Skip to main content Skip to main navigation menu Skip to site footer
Type: Article
Published: 2019-11-01
Page range: 333–358
Abstract views: 85
PDF downloaded: 2

Molecular systematics of the heteronemertean genus Dushia (Nemertea, Pilidiophora), with descriptions of D. wijnhoffae sp. nov. and D. nigra species complex comb. nov.

Graduate School/Faculty of Science, Hokkaido University, Sapporo 060-0810, Japan
University of Puget Sound, 1500 N. Warner St., Tacoma, WA 98416, USA
Graduate School/Faculty of Science, Hokkaido University, Sapporo 060-0810, Japan
Department of Invertebrate Zoology, Smithsonian National Museum of Natural History, Washington, DC 20560-0163, USA
Nemertea Heteronemertea Lineidae marine invertebrates MEGA MrBayes new species phylogeny RAxML taxonomy TCS

Abstract

The heteronemertean genus Dushia Corrêa, 1963 was established for what was identified as D. atra (Girard, 1851) (originally Meckelia atra) based on material from littoral, shallow waters in Curaçao, while the nominal species Meckelia atra was originally described from deep water off Florida Cape. In this paper, we conclude that the type species for Dushia has been misidentified. Based on specimens from the Caribbean, we establish D. wijnhoffae Schwartz & Norenburg sp. nov. to represent the true identity of the genus, according to Article 70.3.2 of the International Code of Zoological Nomenclature; Meckelia atra should be regarded as a nomen dubium. While the genus has remained monotypic since its establishment, our molecular analysis discovered a second member—or rather a group of members—from the West Pacific. This ‘group of members’, herein termed Dushia nigra (Stimpson, 1855) species complex comb. nov., involves i) at least two genetically separated biological entities, 0.136–0.148 (p-distance) and 0.152–0.168 (K2P) apart in terms of 513-bp COI sequences, which we interpret as likely to represent cryptic species, ii) three color forms, orange, brown, and black, with the last one occurring most frequently, and iii) four nominal species, Meckelia nigra Stimpson, 1855 (now Cerebratulus niger), Meckelia rubella Stimpson, 1855 (now Cerebratulus rubellus), Micrura formosana Yamaoka, 1939, and Micrura japonica Iwata, 1952. At present, however, we have no objective ground as to which of the four potentially available names (i.e., formosana, japonica, nigra, and rubella) should be allotted to the two cryptic species discovered in the analysis, because i) a single locality can harbor two cryptic species, ii) a single cryptic species may contain three different color morphs (i.e., orange, brown, black), and iii) no data from the type localities for these four nominal species are available at the moment. Our multi-locus analysis of heteronemerteans—for which 16S rRNA, COI, 18S rRNA, 28S rRNA, histone H3 genes are available in public databases—shows that Dushia wijnhoffae sp. nov. and Dushia nigra species complex comb. nov. form a clade, which is closely related to Gorgonorhynchus albocinctus Kajihara, 2015 and an undetermined heteronemertean that has been misidentified as Cerebratulus leucopsis (Coe, 1901). Members of Dushia thus show a vicariant Caribbean–West-Pacific distribution, indicating that the lineage predates the rise of the Isthmus of Panama.

 

References

  1. 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. & Sundberg, P. (2012) Disentangling ribbon worm relationships: multi-locus analysis supports traditional classification of the phylum Nemertea. Cladistics, 27, 1–19.

    https://doi.org/10.1111/j.1096-0031.2011.00376.x

    Bourque, D., Miron, G. & Landry, T. (2001) Predation of soft-shell clams (Mya arenaria) by the nemertean Cerebratulus lacteus in Atlantic Canada: implications for control measures. Hydrobiologia, 456, 33–44.

    https://doi.org/10.1023/A:1013061900032

    Bürger, O. (1890) Untersuchungen über die Anatomie und Histologie der Nemertinen nebst Beiträgen zur Systematik. Zeitschrift für wissenschaftliche Zoologie, 50, 1–277.

