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

Placing the forgotten: on the positions of Euenchytraeus and Chamaedrilus in an updated enchytraeid phylogeny (Clitellata : Enchytraeidae)

Svante Martinsson A D , Klára Dózsa-Farkas B , Emilia Rota C and Christer Erséus A
+ Author Affiliations
- Author Affiliations

A Systematics and Biodiversity, Department of Biological and Environmental Sciences, University of Gothenburg, Box 463, SE-405 30 Göteborg, Sweden.

B Eötvös Loránd University, Department of Systematic Zoology and Ecology, H-1117 Budapest, Pázmány Péter sétány 1/C, Hungary.

C Department of Physics, Earth and Environmental Sciences, University of Siena, Via P.A. Mattioli 4, IT-53100 Siena, Italy.

D Corresponding author. Email: svante.martinsson@bioenv.gu.se

Invertebrate Systematics 31(1) 85-90 https://doi.org/10.1071/IS16042
Submitted: 16 May 2016  Accepted: 15 August 2016   Published: 16 March 2017

Abstract

The phylogeny of Enchytraeidae was re-estimated to establish the relationships of the now resurrected Chamaedrilus and Euenchytraeus and to confirm their status as separate taxa. The former Cognettia (Enchytraeidae) was recently revised and split into its two senior synonyms, Chamaedrilus and Euenchytraeus, with the majority of the species transferred to Chamaedrilus. Euenchytraeus was re-established for three species sharing a unique anatomical trait, but has never before been represented in any phylogenetic study. We included representatives from 21 (of 33) valid enchytraeid genera and used three mitochondrial and four nuclear genes. The dataset (4164 base pairs) was analysed using multi-species coalescent (MSC) and maximum likelihood (ML) methods. Chamaedrilus (represented by eight species) and Euenchytraeus (represented by Eu. clarae) were found in a clade together with the monotypic Stercutus. Chamaedrilus was found to be monophyletic with maximum support in both analyses. The ML tree supported Euenchytraeus and Chamaedrilus as sister groups, whereas the MSC tree placed Euenchytraeus together with Stercutus, both with low support. A Bayes factor test weakly supported Euenchytraeus and Chamaedrilus as sister groups over Euenchytraeus + Stercutus. Possible morphological synapomorphies for these genera are discussed, and we conclude that Chamaedrilus and Euenchytraeus are closely related, but their status as separate genera is justified.


References

Anisimova, M., and Gascuel, O. (2006). Approximate likelihood-ratio test for branches: a fast, accurate, and powerful alternative. Systematic Biology 55, 539–552.
Approximate likelihood-ratio test for branches: a fast, accurate, and powerful alternative.Crossref | GoogleScholarGoogle Scholar |

Bauer, R. (1993). Cognettia clarae n. sp. – eine neue Enchytraeiden-Art aus einem österreichischen Fichtenwald (Oligochaeta; Enchytraeidae). Linzer Biologische Beiträge 25, 685–689.

Bretscher, K. (1906). Über ein neues Enchytraeiden genus. Zoologischer Anzeiger 29, 672–674.

Černosvitov, L. (1937). System der Enchytraeiden. Bulletin de l’Association Russe pour les Recherches Scientifiques à Prague (Section des Sciences Naturelles et Matématiques) 5, 263–295.

Christensen, B., and Dózsa-Farkas, K. (1999). The enchytraeid fauna of the Siberian tundra (Oligochaeta, Enchytraeidae). The Royal Danish Academy of Sciences and Letters. Biologiske Skrifter 52, 1–37.

Christensen, B., and Glenner, H. (2010). Molecular phylogeny of Enchytraeidae (Oligochaeta) indicates separate invasions of the terrestrial environment. Journal of Zoological Systematics and Evolutionary Research 48, 208–212.

