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

An integrated morphological–molecular approach reveals new insights on the systematics of the octocoral Telestula humilis (Thomson, 1927) (Octocorallia : Alcyonacea : Clavulariidae)

Angelo Poliseno https://orcid.org/0000-0001-9939-705X A B H , Alvaro Altuna C , Lara C. Puetz A , Sarah S. T. Mak A , Pilar Ríos https://orcid.org/0000-0001-9710-9114 D , Emily Petroni E , Catherine S. McFadden E , Martin V. Sørensen F and M. Thomas P. Gilbert A G
+ Author Affiliations
- Author Affiliations

A Centre for Evolutionary Hologenomics, The GLOBE Institute, University of Copenhagen, Øster Farimagsgade 5A, DK-1352 Copenhagen, Denmark.

B Molecular Invertebrate Systematics and Ecology Laboratory, Graduate School of Engineering and Science, University of the Ryukyus, 1 Senbaru, JP-903-0213, Nishihara, Japan.

C INSUB, Zemoria 12, E-20013 San Sebastián, Spain.

D Instituto Español de Oceanografía, Centro Oceanográfico de Gijón, Príncipe de Asturias 70 bis, E-33212 Gijón, Spain.

E Department of Biology, Harvey Mudd College, Claremont, CA 91711, USA.

F Natural History Museum of Denmark, University of Copenhagen, Universitetsparken 15, DK-2100 Copenhagen, Denmark.

G University Museum, NTNU, Shøninghuset, B-224, Erling Skakkes gate 47A, NO-7012 Trondheim, Norway.

H Corresponding author. Email: a.poliseno.ita@gmail.com

Invertebrate Systematics 35(3) 261-281 https://doi.org/10.1071/IS20009
Submitted: 26 February 2020  Accepted: 5 October 2020   Published: 24 March 2021

Abstract

Telestula humilis (Thomson, 1927) is a rare deep-sea stoloniferan octocoral distributed in the eastern Atlantic. Here we compared seven putative colonies of this species collected off Spain with the lectotype from the Oceanographic Museum of Monaco and found them to be identical morphologically. Phylogenetic analyses on both full mitogenomes and a concatenated alignment containing two mtDNA genes (mtMutS and Cox1) and nuclear 28S rRNA gene recovered Telestula humilis sister to Incrustatus and Inconstantia rather than to other species of Telestula. This therefore supports its taxonomic reassignment to Pseudotelestula gen. nov. as Pseudotelestula humilis comb. nov. The taxonomic reassignment is also supported by subtle differences observed between the morphology of the colony and the sclerome of Pseudotelestula humilis comb. nov. and the two sister genera. The occurrence of an intrusion tissue with sclerites in the basal part of the gastric cavity of the adult polyps is shared among Telestula and Pseudotelestula gen. nov. However, Pseudotelestula gen. nov. has sclerites arranged in a collaret and points below the tentacles, the sclerites of the calyx wall and the stolon are plump warty spindles, and the intrusion tissue has long sticks and spindles with cone-like spines.

Keywords: Cnidaria, mitochondrial genome, molecular phylogenetics, systematics, taxonomy.


References

Abadi, S., Azouri, D., Pupko, T., and Mayrose, I. (2019). Model selection may not be a mandatory step for phylogeny reconstruction. Nature Communications 10, 934.
Model selection may not be a mandatory step for phylogeny reconstruction.Crossref | GoogleScholarGoogle Scholar | 30804347PubMed |

Acosta Yepes, J., and Sánchez Delgado, F. (2010). Plan de campaña INDEMARES-AVILES 0410. Gobierno de España, Ministerio de Medio Ambiente y Medio Rural y Marino, Madrid, Spain.

Altuna, A. (2015). Cnidarios bentónicos (Cnidaria) del Golfo de Vizcaya y zonas próximas (Atlántico NE) (42°N a 48°30′N y 13°W). Lista de especies, batimetría y anotaciones. Proyecto Fauna Ibérica, Museo Nacional de Ciencias Naturales, Madrid, Spain.

