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Systematics, phylogeny and biogeography
RESEARCH ARTICLE

Polyphyly and cryptic diversity in the hydrozoan families Lafoeidae and Hebellidae (Cnidaria : Hydrozoa)

Carlos J. Moura A E , Marina R. Cunha A , Filipe M. Porteiro B and Alex D. Rogers C D
+ Author Affiliations
- Author Affiliations

A Centro de Estudos do Ambiente e do Mar (CESAM), Departamento de Biologia, Universidade de Aveiro, Campus Universitário de Santiago, 3810-193, Aveiro, Portugal.

B Departamento de Oceanografia e Pescas, Universidade dos Açores, Cais de Santa Cruz, 9901-862, Horta, Açores, Portugal.

C Institute of Zoology, Zoological Society of London, Regent’s Park, London, NW1 4RY, UK.

D Present address: Department of Zoology, University of Oxford, Tinbergen Building, South Parks Road, Oxford, OX1 3PS, UK.

E Corresponding author. Email: carlos.moura@mail.com

Invertebrate Systematics 25(5) 454-470 https://doi.org/10.1071/IS11045
Submitted: 9 November 2011  Accepted: 28 November 2011   Published: 14 February 2012

Abstract

The taxonomy of the putative superfamily Lafoeoidea (Hydrozoa), which includes the families Hebellidae and Lafoeidae, has been widely disputed at all systematic levels, mainly because these are morphologically simple and plastic animals. We used the molecular marker 16S mRNA to address phylogenetic relations of ‘Lafoeoidea’ hydroids mainly from shallow and deep waters of the north-east Atlantic and west Mediterranean. This study proves that the morphological simplicity of the ‘Lafoeoidea’ has led to several erroneous taxonomic assignments. We demonstrate that the superfamily ‘Lafoeoidea’ is not monophyletic and thus not valid; the families Hebellidae and Lafoeidae are polyphyletic. The ‘Lafoeidae’ subfamilies ‘Lafoeinae’ and ‘Zygophylacinae’ were recovered as monophyletic but quite distantly related and should be erected to the level of distinct families. The 16S haplotype data analysed in conjunction with morphological characters and distribution data were useful in differentiating morphologically undistinguishable, nominal and cryptic or pseudo-cryptic species, including undescribed taxa. Particularly within the ‘Lafoeinae’ group, unexpectedly high genetic biodiversity (including cryptic species) was encountered in the possibly not monophyletic genera Lafoea, Acryptolaria and Filellum. Cryptic diversity is also likely associated with the ‘Zygophylacinae’ nominal species Cryptolaria pectinata. The indications of genetic segregation by geographical distance of the ‘Lafoeoidea’ hydroids, particularly verified in deep waters, is probably a consequence of their reduced potential for large-scale dispersal, which likely interacts with the influence of the seabed topography, oceanographic circulation and adaptability to tolerate different abiotic conditions.


References

Andrade, L. P., and Migotto, A. E. (1997). Is there a link between Hebella hydroids (Hydrozoa, Lafoeidae) and Staurodiscus medusa (Hydrozoa, Laodiceidae)? In ‘Proceedings of the VII Colacmar – Congresso Latino-Americano sobre Ciências do Mar, Santos’. pp. 35–36.

Boero, F., Bouillon, J., and Kubota, K. (1997). The medusae of some species of Hebella Allman, 1888, and Anthohebella gen. nov. (Cnidaria, Hydrozoa, Lafoeidae), with a world synopsis of species. Zoologische Verhandelingen 310, 1–53.

Bouillon, J., Gravili, C., Pagès, F., Gili, J.-M., and Boero, F. (2006). An introduction to Hydrozoa. Mémoires du Muséum National d’Histoire Naturelle 194, 1–591.

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 |

Castresana, J. (2000). Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Molecular Biology and Evolution 17, 540–552.
| 1:CAS:528:DC%2BD3cXisVSgt7g%3D&md5=80266c69ff06e9597e174b5b279ae87bCAS |

Cornelius, P. F. S. (1975). A revision of the species of Lafoeidae and Haleciidae (Coelenterata: Hydroida) recorded from Britain and nearby seas. Zoology (Jena, Germany) 28, 375–426.

