ISSN 00963925, Moscow University Biological Sciences Bulletin, 2010, Vol. 65, No. 4, pp. 164–166. © Allerton Press, Inc., 2010. Original Russian Text © I.A. Kaygorodova, 2010, published in Vestnik Moskovskogo Universiteta. Biologiya, 2010, No. 4, pp. 39–41.
Molecular Phylogeny and Systematics of Oligochaeta: Pro et Contra I. A. Kaygorodova Limnological Institute, Siberian Branch, Russian Academy of Sciences, Irkutsk, 664033 Russia email:
[email protected] Received April 15, 2010
Abstract—The systematics of oligochaete worms was discussed by experts for the entire 20th century. The development of computing and molecular techniques hold promise for the construction of a phylogenetically reasonable system. However, the eliminating of some paraphyletic lineages did not result in unanimous approval among a wide range of biologists (mainly morphologists and ecologists). Molecular systematics has helped clear up the position of many controversial species and genera, while causing doubts about the classi fication of higher rank taxa, which seemed to be logical and stable until recently. Keywords: molecular phylogeny, systematics, Oligochaeta. DOI: 10.3103/S0096392510040115
Oligochaete worms (Oligochaeta) belong to the Clitellata, which include three other groups of leech like worms: Acanthobdellea, Branchiobdellea, and Hirudinea. About 1700 oligochaete species inhabit seas, estuaries, and fresh reservoirs, being the main faunal element of benthic communities, and nearly 3300 species occur in terrestrial environs. The mono phyly of earthworms (Megadrili) is not doubtful and is supported by both morphological and molecular data. The phylogenetic relationships within the group Microdrili (aquatic worms) in contrast have been widely discussed during the 150year history of their study. Since the middle of the 1990s with the develop ment of the new and more effective methods of molec ular analysis (sequencing and DNA analysis) that rev olutionized systematics, interest in the controversial issues of Oligochaeta systematics has risen again. Cur rent molecular systematics has not defined the final answers to many questions on the phylogeny of aquatic oligochaetes, but now there is a chance to review the first steps toward reconstructing a phyloge netically based system for this group. Position of Oligochaeta in Clitellata The classical school [1–3] accepted the polyphyl etic origin of oligochaetes from polychaetes, recogniz ing three independent lineages, now called Megadrili, Lumbriculata, and Tubificata (Table 1). Moreover, it was thought that sister groups of parasitic clitellates originated from Haplotaxida [2] or Lumbriculida [1] or are a parallel branch to oligochaetes [3]. Molecular genetic studies confirmed the hypothe sis of an oligochaete ancestor of leechlike worms
(Hirudinea, Acanthobdellea, and Branchiobdellea) and brought the group out of Lumbriculida [4–7]. The Oligochaeta group appeared to be paraphyletic. This fact led researchers to state the synonymy of Clitellata and Oligochaeta following the rules of modern zoo logical nomenclature [5, 6, and others], which com plicates the higher systematics of the group as a whole. However, due to the ongoing phylogenetic reassess ment of Clitellata is still opened. Relationships between Oligochaeta Families Traditionally, aquatic Oligochaeta included nine families: Alluroidae, Lumbriculidae, Enchytraeidae, Haplotaxidae, Naididae, Opistocystidae, Phreodril idae, Tubificidae, and Aelosomatidae [3]. Later, Narapidae, Propappidae, Dorydrilidae, Capilloven tridae, and Randellidae were added, while Aelosoma tidae were moved to Polychaeta. Recent studies using 18S rDNA have demonstrated the close relationship between Enchytraeidae and Crassiclitellata [6–8], which are taxa dominated by soil species. These two lineages form a clade, which is a derivative of aquatic oligochaetes, disproving the recent hypothesis of a ter restrial ancestor of the Clitellata [9]. Molecular data confirm the position of Naididae within Tubificidae and the position of Phreodrilidae close to but outside of Tubificidae [10]. The recently discovered marine worms Capilloventridae is a sister group with regard to other Clitellata [10]. The group Naididae is paraphyletic, while it includes the species of the genus Pristina [11]. Relying on the molecular phylogeny, Erseus et al. [10] hastened to combine Tubificidae and Naididae into one family without tak