Altuna, A., and Poliseno, A. (2019). Taxonomy, genetics and biodiversity of Mediterranean deep-sea corals and cold-water corals. In ‘Mediterranean Cold-Water Corals: Past, Present and Future’. (Eds C. Orejas, and C. Jiménez.) pp. 121–156. (Springer International Publishing.)

Altuna Prados, A. (1994). Observaciones biogeográficas sobre los cnidarios bentónicos de la costa vasca. Kobie 22, 41–57.

Álvarez Claudio, C. (1993). Hidrozoos bentónicos y catálogo de antozoos de la plataforma y talud continentales de la costa central de Asturias. Ph.D. Thesis, Universidad de Oviedo, Oviedo, Spain.

Álvarez Claudio, C. (1995). Octocoralarios (Cnidaria: Anthozoa) de la plataforma y talud continental de Asturias (Mar Cantábrico). Thalassas 11, 87–92.

Bayer, F. M. (1952). Descriptions of the Hawaiian octocorals collected by the US Fish Commission Steamer Albatross (1. Alcyonacea, Stolonifera, and Telestacea). Pacific Science 6, 126–136.

Bayer, F. M. (1956). Octocorallia. In ‘Treatise on Invertebrate Paleontology, Part F, Coelenterata’. (Ed R. C. Moore.) pp. 166–231. (University of Kansas Press: Lawrence, KS, USA.)

Bayer, F. M. (1961). ‘The Shallow-water Octocorallia of the West Indian Region.’ (Martinus Nijhoff: The Hague, Netherlands.)

Bayer, F. M. (1981). On some genera of Stoloniferous octocorals (Coelenterata: Anthozoa), with descriptions of new taxa. Proceedings of the Biological Society of Washington 94, 879–901.

Bayer, F. M., Grasshoff, M., and Verseveldt, J. (1983). ‘Illustrated Trilingual Glossary of Morphological and Anatomical Terms applied to Octocorallia.’ (E.J. Brill/Dr W. Backhuys: Leiden, Netherlands.)

Braga-Henriques, A., Porteiro, F. M., Ribeiro, P. A., de Matos, V., Sampaio, Í., Ocaña, O., and Santos, R. S. (2013). Diversity, distribution and spatial structure of the cold-water coral fauna of the Azores (NE Atlantic). Biogeosciences 10, 4009–4036.
Diversity, distribution and spatial structure of the cold-water coral fauna of the Azores (NE Atlantic).Crossref | GoogleScholarGoogle Scholar |

Brockman, S. A., and McFadden, C. S. (2012). The mitochondrial genome of Paraminabea aldersladei (Cnidaria: Anthozoa: Octocorallia) supports intramolecular recombination as the primary mechanism of gene rearrangement in octocoral mitochondrial genomes. Genome Biology and Evolution 4, 994–1006.
The mitochondrial genome of Paraminabea aldersladei (Cnidaria: Anthozoa: Octocorallia) supports intramolecular recombination as the primary mechanism of gene rearrangement in octocoral mitochondrial genomes.Crossref | GoogleScholarGoogle Scholar | 22975720PubMed |

Carøe, C., Gopalakrishnan, S., Vinner, L., Mak, S. S. T., Sinding, M. H. S., Samaniego, J. A., Wales, N., Sicheritz‐Pontén, T., and Gilbert, M. T. P. (2018). Single-tube library preparation for degraded DNA. Methods in Ecology and Evolution 9, 410–419.
Single-tube library preparation for degraded DNA.Crossref | GoogleScholarGoogle Scholar |

Castro, C. B., Pires, D. O., Medeiros, M. S., Loiola, L. L., Arantes, R. C. M., Thiago, C. M., and Berman, E. (2006). Capítulo 4. Filo Cnidaria. Corais. In ‘Biodiversidade Bentônica da Região Central da Zona Econômica Exclusiva Brasileira’. (Eds H. P. Lavrado, and B. L. Ignacio.) p. 147–192. (Série Livros n. 18.) (Museu Nacional: Rio de Janeiro, Brazil.)