Gili, J. M., Vervoort, W., and Pages, F. (1989). Hydroids from the West African coast: Guinea Bissau, Namibia and South Africa. Scientia Marina 53, 67–112.

Guindon, S., and Gascuel, O. (2003). A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Systematic Biology 52, 696–704.
A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood.Crossref | GoogleScholarGoogle Scholar |

Hernández-Molina, F. J., Llave, E., Stow, D. A. V., García, M., Somoza, L., Vázquez, J. T., Lobo, F. J., Maestro, A., Río, V. D., León, R., Medialdea, T., and Gardner, J. (2006). The contourite depositional system of the Gulf of Cadiz: a sedimentary model related to the bottom current activity of the Mediterranean outflow water and its interaction with the continental margin. Deep-sea Research. Part II, Topical Studies in Oceanography 53, 1420–1463.
The contourite depositional system of the Gulf of Cadiz: a sedimentary model related to the bottom current activity of the Mediterranean outflow water and its interaction with the continental margin.Crossref | GoogleScholarGoogle Scholar |

Huelsenbeck, J. P., and Ronquist, F. (2001). MRBAYES: Bayesian inference of phylogeny. Bioinformatics (Oxford, England) 17, 754–755.
MRBAYES: Bayesian inference of phylogeny.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3MvotV2isw%3D%3D&md5=89aaec60163cef8dac4fe0ecf046c64cCAS |

Hughes, R. G. (1977). Aspects of the biology and life-history of Nemertesia antennina (L.) (Hydrozoa: Plumulariidae). Journal of the Marine Biological Association of the United Kingdom 57, 641–657.
Aspects of the biology and life-history of Nemertesia antennina (L.) (Hydrozoa: Plumulariidae).Crossref | GoogleScholarGoogle Scholar |

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 |

Marques, A. C., Altuna, A., Peña Cantero, A. L., and Migotto, A. E. (2004). Redescription of Bedotella armata from the Biscay Bay, northern Spain, the type species of Bedotella Stechow, 1913 (Cnidaria, Hydrozoa, Lafoeidae), with comments on its taxonomic position. Hydrobiologia 530–531, 223–230.
Redescription of Bedotella armata from the Biscay Bay, northern Spain, the type species of Bedotella Stechow, 1913 (Cnidaria, Hydrozoa, Lafoeidae), with comments on its taxonomic position.Crossref | GoogleScholarGoogle Scholar |

Marques, A. C., Peña Cantero, A. L., and Migotto, A. E. (2005a). Revision of the genus Cryptolarella Stechow, 1913 (Lafoeidae, Leptothecata, Hydrozoa). Journal of Natural History 39, 709–722.
Revision of the genus Cryptolarella Stechow, 1913 (Lafoeidae, Leptothecata, Hydrozoa).Crossref | GoogleScholarGoogle Scholar |

Marques, A. C., Peña Cantero, A. L., and Migotto, A. E. (2005b). Redescription and systematic status of the Antarctic genus Abietinella Levinsen, 1913 (Lafoeidae, Hydrozoa, Cnidaria). Journal of Natural History 39, 1443–1455.
Redescription and systematic status of the Antarctic genus Abietinella Levinsen, 1913 (Lafoeidae, Hydrozoa, Cnidaria).Crossref | GoogleScholarGoogle Scholar |

Marques, A. C., Peña Cantero, A. L., and Migotto, A. E. (2006). An overview of the phylogeny of the families Lafoeidae and Hebellidae (Hydrozoa: Leptothecata): their composition and classification. Invertebrate Systematics 20, 43–58.
An overview of the phylogeny of the families Lafoeidae and Hebellidae (Hydrozoa: Leptothecata): their composition and classification.Crossref | GoogleScholarGoogle Scholar |

Medel, M. D. (1996). Estudio taxonómico de los hidrozoos del Estrecho de Gibraltar. Ph.D. Thesis, University of Sevilla, Spain.

