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

Phylogenetic analysis of oligochaete Tubificinae (Annelida : Clitellata) based on mitochondrial sequence data

Ainara Achurra A C , M. Arantzazu Elejalde B and Pilar Rodriguez A
+ Author Affiliations
- Author Affiliations

A Department of Zoology and Animal Cell Biology, Faculty of Science and Technology, University of the Basque Country UPV/EHU, Apdo. 644, Bilbao 48080, Spain.

B Department of Invertebrates, Royal Belgian Institute of Natural Sciences, Vautierstraat 29, B-1000 Brussels, Belgium.

C Corresponding author. Email: ainara.achurra@ehu.es

Invertebrate Systematics 25(3) 208-218 https://doi.org/10.1071/IS10040
Submitted: 13 December 2010  Accepted: 14 September 2011   Published: 18 November 2011

Abstract

Partial sequences of the mitochondrial genes 16S rRNA and cytochrome c oxidase subunit I (COI) were used (1) to resolve the internal relationships of the subfamily Tubificinae (Annelida : Clitellata) and (2) to test the existence of cryptic species within the stygobiont oligochaete Troglodrilus galarzai (Giani & Rodriguez, 1988). Phylogenies were estimated using maximum likelihood, Bayesian inference and parsimony. Although trees were incompletely resolved at intergeneric level, a close relationship between Heterochaeta Claparède, 1863 and Troglodrilus Juget, des Châtelliers & Rodriguez was revealed, and the separation of Lophochaeta ignota Štolc, 1886 and Heterochaeta costata Claparède, 1863 from Tubifex Lamarck, 1816 was corroborated by mitochondrial molecular data. Maximum genetic divergence between allopatric populations of T. galarzai was 18% for COI (uncorrected pairwise distance), suggesting cryptic speciation within this nominal species.


References

Beauchamp, K. A., Kathman, R. D., McDowell, T. S., and Hedrick, R. P. (2001). Molecular phylogeny of tubificid oligochaete with special emphasis on Tubifex tubifex (Tubificidae). Molecular Phylogenetics and Evolution 19, 216–224.
Molecular phylogeny of tubificid oligochaete with special emphasis on Tubifex tubifex (Tubificidae).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXjt1GmsL8%3D&md5=e87dd36b2f8782867b1b91d8a93e7706CAS |

Bely, A. E., and Wray, G. A. (2004). Molecular phylogeny of naidid worms (Annelida: Clitellata) based on cytochrome oxidase I. Molecular Phylogenetics and Evolution 30, 50–63.
Molecular phylogeny of naidid worms (Annelida: Clitellata) based on cytochrome oxidase I.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXpt1Sis7c%3D&md5=0a90df615a8d1666b5e126482ac2f1e9CAS |

Brinkhurst, R. O. (1991). A phylogenetic analysis of the Tubificinae (Annelida, Oligochaeta). Canadian Journal of Zoology 69, 392–397.
A phylogenetic analysis of the Tubificinae (Annelida, Oligochaeta).Crossref | GoogleScholarGoogle Scholar |

Brinkhurst, R. O., and Jamieson, B. G. M. (1971). ‘Aquatic Oligochaeta of the World.’ (University of Toronto Press: Toronto, ON.)

Crottini, A., Marotta, R., Barbuto, M., Casiraghi, M., and Ferraguti, M. (2008). The world in a river? A preliminary analysis of the 16S rDNA variability of Tubifex species (Clitellata: Tubificidae) from the Lambro River. Molecular Phylogenetics and Evolution 48, 1189–1203.
The world in a river? A preliminary analysis of the 16S rDNA variability of Tubifex species (Clitellata: Tubificidae) from the Lambro River.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtVyntL7P&md5=e5fa28831d978c21a6de7c650bfcef64CAS |

Des Châtelliers, M. C., Juget, J., Lafont, M., and Martin, P. (2009). Subterranean aquatic Oligochaeta. Freshwater Biology 54, 678–690.
Subterranean aquatic Oligochaeta.Crossref | GoogleScholarGoogle Scholar |

Dzwillo, M. (1984). Phylogenetic and taxonomic problems in freshwater Oligochaeta with special emphasis on chitinous structures in Tubificinae. Hydrobiologia 115, 19–23.
Phylogenetic and taxonomic problems in freshwater Oligochaeta with special emphasis on chitinous structures in Tubificinae.Crossref | GoogleScholarGoogle Scholar |

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 | 1:CAS:528:DC%2BD2cXisF2ks7w%3D&md5=3e859bb18f8df064e5a4e423e95f0114CAS |

Envall, I., Källersjö, M., and Erséus, C. (2006). Molecular evidence for the non-monophyletic status of Naidinae (Annelida, Clitellata, Tubificidae). Molecular Phylogenetics and Evolution 40, 570–584.
Molecular evidence for the non-monophyletic status of Naidinae (Annelida, Clitellata, Tubificidae).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XntFWqsb0%3D&md5=cd364ebf79c9a2f14dbcb44734ea001aCAS |

Erséus, C. (1989). Four new West Atlantic species of Tubificoides (Oligochaeta, Tubificidae). Proceedings of the Biological Society of Washington 102, 878–886.