Degnan, J. H., and Rosenberg, N. A. (2009). Gene tree discordance, phylogenetic inference and the multispecies coalescent. Trends in Ecology & Evolution 24, 332–340.
Gene tree discordance, phylogenetic inference and the multispecies coalescent.Crossref | GoogleScholarGoogle Scholar |

Dózsa-Farkas, K. (1973). Ananeosis, a new phenomenon in the life-history of the enchytraeids (Oligochaeta). Opuscula Zoologica 12, 43–55.

Dózsa-Farkas, K. (2010). Significance of using nephridia in the taxonomy of family Enchytraeidae. Zoology in the Middle East 51(Suppl. 2), 41–53.

Drummond, A. J., Suchard, M. A., Xie, D., and Rambaut, A. (2012). Bayesian phylogenetics with BEAUti and the BEAST 1.7. Molecular Biology and Evolution 29, 1969–1973.
Bayesian phylogenetics with BEAUti and the BEAST 1.7.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtFagu7fO&md5=1128fe2c54a768f2b18bd3a1ecbe3c88CAS |

Erséus, C., Rota, E., Matamoros, L., and De Wit, P. (2010). Molecular phylogeny of Enchytraeidae (Annelida, Clitellata). Molecular Phylogenetics and Evolution 57, 849–858.
Molecular phylogeny of Enchytraeidae (Annelida, Clitellata).Crossref | GoogleScholarGoogle Scholar |

Friend, H. (1913). British enchytraeids. V. Species new to science. Journal of the Royal Microscopical Society 33, 255–271.
British enchytraeids. V. Species new to science.Crossref | GoogleScholarGoogle Scholar |

Guindon, S., Dufayard, J. F., Lefort, V., Anisimova, M., Hordijk, W., and Gascuel, O. (2010a). New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Systematic Biology 59, 307–321.
New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXks1Kms7s%3D&md5=6a4b4bad9d044d087ef5f497493b1c43CAS |

Guindon, S., Dufayard, J. F., Lefort, V., Anisimova, M., Hordijk, W., and Gascuel, O. (2010b). New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Systematic Biology 59, 307–321.
New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXks1Kms7s%3D&md5=6a4b4bad9d044d087ef5f497493b1c43CAS |

Kass, R. E., and Raftery, A. E. (1995). Bayes factors. Journal of the American Statistical Association 90, 773–795.
Bayes factors.Crossref | GoogleScholarGoogle Scholar |

Klinth, M. J., Martinsson, S., and Erséus, C. (2016). Phylogeny and species delimitation of North European Lumbricillus (Clitellata, Enchytraeidae). Zoologica Scripta 46, 96–110.
Phylogeny and species delimitation of North European Lumbricillus (Clitellata, Enchytraeidae).Crossref | GoogleScholarGoogle Scholar |

Martinsson, S., and Erséus, C. (2014). Cryptic diversity in the well-studied terrestrial worm Cognettia sphagnetorum (Clitellata: Enchytraeidae). Pedobiologia 57, 27–35.
Cryptic diversity in the well-studied terrestrial worm Cognettia sphagnetorum (Clitellata: Enchytraeidae).Crossref | GoogleScholarGoogle Scholar |

Martinsson, S., Rota, E., and Erséus, C. (2015a). Revision of Cognettia (Clitellata, Enchytraeidae): re-establishment of Chamaedrilus and description of cryptic species in the sphagnetorum complex. Systematics and Biodiversity 13, 257–277.
Revision of Cognettia (Clitellata, Enchytraeidae): re-establishment of Chamaedrilus and description of cryptic species in the sphagnetorum complex.Crossref | GoogleScholarGoogle Scholar |

Martinsson, S., Rota, E., and Erséus, C. (2015b). On the identity of Chamaedrilus glandulosus (Michaelsen, 1888) (Clitellata, Enchytraeidae), with the description of a new species. ZooKeys 501, 1–14.
On the identity of Chamaedrilus glandulosus (Michaelsen, 1888) (Clitellata, Enchytraeidae), with the description of a new species.Crossref | GoogleScholarGoogle Scholar |

Nielsen, C. O., and Christensen, B. (1959). The Enchytraeidae. Critical revision and taxonomy of European species. Natura Jutlandica 8–9, 1–160.

