Incongruent cladistics reveal a new hydrozoan genus (Cnidaria : Sertularellidae) endemic to the eastern and western coasts of the North Pacific Ocean
Xikun Song A B C H , Cinzia Gravili D E , Bernhard Ruthensteiner F , Mingxin Lyu A and Jianjun Wang GA State Key Laboratory of Marine Environmental Science, College of Ocean and Earth Sciences, Xiamen University, South Xiang’an Road, Xiamen 361102, China.
B Institute of Oceanology, Chinese Academy of Sciences, 7 Nanhai Road, Qingdao 266071, China.
C University of Chinese Academy of Sciences, Beijing 100049, China.
D Dipartimento di Scienze e Tecnologie Biologiche ed Ambientali, Università del Salento, 73100 Lecce, Italy.
E Consorzio Nazionale Interuniversitario per le Scienze del Mare (CoNISMa), Rome, Italy.
F Zoologische Staatssammlung München, Münchhausenstraße 21, 81247 München, Germany.
G Third Institute of Oceanography, State Oceanic Administration, 178 Daxue Road, 361005 Xiamen, China.
H Corresponding author. Email: xksong@xmu.edu.cn
Invertebrate Systematics 32(5) 1083-1101 https://doi.org/10.1071/IS17070
Submitted: 25 August 2017 Accepted: 14 March 2018 Published: 4 October 2018
Abstract
Molecular phylogenetics provides objective references for zoological systematics which sometimes are inconsistent with morphological data. This applies particularly for some primitive phyla such as Cnidaria. The marine hydrozoan Symplectoscyphus turgidus (Sertularellidae) is a recent questionable case reported to occupy an unexpected phylogenetic position and suggested to belong to a new genus. However, its position, based on a single Californian specimen, seemed doubtful. Here we contributed 16S, 18S and 28S rRNA data of another morphologically related species from the Yellow Sea, forming a monophyletic clade with the Californian sample, confirming the clade stability. Further integrative analyses support describing this clade as the new genus Xingyurella, gen. nov., and lead to a taxonomic revision of species characterised by three hydrothecal marginal teeth and strong gonothecal spines. This resulted in a new species and three new combinations: Xingyurella xingyuarum, sp. nov., X. gotoi, comb. nov., X. pedrensis, comb. nov. and X. turgida, comb. nov. Future investigations are required to understand the evolution and speciation involved in the transoceanic distribution pattern of Xingyurella. The approach used herein for dealing with non-monophyletic conditions may be indicative for further studies by integrating trophosome and gonosome traits for Sertularellidae and other hydrozoans.
http://zoobank.org/urn:lsid:zoobank.org:pub:E99F8777-8E31-4C4B-A065-71C71371EEBC.
Additional keywords: hydroid, lectotype designation, molecular phylogenetics, new species, taxonomic revision, fine systematics.
References
Allman, G. J. (1888). Report on the Hydroida dredged by H. M. S. Challenger during the years 1873–76. Part II. – The Tubularinae, Corymorphinae, Campanularinae, Sertularinae, and Thalamophora. The Voyage of H. M. S. Challenger, Zoology (Jena, Germany) 23, 1–90.Billard, A. (1925). Les hydroïdes de l’Expédition du Siboga. II. Synthecidae et Sertularidae. Siboga-Expeditie 7, 1–232.
Bouillon, J., Gravili, C., Pagès, F., Gili, J. M., and Boero, F. (2006). ‘An introduction to Hydrozoa.’ (Memoires du Museum National D’Histoire Naturelle: Paris, France.)
Calkins, G. N. (1899). Some hydroids from Puget Sound. Proceedings of the Boston Society of Natural History 28, 333–367.
