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

The genus Pycnoclavella (Ascidiacea) in the Atlanto-Mediterranean region: a combined molecular and morphological approach

Rocío Pérez-Portela A B , Sandra Duran A , Cruz Palacín A and Xavier Turon A
+ Author Affiliations
- Author Affiliations

A Department of Animal Biology (Invertebrates), Faculty of Biology, University of Barcelona, 645 Diagonal Ave, Barcelona 08028, Spain.

B Corresponding author. Email: rocio_perez@ub.edu

Invertebrate Systematics 21(2) 187-205 https://doi.org/10.1071/IS06015
Submitted: 31 May 2006  Accepted: 27 February 2007   Published: 21 May 2007

Abstract

The taxonomy of the genus Pycnoclavella on European shores has been controversial. Variability in colour patterns and other characters and the incompleteness of descriptions have contributed to the confusion. To clarify the taxonomic positions of the variety of forms attributable to this genus, western Mediterranean and north-eastern Atlantic sites were sampled. The present study employed morphological descriptions and a molecular approach, using a fragment of the cytochrome c oxidase I gene of 120 colonies for phylogenetic analyses. The results reveal an unexpected species richness of the genus Pycnoclavella in the Atlanto-Mediterranean region, with genetic data indicating there are six different species of Pycnoclavella in the area and morphological observations supporting these results. Pigment distribution, larval type and incubation mode were found to be the most useful morphological characters for discriminating the species. Based on collections at the type localites, Pycnoclavella aurilucens, which has an Atlanto-Mediterranean distribution, is assigned to one of the genetic clades. Clavelina nana is assigned to a Mediterranean clade of the genus Pycnoclavella. Three new species are described: Pycnoclavella communis, Pycnoclavella brava and Pycnoclavella atlantica. One of the genetic clades is left unnamed, because characters are insufficiently clear to allow the description of a morphospecies.

Additional keywords: Clavelina, COI, cryptic species, phylogeny.


Acknowledgements

Dr John Bishop and Dr Keith Hiscock sent samples and pictures of Pycnoclavella aurilucens from the type location (Plymouth). Dr Peter Wirtz provided samples of Pycnoclavella communis from Madeira. Dr Riccardo Brunetti sent samples of Pycnoclavella taureanensis from Palmi. Dr Enric Ballesteros offered his collection of underwater pictures. The research was funded by project CTM2004-05265-C02-01 of the Spanish Ministry of Education and Science.


References


Avise J. C., Arnold J., Ball R. M., Bermingham E., Lamb T., Neigel J. E., Reeb C. A., Saunders N. C. (1987) Intraspecific phylogeography: the mitochondrial DNA bridge between population genetics and systematics. Annual Review of Ecology and Systematics 18, 489–522. open url image1

Baric S., Sturmbauer C. (1999) Ecological parallelism and cryptic species in the genus Ophiothrix derived from mitochondrial DNA sequences. Molecular Phylogenetics and Evolution 11, 157–162.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Berrill N. J. (1947) The structure, tadpole and budding of the ascidian Pycnoclavella aurilucens Garstang. Journal of the Marine Biological Association of the United Kingdom 27, 245–251. open url image1

Berrill N. J. (1950). ‘The Tunicata.’ (Ray Society: London.)

Berrill N. J. (1951) Regeneration and budding in tunicates. Biological Reviews 26, 456–475. open url image1

Borsa P., Naciri M., Bahri L., Chikhi L., Garcia de León F. J., Kotoulas G., Bonhomme F. (1997) Intraspecific zoogeography of the Mediterranean: population genetic analysis on sixteen atlanto-mediterranean species (fishes and invertebrates). Vie et Milieu 47, 295–305. open url image1

Brunetti R. (1987) Species of Clavelina in the Mediterranean Sea. Annals de L’Institut océanografique (Paris) , 101–118. open url image1

Brunetti R. (1991) Pycnoclavella taureanensis n.sp. (Ascidiacea) from the Mediterranean Sea. Vie et Milieu 41, 245–248. open url image1

Felsenstein J. (1981) Evolutionary trees from DNA sequences: a maximum likelihood approach. Journal of Molecular Evolution 17, 368–376.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Folmer O., Black M., Hoeh W., Lutz R., Vrijenhoek R. (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology 3, 294–299.
PubMed |
open url image1

France S. C., Hoover L. L. (2002) DNA sequences of the mitochondrial COI gene have low levels of divergence among deep-sea octocorals (Cnidaria: Anthozoa). Hydrobiologia 471, 149–155.
Crossref | GoogleScholarGoogle Scholar | open url image1