Piper, S. R., MacLean, S. F., and Christensen, B. (1982). Enchytraeidae (Oligochaeta) from taiga and tundra habitats of northeastern U.S.S.R. Canadian Journal of Zoology 60, 2594–2609.
Enchytraeidae (Oligochaeta) from taiga and tundra habitats of northeastern U.S.S.R.Crossref | GoogleScholarGoogle Scholar |

Rambaut, A. (2014). FigTree v1.4.2. Available from http://tree.bio.ed.ac.uk/software/figtree/ [Accessed 30 November 2015]

Rota, E., Matamoros, L., and Erséus, C. (2008). In search of Marionina (Clitellata, Enchytraeidae): a taxonomic history of the genus and re-description of the type species Pachydrilus georgianus Michaelsen, 1888. The Italian Journal of Zoology 75, 417–436.
In search of Marionina (Clitellata, Enchytraeidae): a taxonomic history of the genus and re-description of the type species Pachydrilus georgianus Michaelsen, 1888.Crossref | GoogleScholarGoogle Scholar |

Rota, E., Martinsson, S., and Erséus, C. (2015). Comment on the proposed precedence of Cognettia Nielsen & Christensen, 1959 over Euenchytraeus Bretscher, 1906 and Chamaedrilus Friend, 1913 (Annelida, Oligochaeta, Enchytraeidae) (Case 3689; see BZN 72: 186–192). Bulletin of Zoological Nomenclature 72, 303–307.

Schmelz, R. M., and Collado, R. (2010). A guide to European terrestrial and freshwater species of Enchytraeidae (Oligochaeta). Soil Organisms 82, 1–176.

Schmelz, R. M., and Collado, R. (2015). Checklist of taxa of Enchytraeidae (Oligochaeta): an update. Soil Organisms 87, 149–153.

Schmelz, R. M., Collado, R., and Rombke, J. (2011). Mata Atlantica enchytraeids (Parana, Brazil): a new genus, Xetadrilus gen. nov., with three new species, and four new species of Guaranidrilus Cernosvitov (Enchytraeidae, Oligochaeta). Zootaxa 2838, 1–29.

Schmelz, R. M., Collado, R., and Römbke, J. (2015). Case 3689: Cognettia Nielsen & Christensen, 1959 (Annelida, Oligochaeta, Enchytraeidae): proposed precedence over Euenchytraeus Bretscher, 1906 and Chamaedrilus Friend, 1913. Bulletin of Zoological Nomenclature 72, 186–192.

Shimodaira, H., and Hasegawa, M. (1999). Multiple comparisons of log-likelihoods with applications to phylogenetic inference. Molecular Biology and Evolution 16, 1114–1116.
Multiple comparisons of log-likelihoods with applications to phylogenetic inference.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXltVyksrg%3D&md5=e7acde88a60fec088f4d94d38a1be8c0CAS |

Vejdovský, F. (1878). Zur anatomie und systematik der enchytraeiden. Sitzungsberichte der Königlich Böhmischen Gesellschaft der Wissenschaften 1877, 294–304.

Xi, Z., Liu, L., Rest, J. S., and Davis, C. C. (2014). Coalescent versus concatenation methods and the placement of Amborella as sister to water lilies. Systematic Biology 63, 919–932.
Coalescent versus concatenation methods and the placement of Amborella as sister to water lilies.Crossref | GoogleScholarGoogle Scholar |

Xie, W., Lewis, P. O., Fan, Y., Kuo, L., and Chen, M. H. (2011). Improving marginal likelihood estimation for Bayesian phylogenetic model selection. Systematic Biology 60, 150–160.
Improving marginal likelihood estimation for Bayesian phylogenetic model selection.Crossref | GoogleScholarGoogle Scholar |