    Bürger, O. (1895) Fauna und Flora des Golfes von Neapel und der angrenzenden Meeres-abschnitte herausgegeben von der Zoologischen Stazion zu Neapel, 22. Monographie: Nemertinen. R. Friedländer & Sohn, Berlin, xvi + 743 pp., 31 pls.

    https://doi.org/10.5962/bhl.title.14030

    Bürger, O. (1897–1907) Nemertini (Schnurwürmer). In: Bronn, H.G. (Ed.), Klassen und Ordnungen des Tier-Reichs. Supplement 4. C.F. Winter, Leipzig, pp. 1–542.

    Bürger, O. (1904) Nemertini. Das Tierreich, 20, 1–151.

    https://doi.org/10.1039/pl9042000151

    Capella-Gutiérrez, S., Silla-Martínez, J.M. & Gabaldón, T. (2009) trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics, 25, 1972–1973.

    https://doi.org/10.1093/bioinformatics/btp348

    Chernyshev, A.V. (2010) Confocal laser scanning microscopy analysis of the phalloidin-labelled musculature in nemerteans. Journal of Natural History, 44, 2287–2302.

    https://doi.org/10.1080/00222933.2010.504890

    Chernyshev, A.V. (2015) CLSM analysis of the phalloidin-stained muscle system of the nemertean proboscis and rhynchocoel. Zoological Science, 32, 547–561.

    https://doi.org/10.2108/zs140267

    Chernyshev, A.V. (2016) Nemerteans of the coastal waters of Vietnam. In: Adrianov, A.V. & Lutaenko, K.A. (Eds), Biodiversity of the Western Part of the South China Sea. Dalnauka, Vladivostok, pp. 279–314.

    Chernyshev, A.V., Polyakova, N.E., Turanov, S.V. & 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 Biology, 16 (10), 55–68.

    https://doi.org/10.1080/14772000.2017.1317672

    Clement, M., Posada, D. & Crandall, K.A. (2000) TCS: a computer program to estimate gene genealogies. Molecular Ecology, 9, 1657–1659.

    https://doi.org/10.1046/j.1365-294x.2000.01020.x

    Coe, W.R. (1901) The nemerteans of Porto Rico. Bulletin of the United States Commission of Fish and Fisheries for 1900, 2, 223–229.

    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.

    Coe, W.R. (1951a) The nemertean faunas of the Gulf of Mexico and of southern Florida. Bulletin of Marine Science of the Gulf and Caribbean, 1, 149–186.

    Coe, W.R. (1951b) Geographical distribution of the nemerteans of the northern coast of the Gulf of Mexico as compared with those of the southern coast of Florida, with descriptions of three new species. Journal of the Washington Academy of Sciences, 41, 328–331.

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

    https://doi.org/10.1071/ZO98048

    Corrêa, D.D. (1963) Nemerteans from Curaçao. Studies on the Fauna of Curaçao and other Caribbean Islands, 75, 41–56. Available from: http://www.repository.naturalis.nl/document/550005 (Accessed 31 Oct. 2019)

    Crandall, F., Norenburg, J.L. & Gibson, R. (1998) Gonadogenesis, embryogenesis, and unusual oocyte origin in Notogaeanemertes folzae Riser, 1988 (Nemertea, Hoplonemertea). Hydrobiologia, 365, 93–107.

    https://doi.org/10.1023/A:1003145519006

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

    https://doi.org/10.1093/icb/25.1.5

    Girard, C. (1851) Descriptions of a new Planaria and a new Nemertes from the coast of Florida. Proceedings of the Boston Society of Natural History, 4, 137. Available from: https://www.biodiversitylibrary.org/item/35742#page/145/mode/1up (Accessed 31 Oct. 2019)

    Girard, C. (1893) Recherches sur les Planariés et les Némertiens de l’Amérique du Nord. Annals des Sciences Naturelles, Série 7, Zoologie, 15, 145–310. Available from: https://www.biodiversitylibrary.org/item/111186#page/155/mode/1up (Accessed 31 Oct. 2019)

    Giribet, G., Carranza, S., Baguña, J., Riutort, M. & Ribera, C. (1996) First molecular evidence for the existence of a Tardigrada + Arthropoda clade. Molecular Biology and Evolution, 13, 76–84.