Erséus, C. (1990). Cladistic analysis of the subfamilies within the Tubificidae (Oligochaeta). Zoologica Scripta 19, 57–63.
Cladistic analysis of the subfamilies within the Tubificidae (Oligochaeta).Crossref | GoogleScholarGoogle Scholar |

Erséus, C., and Gustafsson, D. (2009). Cryptic specitation in clitellate model organisms. In ‘Annelids in Modern Biology’. (Ed. Dan Shain) pp. 31–46. (Wiley–Blackwell: Hoboken, NJ.)

Erséus, C., and Kvist, S. (2007). COI variation in Scandinavian marine species of Tubificoides (Annelida: Clitellata: Tubificidae). Journal of the Marine Biological Association of the United Kingdom 87, 1121–1126.
COI variation in Scandinavian marine species of Tubificoides (Annelida: Clitellata: Tubificidae).Crossref | GoogleScholarGoogle Scholar |

Ferraguti, M., and Ruprecht, D. (1992). The double sperm line in Clitellio arenarius (Annelida, Oligochaeta, Tubificinae). The Italian Journal of Zoology 59, 349–362.

Finogenova, N. P., and Poddubnaja, T. L. (1990). One more revision of the genus Potamothrix Vejdovský et Mrázek, 1902 (Oligochaeta, Tubificidae). Zoologische Jahrbucher. Abteilung fur Systematik, Ökologie und Geographie der Tiere 117, 55–83.

Folmer, O., Black, M., Hoeh, W., Lutz, R., and 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.
| 1:CAS:528:DyaK2MXjt12gtLs%3D&md5=002ef50a594fc86f823ca8ae866828c6CAS |

Giani, N., and Rodriguez, P. (1988). Description de quelques especes nouvelles de Tubificidae (Oligochaeta) de grottes et de sources karstiques de la peninsule iberique. Stygologia 4, 121–137.

Giani, N., Martinez-Ansemil, E., and Brinkhurst, R. O. (1984). Revision du statut taxonomique des Aulodrilinae (Tubificidae, Oligochaeta). Bulletin de la Société d’Histoire Naturelle de Toulouse 120, 17–22.

Gustafsson, D. R., Price, D. A., and Erséus, C. (2009). Genetic variation in the popular lab worm Lumbriculus variegatus (Annelida: Clitellata: Lumbriculidae) reveals cryptic speciation. Molecular Phylogenetics and Evolution 51, 182–189.
Genetic variation in the popular lab worm Lumbriculus variegatus (Annelida: Clitellata: Lumbriculidae) reveals cryptic speciation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXltFemtLc%3D&md5=0d4f7f85cf967d8b7ee2ee67ba3cef0dCAS |

Gustavsson, L. M. (1995). Morphological investigation of the tubificid Clitellio arenarius (Annelida, Oligochaeta). Sarsia 80, 159–171.

Halanych, K. M., and Janosik, A. M. (2006). A review of molecular markers used for Annelid phylogenetics. Integrative and Comparative Biology 46, 533–543.
A review of molecular markers used for Annelid phylogenetics.Crossref | GoogleScholarGoogle Scholar |

Holmquist, C. (1985). A revision of the genera Tubifex Lamarck, Ilyodrilus Eisen, and Potamothrix Vejdovsky & Mrazek (Oligochaeta, Tubificidae) with extensions to some connected genera. Zoologischer Jahrbücher. Abteilung für Systematik 112, 311–366.

Juget, J., des Chatelliers, M., and Rodriguez, P. (2006). Troglodrilus (Annelida, Oligochaeta, Tubificidae), a new genus from subterranean habitats in southwestern Europe. Hydrobiologia 564, 7–17.
Troglodrilus (Annelida, Oligochaeta, Tubificidae), a new genus from subterranean habitats in southwestern Europe.Crossref | GoogleScholarGoogle Scholar |

Källersjö, M., Albert, V. A., and Farris, J. S. (1999). Homoplasy increases phylogenetic structure. Cladistics 15, 91–93.
Homoplasy increases phylogenetic structure.Crossref | GoogleScholarGoogle Scholar |

Kennedy, C. R. (1969). The variability of some characters used for species recognition in the genus Limnodrilus Claparède (Oligochaeta: Tubificidae). Journal of Natural History 3, 53–60.
The variability of some characters used for species recognition in the genus Limnodrilus Claparède (Oligochaeta: Tubificidae).Crossref | GoogleScholarGoogle Scholar |

Lefébure, T., Douady, C. J., Gouy, M., and Gibert, J. (2006). Relationship between morphological taxonomy and molecular divergence within Crustacea: proposal of a molecular threshold to help species delimitation. Molecular Phylogenetics and Evolution 40, 435–447.
Relationship between morphological taxonomy and molecular divergence within Crustacea: proposal of a molecular threshold to help species delimitation.Crossref | GoogleScholarGoogle Scholar |