Cartwright, P., and Nawrocki, A. M. (2010). Character evolution in Hydrozoa (phylum Cnidaria). Integrative and Comparative Biology 50, 456–472.
| Character evolution in Hydrozoa (phylum Cnidaria).Crossref | GoogleScholarGoogle Scholar |
Cartwright, P., Evans, N. M., Dunn, C. W., Marques, A. C., Miglietta, M. P., Schuchert, P., and Collins, A. G. (2008). Phylogenetics of Hydroidolina (Hydrozoa: Cnidaria). Journal of the Marine Biological Association of the United Kingdom 88, 1663–1672.
| Phylogenetics of Hydroidolina (Hydrozoa: Cnidaria).Crossref | GoogleScholarGoogle Scholar |
Choong, H. H. C. (2015). Hydroids of the genus Sertularella (Cnidaria: Hydrozoa: Sertulariidae) from the Pacific coast of Canada in the collection of the Royal Ontario Museum, with descriptions of four new species. Zootaxa 3925, 387–408.
| Hydroids of the genus Sertularella (Cnidaria: Hydrozoa: Sertulariidae) from the Pacific coast of Canada in the collection of the Royal Ontario Museum, with descriptions of four new species.Crossref | GoogleScholarGoogle Scholar |
Clark, S. F. (1877). Report on the hydroids collected on the coast of Alaska and the Aleutian Islands by W.H. Dall, U.S. Coast Survey, and party, from 1871 to 1874 inclusive. Proceedings. Academy of Natural Sciences of Philadelphia 28, 209–238.
Cornelius, P. F. S. (1995) ‘Synopses of the British Fauna, New Series 50: North-west European thecate hydroids and their medusae. Part 2. Sertulariidae to Campanulariidae.’ (Field Studies Council: Shrewsbury, UK.)
Fontaneto, D., Flot, J. F., and Tang, C. Q. (2015). Guidelines for DNA taxonomy, with a focus on the meiofauna. Marine Biodiversity 45, 433–451.
| Guidelines for DNA taxonomy, with a focus on the meiofauna.Crossref | GoogleScholarGoogle Scholar |
Fraser, C. M. (1911). The hydroids of the west coast of North America. With special reference to those of the Vancouver Island region. Bulletin from the Laboratories of Natural History of the State University of Iowa 6, 3–91.
Fraser, C. M. (1914). Some hydroids of the Vancouver Island region. Transactions of the Royal Society of Canada 8, 99–216.
Fraser, C. M. (1935). Some Japanese hydroids, mostly new. Transactions of the Royal Society of Canada 29, 105–112.
Fraser, C. M. (1936). Hydroid distribution in the vicinity of the Queen Charlotte Islands. Canadian Field Naturalist 50, 122–126.
Fraser, C. M. (1937). ‘Hydroids of the Pacific Coast of Canada and the United States.’ (The University of Toronto Press: Toronto.)
Galea, H. R., Häussermann, V., and Försterra, G. (2009). New additions to the hydroids (Cnidaria: Hydrozoa) from the fjords region of southern Chile. Zootaxa 2019, 1–28.
Giribet, G., Okusu, A., Lindgren, A. R., Huff, S. W., Schrödl, M., and 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.
| Evidence for a clade composed of molluscs with serially repeated structures: Monoplacophorans are related to chitons.Crossref | GoogleScholarGoogle Scholar |
Govindarajan, A. F., Boero, F., and Halanych, K. M. (2006). Phylogenetic analysis with multiple markers indicates repeated loss of the adult medusa stage in Campanulariidae (Hydrozoa, Cnidaria). Molecular Phylogenetics and Evolution 38, 820–834.
| Phylogenetic analysis with multiple markers indicates repeated loss of the adult medusa stage in Campanulariidae (Hydrozoa, Cnidaria).Crossref | GoogleScholarGoogle Scholar |
Gravili, C., De Vito, D., Di Camillo, C. G., Martell, L., Piraino, S., and Boero, F. (2015). The non-Siphonophoran Hydrozoa (Cnidaria) of Salento, Italy with notes on their life-cycles: an illustrated guide. Zootaxa 3908, 1–187.
| The non-Siphonophoran Hydrozoa (Cnidaria) of Salento, Italy with notes on their life-cycles: an illustrated guide.Crossref | GoogleScholarGoogle Scholar |
Hartlaub, C. (1901a). Hydroiden aus dem Stillen Ocean. Ergebnisse einer Reise nach dem Pacific (Schauinsland 1896–97). Zoologische Jahrbuecher, Systematik 14, 349–379.
