecular evidence for the existence of a Tardigrada + Arthropoda clade.Crossref | GoogleScholarGoogle Scholar | 8583909PubMed |

Graveley, F. H. (1927). Nemertinea. Bulletin of the Madras Government Museum – New Series. Natural History 1, 53–54.

Hillis, D. M., and Dixon, M. T. (1991). Ribosomal DNA: molecular evolution and phylogenetic inference. The Quarterly Review of Biology 66, 411–453.
Ribosomal DNA: molecular evolution and phylogenetic inference.Crossref | GoogleScholarGoogle Scholar | 1784710PubMed |

Hookabe, N., Schwartz, M. L., Kajihara, H., and Norenburg, J. L. (2019). Molecular systematics of the heteronemertean genus Dushia (Nemertea, Pilidiophora), with descriptions of D. wijnhoffae sp. nov. and D. nigra species complex comb. nov. Zootaxa 4691, 333–358.
Molecular systematics of the heteronemertean genus Dushia (Nemertea, Pilidiophora), with descriptions of D. wijnhoffae sp. nov. and D. nigra species complex comb. nov.Crossref | GoogleScholarGoogle Scholar |

Humann, P., and DeLoach, N. (2010). ‘Reef Creature Identification, Tropical Pacific.’ (New World Publications: Jacksonville, FL, USA.)

Kajihara, H. (2015). A histology-free description of the branched-proboscis ribbonworm Gorgonorhynchus albocinctus sp. nov. (Nemertea: Heteronemertea). Publications of the Seto Marine Biological Laboratory 43, 92–102.
A histology-free description of the branched-proboscis ribbonworm Gorgonorhynchus albocinctus sp. nov. (Nemertea: Heteronemertea).Crossref | GoogleScholarGoogle Scholar |

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 : An International Journal for Taxonomy, Systematics, Speciation, Biogeography, and Life History Research of Animals 13, 245–274.
Checklist of nemertean genera and species published between 1995 and 2007.Crossref | GoogleScholarGoogle Scholar |

Kajihara, H., Yoshida, R., and Naruse, T. (2019). Gorgonorhynchus albocinctus (Nemertea: Heteronemertea) from Sotobanari, Yaeyama Islands, Japan. Fauna Ryukyuana 48, 45–47.

Kang, X. X., Fernández-Álvarez, F. Á., Alfaya, J. E., Machordom, A., Strand, M., Sundberg, P., and Sun, S. C. (2015). Species diversity of Ramphogordius sanguineus/Lineus ruber-like nemerteans (Nemertea: Heteronemertea) and geographic distribution of R. sanguineus. Zoological Science 32, 579–589.
Species diversity of Ramphogordius sanguineus/Lineus ruber-like nemerteans (Nemertea: Heteronemertea) and geographic distribution of R. sanguineus.Crossref | GoogleScholarGoogle Scholar | 26654041PubMed |

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 | GoogleScholarGoogle Scholar | 23329690PubMed |

Kimura, M. (1980). A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. Journal of Molecular Evolution 16, 111–120.
A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences.Crossref | GoogleScholarGoogle Scholar | 7463489PubMed |

Krämer, D., Schmidt, C., Podsiadlowski, L., Beckers, P., Horn, L., and von Döhren, J. (2017). Unravelling the Lineus ruber/viridis species complex (Nemertea, Heteronemertea). Zoologica Scripta 46, 111–126.
Unravelling the Lineus ruber/viridis species complex (Nemertea, Heteronemertea).Crossref | GoogleScholarGoogle Scholar |

Kumar, S., Stecher, G., and Tamura, K. (2016). MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Molecular Biology and Evolution 33, 1870–1874.
MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets.Crossref | GoogleScholarGoogle Scholar | 27004904PubMed |