164
MOLECULAR PHYLOGENY AND SYSTEMATICS OF OLIGOCHAETA
165
Modern classification of oligochaetes (in brief) Classis
Subclassis
Superodo
Ordo
Familia Ocnerodrildae Eudrilidae
CRASSICLITELLATA
–
Glossoscolecidae Lumbricidae
MEGADRILI
Megascolecidae DIPLOTESTICULATA
OLIGOCHAETA LUMBRICULATA
Haplotaxida
Haplotaxidae
Opisthopora
Alluroididae
Moniligastrida
Moniligastridae
Lumbriculida
Lumbriculidae Enchytraeidae Capilloventridae
Enchytraeida MICRODRILI
Propappidae
TUBIFICATA
Naididae Phreodrilidae
Tubificida
Tubificidae
ing into account their ecological and morphological peculiarities. In our opinion, all problems with Naid idae can be solved by assigning Pristininae as a family within Tubificida equal with Naididae, Phreodrilidae, and Tubificidae. The Opistocystidae family combines mostly neo tropical species. Its status has never been disputed. However, 12S, 16S, and 18S rDNA analyses have shown that Opistocystidae cluster within Naididae and are closely related to Pristininae, which probably will influence their taxonomic position [12]. Some Controversial Species The disputed status of several species belonging to the Lumbriculidae family has recently been success fully resolved. Phylogenetic studies based on morpho logical characters, 18S rDNA, and COI revalidated the status of the independent genus Pseudorhynchelmis to the group of Baikal species [4, 13–15], as was intu itively assumed by some morphologists [16, 17]. The systematic belonging of the taxa of three genera, Lam prodrilus, Teleuscolex, and Agriodrilus, has not been unanimously accepted. For example, Cook [18] con sidered them to be single genus. Molecular data have showed that the formation of the large Lamprodrilus group occurred relatively recently as the result of the Baikal “burst of speciation” [14, 15, 19]. Neverthe less, differences in the structure of the genitals (a tax onomically significant feature) do not allow combin ing them into one genus.
Moreover, due to 16S rDNA and COI it has been determined that the widespread and morphologically highly variable oligochaetes Tubifex tubifex and Lum briculus variegatus, which are used as marker and model organisms in ecology and toxicology, are com plexes of cryptic species [20–22]. CONCLUSIONS The overview of molecular phylogenetic studies has shown that despite the successful solution of some controversial points in the Lumbriculidae family and the identification of at least two complexes of cryptic species there are many unsolved key questions in the taxonomy of aquatic oligochaetes, such as the group ing of families in orders, the paraphyly of higher rank taxa and the origin of the group as a whole. REFERENCES 1. Michaelsen, W., Zur Stammesgeschichte der Oligocha eten, Zeitschr. Wiss. Zool., 1929, vol. 134, pp. 693–716. 2. Livanow, N., Die Organization der Hirudineen und die Beziehungen die Beziehungen Dieser Gruppe zu den Oligochaeten, Ergeb. Fortschritte Zool., 1931, vol. 7, pp. 387–484. 3. Chekanovskaya, O.V., Vodnye maloshchetinkovye chervi fauny SSSR (Aquatic Oligochaetes of the Fauna of the USSR), Moscow: Akad. Nauk SSSR, 1962. 4. Martin, P., Kaygorodova, I., Sherbakov, D., and Ver heyen, E., Rapidly Evolving Lineages Impede the Res olution of Phylogenetic Relationships among Clitellata
MOSCOW UNIVERSITY BIOLOGICAL SCIENCES BULLETIN
Vol. 65
No. 4
2010
166
5. 6.
7.
8. 9. 10.
11.
12.
13.