Hartlaub, C. (1901b). Revision der Sertularella Arten. Abhandlungen aus dem Gebiete der Naturwissenschaften, Naturwissenschaftlicher Verein in Hamburg 16, 1–143.
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 |
Hirohito [Emperor of Japan] (1983). Hydroids from Izu Ôshima and Niijima. Publications of the Biological Laboratory, Imperial Household, Tokyo 6, 1–83.
Hirohito [Emperor of Japan] (1995). The hydroids of Sagami Bay. II. Thecata. Publications of the Biological Laboratory, Imperial Household, Tokyo 1–244.
Inaba, M. (1890). Hydroida collected at Misaki, Miura, Soshu. Zoological Magazine 2, 292–297.
Jäderholm, E. (1896). Ueber aussereuropäische Hydroiden des zoologischen Museums der Universität Upsala. Bihang till Kongl, Svenska Vetenskaps-Akademiens Handligar 4, 1–20.
Leclère, L., Schuchert, P., Cruaud, C., Couloux, A., and Manuel, M. (2009). Molecular phylogenetics of Thecata (Hydrozoa, Cnidaria) reveals long-term maintenance of life history traits despite high frequency of recent character changes. Systematic Biology 58, 509–526.
| Molecular phylogenetics of Thecata (Hydrozoa, Cnidaria) reveals long-term maintenance of life history traits despite high frequency of recent character changes.Crossref | GoogleScholarGoogle Scholar |
Maronna, M. M., Miranda, T. P., Peña Cantero, Á. L., Barbeitos, M. S., and Marques, A. C. (2016). Towards a phylogenetic classification of Leptothecata (Cnidaria, Hydrozoa). Scientific Reports 6, 18075.
| Towards a phylogenetic classification of Leptothecata (Cnidaria, Hydrozoa).Crossref | GoogleScholarGoogle Scholar |
Medel Soteras, M. D., García, F. J., and García-Gómez, J. C. (1991). La familia Sertulariidae (Cnidaria: Hydrozoa) en el Estrecho de Gibraltar y la peninsula iberica: aspectos taxonómicos y zoogeográficos. Cahiers de Biologie Marine 32, 503–543.
Millard, N. A. H. (1975). ‘Annals of The South African Museum: Monograph on the Hydroida of southern Africa.’ (Trustees of the South African Museum: Cape Town, South Africa.)
Moura, C. J., Harris, D. J., Cunha, M. R., and Rogers, A. D. (2008). DNA barcoding reveals cryptic diversity in marine hydroids (Cnidaria, Hydrozoa) from coastal and deep-sea environments. Zoologica Scripta 37, 93–108.
| DNA barcoding reveals cryptic diversity in marine hydroids (Cnidaria, Hydrozoa) from coastal and deep-sea environments.Crossref | GoogleScholarGoogle Scholar |
Moura, C. J., Cunha, M. R., Porteiro, F. M., and Rogers, A. D. (2011). The use of the DNA barcode gene 16S mRNA for the clarification of taxonomic problems within the family Sertulariidae (Cnidaria, Hydrozoa). Zoologica Scripta 40, 520–537.
| The use of the DNA barcode gene 16S mRNA for the clarification of taxonomic problems within the family Sertulariidae (Cnidaria, Hydrozoa).Crossref | GoogleScholarGoogle Scholar |
Nutting, C. C. (1904). American hydroids. Part II. The Sertularidae. Proceedings of the United States National Museum 4, 1–151.
Padial, J. M., Miralles, A., De la Riva, I., and Vences, M. (2010). The integrative future of taxonomy. Frontiers in Zoology 7, 1–14.
| The integrative future of taxonomy.Crossref | GoogleScholarGoogle Scholar |
Park, J. H. (1990). Systematic study on the marine hydroids (Cnidaria, Hydrozoa) in Korea. I. The Korean Journal of Systematic Zoology 6, 71–86.
Park, J. H. (1992). Zoogeographical distribution of marine hydroids (Cnidaria: Hydrozoa: Hydroida) in Korea. The Korean Journal of Systematic Zoology 8, 279–299.