Migotto, A. E., and Andrade, L. P. (2000). The life cycle of Hebella furax (Cnidaria: Hydrozoa): a link between a lafoeid hydroid and a laodiceidae medusae. Journal of Natural History 34, 1871–1888.
The life cycle of Hebella furax (Cnidaria: Hydrozoa): a link between a lafoeid hydroid and a laodiceidae medusae.Crossref | GoogleScholarGoogle Scholar |

Millard, N. A. H. (1975). Monograph on the Hydroida of southern Africa. Annals of South African Museum 68, 1–513.

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.

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 |

Moura, C. J., Cunha, M. R., Porteiro, F. M., Yesson, C., and Rogers, A. D. (2012). Evolution of Nemertesia hydroids (Cnidaria: Hydrozoa, Plumulariidae) from the shallow and deep waters of the NE Atlantic and W Mediterranean. Zoologica Scripta 41, 79–96.
Evolution of Nemertesia hydroids (Cnidaria: Hydrozoa, Plumulariidae) from the shallow and deep waters of the NE Atlantic and W Mediterranean.Crossref | GoogleScholarGoogle Scholar |

Nylander, J. A. A. (2004). ‘MrModeltest v2.’ Program distributed by the author. (Evolutionary Biology Centre: Uppsala University, Sweden.)

Peña, A. L., and García-Carrascosa, A. M. (1993). The coppinia of Abietinella operculata (Lafoeidae: Hydrozoa Leptomedusae) and its systematic position. Journal of Natural History 27, 1003–1011.
The coppinia of Abietinella operculata (Lafoeidae: Hydrozoa Leptomedusae) and its systematic position.Crossref | GoogleScholarGoogle Scholar |

Peña Cantero, A. L., and García Carrascosa, A. M. (2002). The benthic hydroid fauna of the Chafarinas Islands (Alborán Sea, western Mediterranean). Zoologische Verhandelingen 337, 1–180.

Peña Cantero, A. L., García Carrascosa, A. M., and Vervoort, W. (1998). On the species of Filellum Hincks, 1868 (Cnidaria: Hydrozoa) with the description of a new species. Journal of Natural History 32, 297–315.
On the species of Filellum Hincks, 1868 (Cnidaria: Hydrozoa) with the description of a new species.Crossref | GoogleScholarGoogle Scholar |

Peña Cantero, A. L., Marques, A. C., and Migotto, A. E. (2007). Revision of the genus Acryptolaria Norman, 1875 (Cnidaria, Hydrozoa, Lafoeidae). Journal of Natural History 41, 229–291.
Revision of the genus Acryptolaria Norman, 1875 (Cnidaria, Hydrozoa, Lafoeidae).Crossref | GoogleScholarGoogle Scholar |

Peña Cantero, A. 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 |

Pérez, F. F., Rios, A. F., Castro, C. G., and Fraga, F. (1998). Mixing analysis of nutrients, oxygen and dissolved inorganic carbon in the upper and middle North Atlantic ocean east of the Azores. Journal of Marine Systems 16, 219–233.
Mixing analysis of nutrients, oxygen and dissolved inorganic carbon in the upper and middle North Atlantic ocean east of the Azores.Crossref | GoogleScholarGoogle Scholar |

Ramil, F., and Vervoort, W. (1992). Report on the Hydroida collected by the ‘BALGIM’ expedition in and around the Strait of Gibraltar. Zoologische Verhandelingen 277, 3–262.

Schuchert, P. (2001). The hydroids of Greenland and Iceland (Cnidaria, Hydrozoa). Meddelelser om Grønland 53, 1–184.

Sommer, C. (1992). Larval biology and dispersal of Eudendrium racemosum (Hydrozoa, Eudendriidae). Scientia Marina 56, 205–211.

Stepanjants, S. D. (1979). Hydroids of the Antarctic and subantarctic waters. Explorations of the fauna of the seas. Biological results of the Soviet Antarctic expeditions, 6. Issledovaniya Fauny Morei 22, 1–200.

Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M., and Kumar, S. (2011). MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution 28, 2731–2739.
MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXht1eiu73K&md5=ff48f25899fc988f16ef1534cf14445fCAS |

Vervoort, W. (1972). Hydroids from the Theta, Vema and Yelcho cruises of the Lamont-Doherty geological observatory. Zoologische Verhandelingen 120, 1–247.