Garstang W. (1891) Report on the Tunicata of Plymouth. 1. Clavelinidae, Perophoridae, Diazonidae. Journal of the Marine Biological Association of the United Kingdom 2, 47–67. open url image1

Goodbody I. (1996) Pycnoclavella belizeana, a new species of ascidian from the Caribbean. Bulletin of Marine Science 58, 590–597. open url image1

Hall T. A. (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series 41, 95–98. open url image1

Hart M. W., Podolsky R. D. (2005) Mitochondrial DNA phylogeny and rates of larval evolution in Macrophiothrix brittlestars. Molecular Phylogenetics and Evolution 34, 438–447.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Hebert P. D. N., Ratnasingham S., deWaard J. R. (2003) Barcoding animal life: cytochrome c oxidase subunit 1 divergences among closely related species. Proceedings of The Royal Society of London B: Biological Sciences 270, S96–S99.
Crossref | GoogleScholarGoogle Scholar | open url image1

Huelsenbeck J. P., Ronquist F. (2001) MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatic 17, 754–755.
Crossref | GoogleScholarGoogle Scholar | open url image1

Jobb G., Von Haeseler A., Strimmer K. (2004) TREEFINDER: a powerful graphical analysis environment for molecular phylogenetics. BMC Evolutionary Biology 28, 4–18. open url image1

Kolaczkowski B., Thornton J. (2004) Performance of maximum parsimony and likelihood phylogenetics when evolution is heterogeneous. Nature 431, 980–984.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Kott P. (1990) The Australian Ascidiacea. Part 2, Aplousobranchiata (1) Memoirs of the Queensland Museum 29, 1–299. open url image1

Kott P. (2003) New syntheses and new species in the Australian Ascidiacea. Journal of Natural History 37, 1611–1653.
Crossref | GoogleScholarGoogle Scholar | open url image1

Kott P. (2005) Pycnoclavella (Tunicata: Ascidiacea) species from the West Indian Ocean. African Zoology 40, 205–212. open url image1

Kumar S., Tamura K., Nei M. (2004) MEGA3: Integrated software for Molecular Evolutionary Genetics Analysis and sequence alignment. Briefings in Bioinformatics 5, 150–163.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Lafargue F., Ramos A. A., Turon X., Banaigs B., Wahl M. (1986) The littoral ascidians of the Spanish Mediterranean I. From Port Bou to the Islas Medas. Vie et Milieu 36, 133–139. open url image1

Lahille M. F. (1890). Recherches sur les Tuniciers. Ph.D. Thesis, Faculty of Sciences, University of Paris, Toulouse, France.

Landry C., Geyer L. B., Arakaki Y., Uehara T., Palumbi S. R. (2003) Recent speciation in the Indo-West Pacific: rapid evolution of gamete recognition and sperm morphology in cryptic species of the sea urchin. Proceedings of The Royal Society of London Series B: Biological Sciences 270, 1839–1847.
Crossref | GoogleScholarGoogle Scholar | open url image1

Lazoski C., Solé-Cava A. M., Boury-Esnault N., Klautau M., Russo C. A. M. (2001) Cryptic speciation in a high gene flow scenario in the oviparous marine sponge Chondrosia reniformis. Marine Biology 139, 421–429.
Crossref | GoogleScholarGoogle Scholar | open url image1

López-Legentil S., Turon X. (2005) How do morphotypes and chemotypes relate to genotypes? The colonial ascidian Cystodytes (Polycitoridae). Zoologica Scripta 34, 3–14.
Crossref | GoogleScholarGoogle Scholar | open url image1

López-Legentil S., Turon X. (2006) Population genetics, phylogeography and speciation of Cystodytes (Ascidiacea) in the western Mediterranean Sea. Biological Journal of the Linnean Society 88, 203–214.
Crossref | GoogleScholarGoogle Scholar | open url image1

McGovern T. M., Hellberg M. E. (2003) Cryptic species, cryptic endosymbionts, and geographical variation in chemical defences in the bryozoan Bugula neritina. Molecular Ecology 12, 1207–1215.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Metz E. C., Robles-Sikisaka R., Vacquier V. D. (1998) Nonsynonymous substitution in abalone sperm fertilization genes exceeds substitution in introns and mitochondrial DNA. Evolution 95, 10676–10681. open url image1

Millar R. H. (1953) On a collection of ascidians from the Gold Coast. Proceedings of the Zoological Society of London 123, 277–325. open url image1

Millar R. H. (1970). ‘British Ascidians. Synopses of the British Fauna.’ (The Linnean society of London, Academic Press: London, UK.)