Park, J. H. (1995). Hydroids (Cnidaria: Hydrozoa: Hydroida) from Chindo Island, Korea. The Korean Journal of Systematic Zoology 11, 9–17.
Park, J. H. (1998). Three new records of thecate hydroids from Korean waters. The Korean Journal of Systematic Zoology 14, 59–66.
Park, J. H. (2010). ‘Invertebrate Fauna of Korea, Volume 4, Number 1, Thecates (Cnidaria: Hydrozoa: Thecatae).’ (National Institute of Biological Resources: Incheon, Korea.)
Park, J. H., and Rho, B. J. (1986). A systematic study on the marine hydroids in Korea. 9. The family Sertulariidae. The Korean Journal of Systematic Zoology Special Issue 1, 1–52.
Peña Cantero, Á. L., and Vervoort, W. (2003). Species of Staurotheca Allman, 1888 (Cnidaria: Hydrozoa: Sertulariidae) from US Antarctic expeditions, with the description of three new species. Journal of Natural History 37, 2653–2722.
| Species of Staurotheca Allman, 1888 (Cnidaria: Hydrozoa: Sertulariidae) from US Antarctic expeditions, with the description of three new species.Crossref | GoogleScholarGoogle Scholar |
Peña Cantero, Á. L., Sentandreu, V., and Latorre, A. (2010). Phylogenetic relationships of the endemic Antarctic benthic hydroids (Cnidaria, Hydrozoa): what does the mitochondrial 16S rRNA tell us about it? Polar Biology 33, 41–57.
| Phylogenetic relationships of the endemic Antarctic benthic hydroids (Cnidaria, Hydrozoa): what does the mitochondrial 16S rRNA tell us about it?Crossref | GoogleScholarGoogle Scholar |
Rho, B. J. (1977). ‘Illustrated Flora and Fauna of Korea. 20. Porifera, Hydrozoa and Ascidiacea.’ (Ministry of Education: Seoul, Korea.)
Rho, B. J., and Chang, S. R. (1974). On the classification and the distribution of the marine benthic animals in Korea. I. Hydroids. The Journal of Korean Research Institute for Better Living 12, 133–158.
Schuchert, P. (2001). Hydroids of Greenland and Iceland (Cnidaria, Hydrozoa). Meddelelser om Grønland. Bioscience 53, 1–184.
Schuchert, P. (2015). Sertulariidae Lamouroux, 1812. In ‘World Hydrozoa database’. (Ed. P. Schuchert.) Available at: http://www.marinespecies.org/aphia.php?p=taxdetails&id=1614
Sheth, B. P., and Thaker, V. S. (2017). DNA barcoding and traditional taxonomy: an integrated approach for biodiversity conservation. Genome 60, 618–628.
| DNA barcoding and traditional taxonomy: an integrated approach for biodiversity conservation.Crossref | GoogleScholarGoogle Scholar |
Shimabukuro, V., and Marques, A. C. (2006). Morphometrical analysis, histology, and taxonomy of Thyroscyphus ramosus (Cnidaria, Hydrozoa) from the coast of Brazil. Zootaxa 1184, 29–42.
Song, X. (2016). Diversity and evolution of Sertulariidae Larmouroux, 1812 (Cnidaria: Hydrozoa) in China, with records from Chinese Arctic and Antarctic National Research Expeditions. Ph.D. Thesis, University of Chinese Academy of Sciences & Institute of Oceanology, Chinese Academy of Sciences, China.