Coll, M., Piroddi, C., Steenbeek, J., Kaschner, K., Ben Rais Lasram, F., Aguzzi, J., Ballesteros, E., Nike Bianchi, C., Corbera, J., Dailianis, T., Danovaro, R., Estrada, M., Froglia, C., Galil, B. S., Gasol, J. M., Gertwagen, R., Gil, J., Guilhaumon, F., Kesner-Reyes, K., Kitsos, M.-S., Koukouras, A., Lampadariou, N., Laxamana, E., López-Fé de la Cuadra, C. M., Lotze, H. K., Martin, D., Mouillot, D., Oro, D., Raicevich, S., Rius-Barile, J., Saiz-Salinas, J. I., San Vicente, C., Somot, S., Templado, J., Turon, X., Vafidis, D., Villanueva, R., and Voultsiadou, E. (2010). The biodiversity of the Mediterranean Sea: estimates, patterns, and threats. PLoS One 5, e11842.
The biodiversity of the Mediterranean Sea: estimates, patterns, and threats.Crossref | GoogleScholarGoogle Scholar | 20689850PubMed |

Cordeiro, R. (2012). Taxonomia e distribuição de octocorais da plataforma continental e talude norte e nordeste do Brasil. M.Sc. Thesis, Universidade Federal de Pernambuco, Recife, Brazil.

Cordeiro, R., van Ofwegen, L., and Williams, G. (2019a). WoRMS taxon details. Clavulariidae Hickson, 1894. In ‘World Register of Marine Species’. Available at http://www.marinespecies.org/aphia.php?p=taxdetails&id=125270 [Verified 10 July 2019].

Cordeiro, R., van Ofwegen, L., and Williams, G. (2019b). WoRMS taxon details. Telestula Madsen, 1944. In ‘World Register of Marine Species’. Available at http://www.marinespecies.org/aphia.php?p=taxdetails&id=125290 [Verified 1 July 2019].

Deichmann, E. (1936). The Alcyonaria of the western part of the Atlantic Ocean. Memoirs of the Museum of Comparative Zoology at Harvard College 53, 13–17.

Edgar, R. C. (2004). MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research 32, 1792–1797.
MUSCLE: multiple sequence alignment with high accuracy and high throughput.Crossref | GoogleScholarGoogle Scholar | 15034147PubMed |

Gouy, M., Guindon, S., and Gascuel, O. (2010). SeaView version 4: a multiplatform graphical user interface for sequence alignment and phylogenetic tree building. Molecular Biology and Evolution 27, 221–224.
SeaView version 4: a multiplatform graphical user interface for sequence alignment and phylogenetic tree building.Crossref | GoogleScholarGoogle Scholar | 19854763PubMed |

Henry, L. A., and Roberts, J. M. (2007). Biodiversity and ecological composition of macrobenthos on cold-water coral mounds and adjacent off-mound habitat in the bathyal Porcupine Seabight, NE Atlantic. Deep-sea Research – I. Oceanographic Research Papers 54, 654–672.
Biodiversity and ecological composition of macrobenthos on cold-water coral mounds and adjacent off-mound habitat in the bathyal Porcupine Seabight, NE Atlantic.Crossref | GoogleScholarGoogle Scholar |

Instituto Español de Oceanografía (2014). Caracterización ecológica del área marina del sistema de cañones submarinos de Avilés. Informe final área LIFE+ INDEMARES (LIFE07/NAT/E/000732). IEO, Coordinación: Fundación Biodiversidad, Madrid.

Kearse, M., Moir, R., Wilson, A., Stones-Havas, S., Cheung, M., Sturrock, S., Buxton, S., Cooper, A., Markowitz, S., Duran, C., Thierer, T., Ashton, B., Meintjes, P., and Drummond, A. (2012). Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28, 1647–1649.
Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data.Crossref | GoogleScholarGoogle Scholar | 22543367PubMed |

Laackmann, H. (1908). Zur Kenntnis der Alcyonarien-Gattung Telesto Lmx. Zoologische Jahrbucher 11, 41–104.