Monniot C. (1970) Sur quatre ascidies rares ou mal connues des côtes de la Manche. Cahiers de Biologie Marine XI, 145–152. open url image1

Monniot F. (1988) Ascidies de Nouvelle-Calédonie V. Polycitoridae du lagon. Bulletin du Muséum national d'Histoire naturelle de Paris 10, 197–235. open url image1

Monniot C. (1997) Les genres Archidistoma et Clavelina (Ascidiacea, Clavelinidae) dans le canal du Mozambique. Zoosystema 19, 193–209. open url image1

Monniot C., Monniot F., and Laboute P. (1991). ‘Coral Reef Ascidians of New Caledonia.’ (ORSTOM: Paris, France.)

Monniot F., Monniot C. (1996) New collections of ascidians from the Western Pacific and Southeastern Asia. Micronesica 29, 133–279. open url image1

Nikula R., Väinölä R. (2003) Phylogeography of Cerastoderma glaucum (Bivalvia: Cardiidae) across Europe: a major break in the Eastern Mediterranen. Marine Biology 143, 339–350.
Crossref | GoogleScholarGoogle Scholar | open url image1

Pérès J. M. (1953) Remarques systématiques et biologiques sur deux espèces de Clavelinidae (Ascidiacea, Aplousobranchiata) de la région de Marseille. Reccueil des Travaux de la Station marine d’Endoume 9, 67–71. open url image1

Posada D., Crandall K. A. (1998) MODELTEST: testing the model of DNA substitution. Bioinformatics 14, 817–818.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Ramos A. A., Turon X., Wahl M., Banaigs B., Lafargue F. (1991) The littoral ascidians of the Spanish Mediterranean. II. Balearic Islands. Vie et Milieu 41, 153–163. open url image1

Sabbadin A. (1982) Formal genetics of ascidians. American Zoologist 22, 765–773. open url image1

Sanamyan K. (2002). Zoobase 2.30. Ascidians. Available online at http://lithopssoft.com/zoo [Accessed November 2006]

Söller R., Warnke K., Saint-Paul U., Blohm D. (2000) Sequence divergence of mitochondrial DNA indicates cryptic biodiversity in Octopus vulgaris and supports the taxonomic distinctiveness of Octopus mimus (Cephalopoda: Octopodidae). Marine Biology 136, 29–35.
Crossref | GoogleScholarGoogle Scholar | open url image1

Swofford D. L. (2002). ‘PAUP*, Phylogenetic Analysis Using Parsimony (*and Other Methods).’ Version 4. (Sinauer Associates: Sunderland, MA, USA.)

Tarjuelo I., Posada D., Crandall K. A., Pascual M., Turon X. (2001) Cryptic species of Clavelina (Ascidiacea) in two different habitats: harbours and rocky littoral zones in the northwestern Mediterranean. Marine Biology 139, 455–462.
Crossref | GoogleScholarGoogle Scholar | open url image1

Tarjuelo I., Posada D., Crandall K. A., Pascual M. (2004) Phylogeography and speciation of colour morphs in the colonial ascidian Pseudodistoma crucigaster. Molecular Ecology 13, 3125–3136.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Trason W. B. (1963) The life cycle and affinities of the colonial ascidian Pycnoclavella stanleyi. University of California Publications in Zoology 65, 283–326. open url image1

Turon X. (1987). Estudio de las ascidias de las costas de Cataluña e Islas Baleares. Ph.D. Thesis, University of Barcelona, Spain.

Turon X. (1988) The ascidians of Tossa de Mar (NE Spain). II. - Biological cycles of the colonial species. Cahiers de Biologie Marine 29, 407–418. open url image1

Turon X. (2005) A new mode of colony multiplication by modified budding in the ascidian Clavelina gemmae n. sp. (Clavelinidae). Invertebrate Biology 124, 273–283.
Crossref | GoogleScholarGoogle Scholar | open url image1

Turon X., López-Legentil S. (2004) Ascidian molecular phylogeny inferred from mtDNA data with emphasis on Aplousobranchiata. Molecular Phylogenetics and Evolution 33, 309–320.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Turon X., Tarjuelo I., Duran S., Pascual M. (2003) Characterising invasion processes with genetic data: an Atlantic clade of Clavelina lepadiformis (Ascidiacea) introduced into Mediterranean harbours. Hydrobiologia 503, 29–35.
Crossref | GoogleScholarGoogle Scholar | open url image1

Yund P. O., O’Neil P. G. (2000) Microgeographic genetic differentiation in a colonial ascidian (Botryllus schlosseri) population. Marine Biology 137, 583–588.
Crossref | GoogleScholarGoogle Scholar | open url image1