KAYGORODOVA (Annelida), Mol. Phylogenet. Evol., 2000, vol. 15, pp. 355–368. Martin, P., On the Origin of the Hirudinea and the Demise of the Oligochaeta, Proc. R. Soc. Lond. B, 2001, vol. 268, pp. 1089–1098. Siddall, M., Apakupakul, K., Burreson, E., Coates, K., Erseus, C., Kallersjo, M., Gelder, S., and Trapido Rosenthal, H., Validating Livanow: Molecular Data Agree That Leeches, Branchiobdellidans and Acanthob della peledina Are a Monophyletic Group of Oligocha etes, Mol. Phylogenet. Evol., 2001, vol. 21, pp. 346–351. Kaygorodova, I.A. and Shcherbakov, D.Yu., Molecular Phylogenetic Study of the Systematic Position of Baikalian Oligochaetes in Clitellata, Genetika, 2006, vol. 42, no. 12, pp. 1647–1655 [Russ. J. Genet. (Eng. Transl.), 2006, vol. 42, no. 12, pp. 1390–1397]. Erseus, C. and Kallersjo, M., 18S rDNA Phylogeny of Clitellata (Anneleda), Zool. Scripta, 2004, vol. 33, pp. 187–196. Purschke, G., Terrestrial Polychaetes—Models for the Evolution of the Clitellata (Annelida)?, Hydrobiologia, 1999, vol. 406, pp. 87–99. Erseus, C., Kallersjo, M., Ekman, M., and Hovmoller, R., 18S rDNA Phylogeny of the Tubificidae (Clitellata) and Its Constituent Taxa: Dismissal of the Naididae, Mol. Phylogenet. Evol., 2002, vol. 22, pp. 414–422. Envall, I., Kallersjo, M., and Erseus, C., Molecular Evidence for the NinMonophyletic Status of Naidinae (Annelida, Clitellata, Tubificidae), Mol. Phylogenet. Evol., 2006, vol. 40, no. (2), pp. 570–584. Erseus, C., Envall, I., Marchese, M., and Gustavsson, L., The Systematic Position of Opistocys tidae (Annelida, Clitellata) Revealed by DNA Data, Mol. Phylogenet. Evol., 2010, vol. 54, no. (1), pp. 309– 313. Kaygorodova, I. and Liventseva, V., A Test of Mono phyly of the Genus Rhynchelmis hoffmeister, 1843 (Oli gochaeta, Lumbriculidae): Morphology Based Phylog eny, Investigated in Russia, 2007, vol. 139e, pp. 1517– 1527.
14. Kaygorodova, I.A., MolecularPhylogenetic Study of the Evolutionary History of Baikalian Lumbriculidae (Oligochaeta, Annelida), Extended Abstract of Cand. Sci. (Biol.) Dissertation, Novosibirsk: Inst. Tsitol. Genet., 2000. 15. Kaygorodova, I., Sherbakov, D., and Martin, P., Molecular Phylogeny of Baikalian Lumbriculidae (Oli gochaeta): Evidence for Recent Explosive Speciation, Comp. Cytogenet., 2007, vol. 1, no. 1, pp. 71–84. 16. Hrabe, S., Contribution to the Knowledge of Oligocha eta from the Lake Baikal, Verst. cs. Spolec. Zool., 1982, vol. 46, pp. 174–193. 17. Martin, P., Ferraguti, M., and Kaygorodova, I., Description of Two Species of Rhynchelmis (Oligocha eta: Lumbriculidae) from Lake Baikal (Russia), using Classical Morphology and Ultrastructure of Spermato zoa, Ann. Limnol., 1998, vol. 34, no. 3, pp. 283–293. 18. Cook, D.G., Family Lumbriculidae, in Aquatic Oli gochaeta of the World, Brinkhurst, O.R. and Jamieson, B.G.M., Eds., Edinburgh: Oliver and Boyd, 1971, pp. 200–285. 19. Kaygorodova, I.A. and Liventseva, V.G., Molecular Phylogeny of the Baikalian Bundle of Lamrrodrilus Species (Oligochaeta, Lumbriculidae), Izv. IGU, 2008, vol. 1, no. 2, pp. 52–55. 20. Sturmbauer, C., Opadiya, G., Niederstatter, H., Ried mann, A., and Dallinger, R., Mitochondrial DNA Reveals Cryptic Oligochaete Species Differing in Cad mium Resistance, Mol. Biol. Evol., 1999, vol. 16, pp. 967–974. 21. Beauchamp, K., Kathman, R., McDowell, T., and Hedrick, R., Molecular Phylogeny of Tubificid Oli gochaetes with Special Emphasis in Tubifex tubifex (Tubificidae), Mol. Phylogenet. Evol., 2001, vol. 19, pp. 216–224. 22. Gustafsson, D.R., Price, D.A., and Erseus, C., Genetic Variation in the Popular Lab Worm Lumbriculus varie gates (Annelida: Clitellata: Lumbriculidae) Reveals Cryptic Speciation, Mol. Phylogenet. Evol., 2009, vol. 51, no. 2, pp. 182–189.
MOSCOW UNIVERSITY BIOLOGICAL SCIENCES BULLETIN
Vol. 65
No. 4
2010