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 | GoogleScholarGoogle Scholar | 22319168PubMed |

Louzao, M., Anadón, N., Arrontes, J., Álvarez-Claudio, C., Fuente, M., Ocharán, F., Anadón, A., and Acuña, J. L. (2010). Historical macrobenthic community assemblages in the Avilés Canyon, N Iberian Shelf: baseline biodiversity information for a marine protected area. Journal of Marine Systems 80, 47–56.
Historical macrobenthic community assemblages in the Avilés Canyon, N Iberian Shelf: baseline biodiversity information for a marine protected area.Crossref | GoogleScholarGoogle Scholar |

Madsen, F. J. (1944). Octocorallia. The Danish Ingolf-Expedition 5, 1–65.

Mak, S., Gopalakrishnan, S., Carøe, C., Geng, C., Liu, S., Sinding, M. S., Kuderna, L., Zhang, W., Fu, S., Vieira, F. G., Germonpré, M., Bocherens, H., Fedorov, S., Petersen, B., Sicheritz-Pontén, T., Marques-Bonet, T., Zhang, G., Jiang, H., and Gilbert, M. T. P. (2017). Comparative performance of the BGISEQ-500 vs Illumina HiSeq2500 sequencing platforms for palaeogenomic sequencing. GigaScience 6, 1–13.
Comparative performance of the BGISEQ-500 vs Illumina HiSeq2500 sequencing platforms for palaeogenomic sequencing.Crossref | GoogleScholarGoogle Scholar | 28854615PubMed |

McFadden, C. S., and van Ofwegen, L. P. (2012). Stoloniferous octocorals (Anthozoa, Octocorallia) from South Africa, with descriptions of a new family of Alcyonacea, a new genus of Clavulariidae, and a new species of Cornularia (Cornulariidae). Invertebrate Systematics 26, 331–356.
Stoloniferous octocorals (Anthozoa, Octocorallia) from South Africa, with descriptions of a new family of Alcyonacea, a new genus of Clavulariidae, and a new species of Cornularia (Cornulariidae).Crossref | GoogleScholarGoogle Scholar |

McFadden, C. S., and van Ofwegen, L. P. (2013). A second, cryptic species of the soft coral genus Incrustatus (Anthozoa: Octocorallia: Clavulariidae) from Tierra del Fuego, Argentina, revealed by DNA barcoding. Helgoland Marine Research 67, 137–147.
A second, cryptic species of the soft coral genus Incrustatus (Anthozoa: Octocorallia: Clavulariidae) from Tierra del Fuego, Argentina, revealed by DNA barcoding.Crossref | GoogleScholarGoogle Scholar |

McFadden, C. S., Benayahu, Y., Pante, E., Thoma, J. N., Nevarez, P. A., and France, S. C. (2011). Limitations of mitochondrial gene barcoding in the cnidarian sub-class Octocorallia. Molecular Ecology Resources 11, 19–31.
Limitations of mitochondrial gene barcoding in the cnidarian sub-class Octocorallia.Crossref | GoogleScholarGoogle Scholar | 21429097PubMed |

Morri, C., Esposito, F., and Pessani, D. (2008). Anthozoa. Biologia Marina Mediterranea 15, 92–101.

Murillo, F. J., Durán Muñoz, P., Altuna, A., and Serrano, A. (2011). Distribution of deep-water corals of the Flemish Cap, Flemish Pass and the Grand Banks of Newfoundland (northwest Atlantic Ocean): interaction with fishing activities. ICES Journal of Marine Science 68, 319–332.
Distribution of deep-water corals of the Flemish Cap, Flemish Pass and the Grand Banks of Newfoundland (northwest Atlantic Ocean): interaction with fishing activities.Crossref | GoogleScholarGoogle Scholar |