    https://doi.org/10.1093/oxfordjournals.molbev.a025573

    Giribet, G., Okusu, A., Lindgren, A.R., Huff, S.W., Schrödl, M. & Nishiguchi, M.K. (2006) Evidence for a clade composed of molluscs with serially repeated structures: Monoplacophorans are related to chitons. Proceedings of the National Academy of Sciences of the United States of America, 103, 7723–7728.

    https://doi.org/10.1073/pnas.0602578103

    Gonzalez-Cueto, J., Quiroga, S. & Norenburg, J. (2014) A shore-based preliminary survey of marine ribbon worms (Nemertea) from the Caribbean coast of Colombia. ZooKeys, 439, 83–108.

    https://doi.org/10.3897/zookeys.439.5965

    Gunton, M. (2009) Life, Scavenger Swarm. BBC, UK. Available from: http://www.bbc.co.uk/programmes/p005bprk (accessed 12 October 2011)

    Habersham, A.W. (1858) The North Pacific Surveying and Exploring Expedition; Or, My Last Cruise. Where We Went and What We Saw: Being an Account of Visits to the Malay and Loo-Choo Islands, the Coasts of China, Formosa, Japan, Kamtschatka, Siberia, and the Mouth of the Amoor River. J.B. Lippincott & Co., Philadelphia and Trübner & Co., London, 507 pp.

    https://doi.org/10.5962/bhl.title.123286

    Honma, Y. & Kitami, T. (1978) Fauna and flora in the waters adjacent to the Sado Marine Biological Station, Niigata University. Annual Report of the Sado Marine Biological Station, Niigata University, 8, 7–81.

    Heine, J.N., McClintock, J.B., Slattery, M. & Weston, J. (1991) Energetic composition, biomass, and chemical defense in the common Antarctic nemertean Parborlasia corrugatus McIntosh. Journal of Experimental Marine Biology and Ecology, 153, 15–25.

    https://doi.org/10.1016/S0022-0981(05)80003-6

    Hiebert, T.C. & Maslakova, S. (2015) Integrative taxonomy of the Micrura alaskensis Coe, 1901 species complex (Nemertea: Heteronemertea), with descriptions of a new genus Maculaura gen. nov. and four new species from the NE Pacific. Zoological Science, 32, 615–637.

    https://doi.org/10.2108/zs150011

    International Commission on Zoological Nomenclature (1999) International Code of Zoological Nomenclature, 4th Edition. International Trust for Zoological Nomenclature, London, xxix + 306 pp.

    Iwata, F. (1952) Nemertini from the coasts of Kyusyu. Journal of the Faculty of Science, Hokkaido University, Series VI, Zoology, 11, 126–148.

    Iwata, F. (1957) Nemerteans from Sagami Bay. Publications from the Akkeshi Marine Biological Station, 7, 1–31.

    Iwata, F. (1960) Nemertini. In: Okada, T. & Uchida, T. (Eds.), Encyclopaedia Zoologica Illustrated in Colours Vol. 4. Hokuryukan, Tokyo, pp. 166–169. [in Japanese]

    Kajihara, H. (2007) A taxonomic catalogue of Japanese nemerteans (phylum Nemertea). Zoological Science, 24, 287–326.

    https://doi.org/10.2108/zsj.24.287

    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.

    https://doi.org/10.5134/199852

    Kajihara, H. (2017) Species diversity of Japanese ribbon worms (Nemertea). In: Motokawa, M. & Kajihara, H. (Eds), Species Diversity of Animals in Japan. Springer Japan, Tokyo, pp. 419–444.

    https://doi.org/10.1007/978-4-431-56432-4_16

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

    https://doi.org/10.1111/j.1096-3642.2010.00650.x

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

    https://doi.org/10.12782/specdiv.16.149

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

    https://doi.org/10.1093/molbev/mst010

    Kem, W.R. & Blumenthal, K.M. (1978) Purification and characterization of the cytotoxic Cerebratulus A toxins. Journal of Biological Chemistry, 253, 5752–5757.