Kvist, S., Laumer, C. E., Junoy, J., and Giribet, G. (2014). New insights into the phylogeny, systematics and DNA barcoding of Nemertea. Invertebrate Systematics 28, 287–308.
New insights into the phylogeny, systematics and DNA barcoding of Nemertea.Crossref | GoogleScholarGoogle Scholar |

Lanfear, R., Frandsen, P. B., Wright, A. M., Senfeld, T., and Calcott, B. (2017). PartitionFinder 2: new methods for selecting partitioned models of evolution for molecular and morphological phylogenetic analyses. Molecular Biology and Evolution 34, 772–773.
| 28013191PubMed |

Littlewood, D. T. J. (1994). Molecular phylogenetics of cupped oysters based on partial 28S rRNA gene sequences. Molecular Phylogenetics and Evolution 3, 221–229.
Molecular phylogenetics of cupped oysters based on partial 28S rRNA gene sequences.Crossref | GoogleScholarGoogle Scholar |

McDermott, J. J., and Roe, P. (1985). Food, feeding behavior and feeding ecology of nemerteans. American Zoologist 25, 113–125.
Food, feeding behavior and feeding ecology of nemerteans.Crossref | GoogleScholarGoogle Scholar |

Norenburg, J. (1993). Riserius pugetensis gen. n., sp. n. (Nemertina: Anopla), a new mesopsammic species, and comments on phylogenetics of some anoplan orders. Hydrobiologia 266, 203–218.
Riserius pugetensis gen. n., sp. n. (Nemertina: Anopla), a new mesopsammic species, and comments on phylogenetics of some anoplan orders.Crossref | GoogleScholarGoogle Scholar |

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

Park, T., Lee, S. H., Sun, S. C., and Kajihara, H. (2019). Morphological and molecular study on Yininemertes pratensis (Nemertea, Pilidiophora, Heteronemertea) from the Han River Estuary, South Korea, and its phylogenetic position within the family Lineidae. ZooKeys 852, 31–51.
Morphological and molecular study on Yininemertes pratensis (Nemertea, Pilidiophora, Heteronemertea) from the Han River Estuary, South Korea, and its phylogenetic position within the family Lineidae.Crossref | GoogleScholarGoogle Scholar | 31210741PubMed |

Peck, L. S. (1993). Larval development in the Antarctic nemertean Parborlasia corrugatus (Heteronemertea: Lineidae). Marine Biology 116, 301–310.
Larval development in the Antarctic nemertean Parborlasia corrugatus (Heteronemertea: Lineidae).Crossref | GoogleScholarGoogle Scholar |

Pope, E. C. (1943). Animal and plant communities of the coastal rock-platform at Long Reef, New South Wales. Proceedings of the Linnean Society of New South Wales 68, 221–254.

Por, F. D. (1989). ‘The Legacy of Tethys. An Aquatic Biogeography of the Levant’. (Kluwer Academic Publishers: Dordrecht, Netherlands.)

Rambaut, A., Drummond, A. J., Xie, D., Baele, G., and Suchard, M. A. (2018). Posterior summarization in Bayesian phylogenetics using Tracer 1.7. Systematic Biology 67, 901–904.
Posterior summarization in Bayesian phylogenetics using Tracer 1.7.Crossref | GoogleScholarGoogle Scholar | 29718447PubMed |

Ronquist, F., Teslenko, M., van der Mark, P., Ayres, D. L., Darling, A., Höhna, S., Larget, B., Liu, L., Suchard, M. A., and Huelsenbeck, J. P. (2012). MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology 61, 539–542.
MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space.Crossref | GoogleScholarGoogle Scholar | 22357727PubMed |

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.

Schwendinger, P. J., and Giribet, G. (2005). The systematics of the south-east Asian genus Fangensis Rambla (Opiliones: Cyphophthalmi: Stylocellidae). Invertebrate Systematics 19, 297–323.
The systematics of the south-east Asian genus Fangensis Rambla (Opiliones: Cyphophthalmi: Stylocellidae).Crossref | GoogleScholarGoogle Scholar |

Serna de Esteban, C. J., and Moretto, H. J. A. (1969). Un nuevo heteronemertino con proboscis ramificada Panorhynchus argentinensis gen. et sp. nov. Ciencia e Investigacion 25, 166–171.