Nutting, C. C. (1908). Descriptions of the Alcyonaria collected by the US Bureau of Fisheries steamer ‘Albatross’ in the vicinity of the Hawaiian Islands in 1902. Proceedings of the United States National Museum 34, 543–601.
Descriptions of the Alcyonaria collected by the US Bureau of Fisheries steamer ‘Albatross’ in the vicinity of the Hawaiian Islands in 1902.Crossref | GoogleScholarGoogle Scholar |

Nutting, C. C. (1909). Alcyonaria of the California coast. Proceedings of the United States National Museum 35, 681–727.
Alcyonaria of the California coast.Crossref | GoogleScholarGoogle Scholar |

Pax, F., and Müller, I. (1954). Catalogue des types d’Anthozoaires du Musée océanographique de Monaco. Bulletin de l’Institut Océanographique 51, 1–40.

Pires, D. O., and Castro, C. B. (2010). Cnidaria. In ‘Biodiversidade da Região Oceânica Profunda da Bacia de Campos: Megafauna e Ictiofauna Demersal’. (Eds H. P. Lavrado, and A. C. S. Brasil.) pp. 59–112. (SAG Serv.: Rio de Janeiro, Brazil.)

Porebski, S., Bailey, L. G., and Baum, B. (1997). Modification of a CTAB DNA extraction protocol for plants containing high polysaccharide and polyphenol components. Plant Molecular Biology Reporter 15, 8–15.
Modification of a CTAB DNA extraction protocol for plants containing high polysaccharide and polyphenol components.Crossref | GoogleScholarGoogle Scholar |

Quattrini, A. M., Faircloth, B. C., Dueñas, L. F., Bridge, T. C. L., Brugler, M. R., Calixto-Botía, I. F., DeLeo, D. M., Forêt, S., Herrera, S., Lee, S. M. Y., Miller, D. J., Prada, C., Rádis-Baptista, G., Ramírez-Portilla, C., Sánchez, J. A., Rodríguez, E., and McFadden, C. S. (2018). Universal target-enrichment baits for anthozoan (Cnidaria) phylogenomics: new approaches to long-standing problems. Molecular Ecology Resources 18, 281–295.
Universal target-enrichment baits for anthozoan (Cnidaria) phylogenomics: new approaches to long-standing problems.Crossref | GoogleScholarGoogle Scholar | 29131534PubMed |

Quattrini, A. M., Rodríguez, E., Faircloth, B. C., Cowman, P. F., Brugler, M. R., Farfan, G., Hellberg, M. E., Kitahara, M. V., Morrison, C. L., Paz-García, D. A., Reimer, J. D., and McFadden, C. S. (2020). Paleoclimate ocean conditions shaped diversification of coral skeletal composition through deep time. Nature Ecology & Evolution XX, 12–34.

Ronquist, F., and Huelsenbeck, J. (2003). MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19, 1572–1574.
MrBayes 3: Bayesian phylogenetic inference under mixed models.Crossref | GoogleScholarGoogle Scholar | 12912839PubMed |

Sampaio, Í., Freiwald, A., Porteiro, F. M., Menezes, G., and Carreiro-Silva, M. (2019). Census of Octocorallia (Cnidaria: Anthozoa) of the Azores (NE Atlantic) with a nomenclature update. Zootaxa 4550, 451–498.
Census of Octocorallia (Cnidaria: Anthozoa) of the Azores (NE Atlantic) with a nomenclature update.Crossref | GoogleScholarGoogle Scholar |

Sánchez, F., Cristobo, J., Ríos, P., González-Pola, C., Parra, S., Lourido, A., Druet, M., Rivera, J., and Frutos, I. (2012). Informe de las campañas INDEMARES-AVILES 0412, INDEMARES-AVILES 0912. Gobierno de España, Ministerio de Economía y Competitividad.

Sánchez, F., Ríos, P., Prado, E., González-Pola, C., Rodríguez-Cabello, C., Rodríguez Basalo, A., Cristobo, J., Patrocinio, T., Fernandez, R., Díez, I., and Reguera, I. (2019). Informe de Campaña ECOMARG 2019. Gobierno de España, Ministerio de Ciencia, Innovación y Universidades.