    Kirsteuer, E. (1973) A new polystiliferous hoplonemertean, Curranemertes natans gen. et sp. n., from the Caribbean Sea (Nemertina, Polystilifera, Reptantia). Zoologica Scripta, 2, 125–140.

    https://doi.org/10.1111/j.1463-6409.1974.tb00744.x

    Krämer, D., Schmidt, C., Podsiadlowski, L., Beckers, P., Horn, L. & von Döhren, J. (2017) Unravelling the Lineus ruber/viridis species complex (Nemertea, Heteronemertea). Zoologica Scripta, 46, 111–126. https://doi.org/10.1111/zsc.12185

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

    https://doi.org/10.1093/molbev/msw054

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

    https://doi.org/10.1071/IS13061

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

    https://doi.org/10.1007/s10750-015-2310-5

    Lanfear, R., Frandsen, P.B., Wright, A.M., Senfeld, T. & 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.

    https://doi.org/10.1093/molbev/msw260

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

    https://doi.org/10.1006/mpev.1994.1024

    Maslakova, S.A. & Norenburg, J.L. (2008) 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.

    https://doi.org/10.1080/00222930802130286

    McDermott, J.J. & Roe, P. (1985) Food, feeding behavior and feeding ecology of nemerteans. American Zoologist, 25, 113–126.

    https://doi.org/10.1093/icb/25.1.113

    Palumbi, S., Martin, A., Romano, S., McMillan, W.O., Stice, L. & Grabowski, G. (1991) The Simple Fools Guide to PCR. Version 2.0. Department of Zoology and Kewalo Marine Laboratory, University of Hawaii, Honolulu, 47 pp.

    Puerta, P., Andrade, S.C.S. & Junoy, J. (2010) Redescription of Lineus acutifrons Southern, 1913 (Nemertea: Pilidiophora) and comments on its phylogenetic position. Journal of Natural History, 44, 2363–2378.

    https://doi.org/10.1080/00222933.2010.504895

    Puillandre, N., Lambert, A., Brouillet, S. & Achaz, G. (2012) ABGD, automatic barcode gap discovery for primary species delimitation. Molecular Ecology, 21, 1864–1877.

    https://doi.org/10.1111/j.1365-294X.2011.05239.x

    Punnett, R.C. (1900a) On some South Pacific nemertines collected by Dr Willey. Zoological Results based on Material from New Britain, New Guinea, Loyalty Islands and elsewhere, Collected during the Years 1895, 1896 and 1897 by Arthur Willey, 5, 569–584.

    Punnett, R.C. (1900b) On a collection of nemerteans from Singapore. Quarterly Journal of Microscopical Science, 44, 111–139.

    Punnett, R.C. (1900c) On some nemerteans from Torres Straits. Proceedings of the Zoological Society of London, 1900, 825–831.

    Punnett, R.C. & Cooper, C.F. (1909) On some nemerteans from the eastern Indian Ocean. Transactions of the Linnean Society of London, Series 2, 13, 1–15.

    https://doi.org/10.1111/j.1096-3642.1909.tb00405.x

    Rambaut, A., Suchard, M. & Drummond, A. (2018) Tracer. Available from: http://tree.bio.ed.ac.uk/software/tracer/ (accessed 25 June 2018)

    Riser, N.W. (1990) New Zealand nemertines from kelp holdfasts: Heteronemertinea I. Adenorhagas aurantiafrons gen. n., sp. n. New Zealand Journal of Zoology, 17, 597–606.

    https://doi.org/10.1080/03014223.1990.10422957

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

    https://doi.org/10.1093/sysbio/sys029

    Rowell, T.W. (1992) Destruction of a clam population (Mya arenaria Linne) through the synergistic effects of habitat change and predation by a nemertean (Cerebratulus lacteus Verrill). In: Colombo, G., Ferrari, I., Ceccherelli, V.U. & Rossi, R. (Eds), Marine Eutrophication and Population Dynamics: 25th European Marine Biology Symposium, Institute of Zoology, University of Ferrara. Olsen & Olsen, Fredensborg, pp. 263–269.

    Rowell, T.W. & Woo, P. (1990) Predation by the nemertean worm, Cerebratulus lacteus Verrill, on the soft-shell clam, Mya arenaria Linnaeus, 1758, and its apparent role in the destruction of a clam flat. Journal of Shellfish Research, 9, 291–297.

    Saito, M. & Suzuki, H. (1974) Fauna in the littoral zone of Niisaki Beach in the western part of Sagami Bay, I. Science Reports of the Yokohama National University, Section II, Biological and Geological Sciences, 21, 31–48.