Stamatakis, A. (2014). RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30, 1312–1313.
RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies.Crossref | GoogleScholarGoogle Scholar | 24451623PubMed |

Sun, S. C. (2006). On nemerteans with a branched proboscis from Zhanjiang, China. Journal of Natural History 40, 943–965.
On nemerteans with a branched proboscis from Zhanjiang, China.Crossref | GoogleScholarGoogle Scholar |

Sundberg, P., Andrade, S. C. S., Bartolomaeus, T., Beckers, P., Von Döhren, J., Gibson, R., Giribet, G., Herrera-Bachiller, A., Junoy, J., Kajihara, H., Kvist, S., Kånneby, T., Krämer, D., Sun, S., Turbeville, J. M., and Strand, M. (2016a). The future of nemertean taxonomy (phylum Nemertea) – a proposal. Zoologica Scripta 45, 579–582.
The future of nemertean taxonomy (phylum Nemertea) – a proposal.Crossref | GoogleScholarGoogle Scholar |

Sundberg, P., Kvist, S., and Strand, M. (2016b). Evaluating the utility of single-locus DNA barcoding for the identification of ribbon worms (phylum Nemertea). PLoS One 11, e0155541.
Evaluating the utility of single-locus DNA barcoding for the identification of ribbon worms (phylum Nemertea).Crossref | GoogleScholarGoogle Scholar | 27171471PubMed |

Thiel, M., and Kruse, I. (2001). Status of the Nemertea as predators in marine ecosystems. Hydrobiologia 456, 21–32.
Status of the Nemertea as predators in marine ecosystems.Crossref | GoogleScholarGoogle Scholar |

Thollesson, M., and Norenburg, J. L. (2003). Ribbon worm relationships: a phylogeny of the phylum Nemertea. Proceedings of the Royal Society of London – B. Biological Sciences 270, 407–415.
Ribbon worm relationships: a phylogeny of the phylum Nemertea.Crossref | GoogleScholarGoogle Scholar |

Thornhill, D., Mahon, A., Norenburg, J. L., and Halanych, K. (2008). Open-ocean barriers to dispersal: a test case with the Antarctic Polar Front and the ribbon worm Parborlasia corrugatus (Nemertea: Lineidae). Molecular Ecology 17, 5104–5117.
Open-ocean barriers to dispersal: a test case with the Antarctic Polar Front and the ribbon worm Parborlasia corrugatus (Nemertea: Lineidae).Crossref | GoogleScholarGoogle Scholar | 18992005PubMed |

Wheeler, J. F. G. (1940). Notes on Bermudan nemerteans: Gorgonorhynchus bermudensis, sp. n. Annals and Magazine of Natural History, Series 11 6, 433–438.
Notes on Bermudan nemerteans: Gorgonorhynchus bermudensis, sp. n.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.
The Strepsiptera problem: phylogeny of the holometabolous insect orders inferred from 18S and 28S ribosomal DNA sequences and morphology.Crossref | GoogleScholarGoogle Scholar | 11975347PubMed |

Yamaoka, T. (1940). The fauna of Akkeshi Bay. IX. Nemertini. Joumal of the Faculty of Science, Hokkaido Imperial University, Series 6. Zoology 7, 205–261.

Zattara, E. E., Fernández-Álvarez, F. A., Hiebert, T. C., Bely, A. E., and Norenburg, J. L. (2019). A phylum-wide survey reveals multiple independent gains of head regeneration in Nemertea. Proceedings of the Royal Society of London – B. Biological Sciences 286, 20182524.
A phylum-wide survey reveals multiple independent gains of head regeneration in Nemertea.Crossref | GoogleScholarGoogle Scholar |