Sánchez Delgado, F., and Serrano, A. (2010). INDEMARES 0710. Plan de campaña. Gobierno de España, Ministerio de Ciencia e Innovación, Madrid.

Sanmartín Payá, E. (2004). Octocorales (clase Anthozoa: Cnidaria) de Islandia. Sistemática. Unpublished thesis, University of Valencia.

Serrano, A. (2011) INDEMARES 0711. Plan de campaña. Gobierno de España, Ministerio de Ciencia e Innovación, Madrid.

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 | GoogleScholarGoogle Scholar | 16928733PubMed |

Stamatakis, A., Hoover, P., and Rougemont, J. (2008). A rapid bootstrap algorithm for the RAxML Web servers. Systematic Biology 57, 758–771.
A rapid bootstrap algorithm for the RAxML Web servers.Crossref | GoogleScholarGoogle Scholar | 18853362PubMed |

Stiasny, G. (1941). Alcyonaria und Gorgonaria von St. Helena. Zoologische Jahrbucher 74, 473–486.

Stöver, B. C., and Müller, K. F. (2010). TreeGraph 2: combining and visualizing evidence from different phylogenetic analyses. Bioinformatics 11, 7.
| 20051126PubMed |

Studer, T. (1901). Alcyonaires provenant des campagnes de l’Hirondelle (1886–88). Résultats des Campagnes Scientifiques accomplies sur son yacht par Albert Ier Prince Soverain de Monaco 20, 1–64.

Thomson, J. A. (1927). Alcyonaires provenant des campagnes scientifiques du Prince Albert Ier de Monaco. Résultats des Campagnes Scientifiques accomplies sur son yacht par Albert Ier Prince Soverain de Monaco 73, 1–77.

Thomson, J. A., and Dean, L. M. I. (1931). The Alcyonacea of the Siboga expedition. Siboga-Expeditie Monographie 13d, 1–227.

Tixier-Durivault, A. (1964). Stolonifera and Alcyonacea. Galathea Report 7, 43–58.

Tixier-Durivault, A., and d’Hondt, M. J. (1975). Les Octocoralliaires de la campagne Biaçores. Bulletin du Muséum National d’Histoire Naturelle 252, 1361–1433.

Utinomi, H. (1973). Description of a new species of Telesto from the inland Sea of Japan, with a review of the telestacean octocorals. Publications of the Seto Marine Biological Laboratory 20, 145–155.
Description of a new species of Telesto from the inland Sea of Japan, with a review of the telestacean octocorals.Crossref | GoogleScholarGoogle Scholar |

van Ofwegen, L. P., Häussermann, V., and Försterra, G. (2006). A new genus of soft coral (Octocorallia: Alcyonacea: Clavulariidae) from Chile. Zootaxa 1219, 47–57.
A new genus of soft coral (Octocorallia: Alcyonacea: Clavulariidae) from Chile.Crossref | GoogleScholarGoogle Scholar |

Watling, L., and Auster, P. J. (2005). Distribution of deep-water Alcyonacea off the northeast coast of the United States. In ‘Cold-water Corals and Ecosystems’. (Eds A. Freiwald, and J. M. Roberts.) pp. 279–296. (Springer-Verlag: Berlin, Germany.)

Watling, L., France, S. C., Pante, E., and Simpson, A. (2011). Biology of deep-water corals. Advances in Marine Biology 60, 41–122.
Biology of deep-water corals.Crossref | GoogleScholarGoogle Scholar | 21962750PubMed |

Weinberg, S. (1990). A redescription of the specimens of ‘Telesto humilis’ (Octocorallia) collected by Prince Albert Ier of Monaco, with the descriptions of four new species. Beaufortia 41, 205–218.

Wright, E. P., and Studer, T. (1889). Report on the Alcyonaria. Report of the scientific results of the Voyage of H.M.S. Challenger 1873–1876. Zoology 64, 13–14.