    Schander, C. & Willassen, E. (2005) What can biological barcoding do for marine biology? Marine Biology Research, 1, 79–83.

    https://doi.org/10.1080/17451000510018962

    Schwartz, M.L. (2009) Untying a Gordian Knot of Worms: Systematics and Taxonomy of the Pilidiophora (Phylum Nemertea) from Multiple Data Sets. Ph.D. Dissertation, George Washington University, Washington, D.C., 432 pp.

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

    https://doi.org/10.1023/A:1013093629108

    Schwartz, M.L. & 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. & Giribet, G. (2005) The systematics of the south-east Asian genus Fangensis Rambla (Opiliones: Cyphophthalmi: Stylocellidae). Invertebrate Systematics, 19, 297–323.

    https://doi.org/10.1071/IS05023

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

    https://doi.org/10.1093/bioinformatics/btu033

    Staub, J. (1900) Neue Nemertinen aus Amboina. Denkschriften der Medizinischnaturwissenschaftlichen Gesellschaft zu Jena, 8, 76–98.

    Stiasny-Wijnhoff, G. (1925) On a collection of nemerteans from Curaçao. Bijdragen tot de Dierkunde, 24, 97–120.

    https://doi.org/10.1163/26660644-02401007

    Stimpson, W. (1855) Descriptions of some of the new marine Invertebrata from the Chinese and Japanese Seas. Proceedings of the Academy of Natural Sciences of Philadelphia, 7, 375–384.

    https://doi.org/10.5962/bhl.title.51444

    Stimpson, W. (1857) Prodromus descriptionis animalium evertebratorum, quae in Expeditione ad Oceanum Pacificum Septentrionalem, a Republica Federata missa, Cadwaladaro Ringgold et Johanne Rodgers Ducibus, observavit et descripsit. Proceedings of the Academy of Natural Sciences of Philadelphia, 9, 159–165.

    https://doi.org/10.5962/bhl.title.51447

    Strand, M. & Sundberg, P. (2011) A DNA-based description of a new nemertean (phylum Nemertea) species. Marine Biology Research, 7, 63–70.

    https://doi.org/10.1080/17451001003713563

    Sundberg, P., Kvist, S. & Strand, M. (2016) Evaluating the utility of single-locus DNA barcoding for the identification of ribbon worms (phylum Nemertea). PLoS ONE, 11, e0155541.

    https://doi.org/10.1371/journal.pone.0155541

    Templeton, A.R., Crandall, K.A. & Sing, C.F. (1992) A cladistic analysis of phenotypic associations with haplotypes inferred from restriction endonuclease mapping and DNA sequence data. III. Cladogram estimation. Genetics, 132, 619–633.

    Thiel, M. & Kruse, I. (2001) Status of the Nemertea as predators in marine ecosystems. Hydrobiologia, 456, 21–32.

    https://doi.org/10.1023/A:1013005814145

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

    https://doi.org/10.1098/rspb.2002.2254

    Thornhill, D., Mahon, A., Norenburg, J.L. & 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.

    https://doi.org/10.1111/j.1365-294X.2008.03970.x

    Thompson, C.B. (1908) The commissures and the neurochord cells of the brain of Cerebratulus lacteus. Journal of Comparative Neurology and Psychology, 18, 641–661.

    https://doi.org/10.1002/cne.920180606

    Verrill, A.E. (1895) Supplement to the marine nemerteans and planarians of New England. Transactions of the Connecticut Academy of Arts and Sciences, 9, 523–534.

    Yamaoka T. (1939) Two nemerteans from Formosa. Annotationes Zoologicae Japonenses, 18, 283–289.

    Yin, Z. & Zeng, F. (1984) The study of a new species of genus DendrorhynchusDendrorhynchus zhanjiangensis, of lineid heteronemertean, possessing multibranched proboscis. Marine Science Bulletin, 3, 51–58.

    Zhang, J., Kapli, P., Pavlidis, P. & Stamatakis, A. (2013) A general species delimitation method with applications to phylogenetic placements. Bioinformatics, 29, 2869–2876.

    https://doi.org/10.1093/bioinformatics/btt499