Marotta, R., Ferraguti, M., Erséus, C., and Gustavsson, L. M. (2008). Combined-data phylogenetics and character evolution of Clitellata (Annelida) using 18S rDNA and morphology. Zoological Journal of the Linnean Society 154, 1–26.
Combined-data phylogenetics and character evolution of Clitellata (Annelida) using 18S rDNA and morphology.Crossref | GoogleScholarGoogle Scholar |

Martin, P., Martinez-Ansemil, E., and Sambugar, B. (2010). The Baikalian genus Rhyacodriloides in Europe: phylogenetic assessment of Rhyacodriloidinae subfam. N. within the Naididae (Annelida). Zoologica Scripta 39, 462–482.
The Baikalian genus Rhyacodriloides in Europe: phylogenetic assessment of Rhyacodriloidinae subfam. N. within the Naididae (Annelida).Crossref | GoogleScholarGoogle Scholar |

Milinkovitch, M. C., LeDuc, R. G., Adachi, J., Farnir, F., Georges, M., and Hasegawa, M. (1996). Effects of character weighting and species sampling on phylogeny reconstruction: a case study based on DNA sequence data in cetaceans. Genetics 144, 1817–1833.
| 1:CAS:528:DyaK2sXkslymtQ%3D%3D&md5=83bf7417f388138418ef36da6daff90cCAS |

Nylander, J. A. A. (2004). MrModeltest v2. Program distributed by the author. (Evolutionary Biology Centre, Uppsala University: Uppsala.) Available at http://www.abc.se/~nylander/ [verified September 2011]

Nylander, J. A. A., Erséus, C., and Källersjö, M. (1999). A test of monophyly of the gutless Phallodrilinae (Oligochaeta, Tubificidae) and the use of a 573 bp region of the mitochondrial cytochrome oxidase I gene in analysis of annelid phylogeny. Zoologica Scripta 28, 305–313.
A test of monophyly of the gutless Phallodrilinae (Oligochaeta, Tubificidae) and the use of a 573 bp region of the mitochondrial cytochrome oxidase I gene in analysis of annelid phylogeny.Crossref | GoogleScholarGoogle Scholar |

Palumbi, S. R., Martin, A., Romano, S., McMillan, W. O., Stice, L., and Grabowski, G. (1991). ‘A Simple Fool’s Guide to PCR.’ (University of Hawaii Press: Honolulu, HI.)

Pinder, A. M., Eberhard, S. M., and Humphreys, W. F. (2006). New phallodrilines (Annelida: Clitellata: Tubificidae) from Western Australian groundwater. Zootaxa 1304, 31–48.

Rambaut, A., and Drummond, A. J. (2004). Tracer.Version 1.3. Available at http://tree.bio.ed.ac.uk/software/tracer/ [verified September 2011]

Rodriguez, P., and Achurra, A. (2011). New species of aquatic oligochaetes (Annelida: Clitellata) from groundwaters in karstic areas of northern Spain, with taxonomic remarks on Lophochaeta ignota. Zootaxa 2332, 21–39.

Rodriguez, P., and Giani, N. (1984). Description de Varichaetadrilus bizkaiensis n. sp.; nouvelle espèce de Tubificidae (Oligochaeta) d’Espagne. Bulletin de la Société d’Histoire Naturelle de Toulouse 120, 127–130.

Ronquist, F., and Huelsenbeck, J. P. (2003). MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 20, 289–290.

Sambugar, B., Giani, N., and Martínez-Ansemil, E. (1999). Groundwater oligochaetes from southern-Europe. Tubificidae with marine phyletic affinities: new data with description of a new species, review and consideration on their origin. Memoires de Biospeologie XXVI, 107–116.

Shih, H. T., Kamrani, E., Davie, P. J. F., and Liu, M. Y. (2009). Genetic evidence for the recognition of two fiddler crabs, Uca iranica and U. albimana (Crustacea: Brachyura: Ocypodidae), from the northwestern Indian Ocean, with notes on the U. lactea species-complex. Hydrobiologia 635, 373–382.
Genetic evidence for the recognition of two fiddler crabs, Uca iranica and U. albimana (Crustacea: Brachyura: Ocypodidae), from the northwestern Indian Ocean, with notes on the U. lactea species-complex.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXht1Cqur3O&md5=fe492156665a610d0c249672e865bb94CAS |

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 |

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

Thompson, J. D., Gibson, T. J., Plewniak, F., Jeanmougin, F., and Higgins, D. G. (1997). The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Research 25, 4876–4882.
The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXntFyntQ%3D%3D&md5=b3c19ca156212ce20ae590d505087c8cCAS |

Xia, X., and Xie, Z. (2001). DAMBE: Data analysis in molecular biology and evolution. The Journal of Heredity 92, 371–373.
DAMBE: Data analysis in molecular biology and evolution.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3MvptlagtA%3D%3D&md5=a28d4f20effdcf6a6261b695c5a4854fCAS |

Zhou, H., Fend, S. V., Gustafson, D. L., De Wit, P., and Erséus, C. (2010). Molecular phylogeny of Neartic species of Rhynchelmis (Annelida). Zoologica Scripta 39, 378–393.
Molecular phylogeny of Neartic species of Rhynchelmis (Annelida).Crossref | GoogleScholarGoogle Scholar |