Song, X., Gravili, C., Wang, J., Deng, Y., Wang, Y., Fang, L., Lin, H., Wang, S., Zheng, Y., and Lin, J. (2016a). A new deep-sea hydroid (Cnidaria: Hydrozoa) from the Bering Sea Basin reveals high genetic relevance to Arctic and adjacent shallow-water species. Polar Biology 39, 461–471.
| A new deep-sea hydroid (Cnidaria: Hydrozoa) from the Bering Sea Basin reveals high genetic relevance to Arctic and adjacent shallow-water species.Crossref | GoogleScholarGoogle Scholar |
Song, X., Xiao, Z., Gravili, C., Ruthensteiner, B., Mackenzie, M., Wang, S., Chen, J., Yu, N., and Wang, J. (2016b). Worldwide revision of the genus Fraseroscyphus Boero and Bouillon, 1993 (Cnidaria: Hydrozoa): an integrative approach to establish new generic diagnoses. Zootaxa 4168, 1–37.
| Worldwide revision of the genus Fraseroscyphus Boero and Bouillon, 1993 (Cnidaria: Hydrozoa): an integrative approach to establish new generic diagnoses.Crossref | GoogleScholarGoogle Scholar |
Stearns, R. E. C. (1908). Dr. John B. Trask, a pioneer of science on the West Coast. Science 28, 240–243.
| Dr. John B. Trask, a pioneer of science on the West Coast.Crossref | GoogleScholarGoogle Scholar |
Stechow, E. (1913a). Neue Genera thecater Hydroiden aus der Familie der Lafoeiden und neue Species von Thecaten aus Japan. Zoologischer Anzeiger 43, 137–144.
Stechow, E. (1913b). Hydroidpolypen der japanischen Ostküste. II. Teil: Campanularidae, Halecidae, Lafoeidae, Campanulinidae und Sertularidae, nebst Ergänzungen zu den Athecata und Plumularidae. In ‘Beiträge zur Naturgeschichte Ostasiens. Abhandlungen der Königlich Bayerischen Akademie der Wissenschaften’. Supplementband zu den Abhandlungen der Mathematisch-naturwissenschaftlichen Klasse, 3, (Ed. F. Doflein.) pp. 1–162. (Verlag der Königlichen Bayerischen Akademie der Wissenschaften: München.)
Stechow, E. (1920). Neue Ergebnisse auf dem Gebiete der Hydroidenforschung. Sitzungsberichte der Gesellschaft für Morphologie und Physiologie, München 31, 1–30.
Stechow, E. (1923a). Neue Hydroiden der Deutschen Tiefsee Expedition, nebst Bemerkungen über einige andere Formen. Zoologischer Anzeiger 56, 1–20.
Stechow, E. (1923b). Zur Kenntnis der Hydroidenfauna des Mittelmeeres, Amerikas und anderer Gebiete. II. Teil. Zoologische Jahrbücher für Systematik 47, 29–270.
Stechow, E. (1923c). Die Hydroidenfauna der Japanischen Region. Journal of the College of Science, Imperial University of Tokyo 44, 1–23.
Stechow, E. (1925). Hydroiden der deutschen Tiefsee-Expedition. In ‘Wissenschaftliche Ergebnisse der Deutschen Tiefsee-Expedition “Valdivia”’. Vol. 27. (Eds C. Chun, A. Brauer, E. Vanhöffen, and C. Apstein.) pp. 383–546. (Gustav Fischer Verlag, Jena.)
Torrey, H. B. (1902). The Hydroida of the Pacific coast of North America. University of California Publications in Zoology 1, 1–104.
Torrey, H. B. (1904). Contributions from the laboratory of the Marine Biological Association of San Diego. I. The hydroids of the San Diego region. University of California Publications in Zoology 2, 1–43.
Trask, J. B. (1857). On nine new species of zoophytes from the Bay of San Francisco and adjacent localities. Proceedings of the California Academy of Natural Sciences 1, 112–115.
Vervoort, W., and Watson, J. E. (2003). The marine fauna of New Zealand: Leptothecata (Cnidaria: Hydrozoa) (thecate hydroids). NIWA Biodiversity Memoir 119, 1–538.
Yamada, M. (1959). Hydroid fauna of Japan and its adjacent waters. Publications from the Akkeshi Marine Biological Station 9, 1–101.
Yeates, D. K., Seago, A., Nelson, L., Cameron, S. L., Joseph, L., and Trueman, J. W. H. (2011). Integrative taxonomy, or iterative taxonomy? Systematic Entomology 36, 209–217.
| Integrative taxonomy, or iterative taxonomy?Crossref | GoogleScholarGoogle Scholar |