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Soil-Dwelling Polychaetes: Enigmatic As Ever? Some Hints on Their

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Soil-Dwelling Polychaetes: Enigmatic As Ever? Some Hints on Their Contributions to Zoology, 70 (3) 127-138 (2001) SPB Academic Publishing bv, The Hague Soil-dwelling polychaetes: enigmatic as ever? Some hints on their phylogenetic relationships as suggested by a maximum parsimony analysis of 18S rRNA gene sequences ³ Emilia Rota Patrick Martin² & Christer Erséus ¹, 1 di Dipartimento Biologia Evolutivei. Universitd di Siena, via P. A. Mattioli 4. IT-53100 Siena, Italy, e-mail: 2 Institut des Sciences naturelles de des [email protected]; royal Belgique, Biologic Eaux donees, 29 rue Vautier, B-1000 e-mail: 3 Bruxelles, Belgium, [email protected]; Department of Invertebrate Zoology, Swedish Museum of Natural History, Box 50007, SE-104 05 Stockholm, Sweden, e-mail: [email protected] Keywords: Terrestrial Polychaeta, Parergodrilus heideri, Stygocapitella subterranea, Hrabeiella I8S rRNA periglandulata, gene, molecular phylogeny, rapid radiation Abstract Collectionof new specimens 130 DNA extraction, amplification and sequencing 130 Alignment To re-evaluate 130 the various hypotheses on the systematic position of Phylogenetic analyses 130 Parergodrilus heideri Reisinger, 1925 and Hrabeiella Results 132 periglandulata Pizl & Chalupský, 1984,the sole truly terrestrial Discussion 132 non-clitellateannelidsknown to date, their phylogenetic relation- ships Acknowledgements 136 were investigated using a data set of new 18S rDNA References 136 of sequences these and other five relevant annelid taxa, including an unknown of species Ctenodrilidae, as well as homologous sequences available for 18 already polychaetes, one aphano- neuran, 11 clitellates, two pogonophorans, one echiuran, one Introduction sipunculan, three molluscs and two arthropods. Two different alignments were constructed, according to analgorithmic method terrestrial forms constitute (Clustal Truly a tiny minority W) and on the basis of a secondary structure model non-clitellate annelids, (DCSE), A maximum parsimony analysis was performed with among only represented by arthropods asan unambiguous outgroup. With both alignments, Parergodrilus heideri Reisinger. 1925 and Hra- the resulting topology confirms the validity of groupingP. heideri beiella Pizl & periglandulata Chalupsky, 1984 over and Stygocapitella subterranea Knöllner, 1934 into the family a total of 12,000 species (estimate of described Parergodrilidae. Hrabeiellaperiglandulatanever clusters with them ‘Polychaeta’ acc. to K. Fauchald, in Minelli, 1993). and itsposition relative to this and other polychaete fami- lies is This and their unorthodox still obscure, but a close relationship with aphanoneurans disproportion morphol- is suggested the most trees. All these have caused these two to be by parsimonious taxa appear ogy worms omitted to be far fromthe Clitellata. Most relationships polychaetes from the among most zoology textbooks. In case of P. ar e not supported by significant bootstrap and Bremer values. 75 heideri, known years ago, such an omis- These already polytomies are corroborated by independent evidence sion is also and partly explained by its ever ambigu- are interpreted as from ancient and resulting an emergence a ous Rouse & Fauchald rapid radiation ofPolychaeta. phylogenetic position. (1997: 141) recently stated: “The morphological simplic- ity and the lack of essential information for this Contents group [the Parergodrilidae] mean that their place- ment is unresolvable at present”. Indeed, owing to Abstract their unusual habitat (inland 127 soils, mainly in for- Introduction 127 ests), restricted biogeography (middle Europe) and Material and methods 129 meiofaunal body dimensions (1-2 mm, with 8 to Selection oftaxa 129 14 chaetigerous segments), the biology and mor- is the of paper dedicatedto memory Professor Tor Gustav Karling, 1909-98 128 E. Rota, P. Martin & C. Erseus - Phytogeny of soil-dwelling polychaetes the phology of these two taxa were rarely elaborated sistency in supposedly typical ‘archiannelid’ first-hand by polychaete specialists. The bulk of characters {Stygocapitella has an internal nerve cord, information was instead produced and discussed well developed circular muscles, no locomotory terricolous ciliation of and no adhesive by students of different worm groups. epidermis, pygidial of the Erich Reisinger, a specialist of terrestrial flat- glands) precluded a close relationship two first discovered P. heideri in beech for- thus concluded that worms, taxa. Karling Stygocapitella should indeed be the ests in Stciermark, Austria. Reisinger (1925, 1929) placed among Polychaeta in initially assigned this worm (erroneously interpreted Sedentaria Drilomorpha (which Hatschek’s sys- the as hermaphroditic) to a monotypic family (Parergo- tem included Cirratulidae, Arenicolidae, drilidae) in the Archiannelida, suborder “Rotatorio- Capitellidae, Maldanidae, Ctenodrilidae and Sterna- but gona”. In the latter, he included the Nerillidae, spidae; see Fauchald & Rouse, 1997), segre- Histriobdellidae and Dinophilidae, which also (fol- gated in a monotypic family, the Stygocapitellidae, lowing Heider, 1922) he considered to be anatomi- close to the Ctenodrilidae and the Capitellidae. cally intermediate between the rotifers and the Whether Parergodhlus should be accommodated annelids. Reisinger’s work was scathingly criticized in the same family Karling left to Reisinger to the by Meyer (1927), who presented a different analysis decide. In meanwhile, Reisinger had discovered of the structure of Parergodrilus suggesting that the males of Parergodrilus and was preparing an of the it is a reduced enchytraeid oligochaete. The worm updated comparative study reproductive 30 of the was not reinvestigated during the following systems two species. Reisinger (1960) ac- but the of authorities (Michaelsen, to years, majority cepted Karling’s suggestion unify Stygocapitel- lidae 1928; Stephenson, 1930; Cernosvitov, 1937; Du and Parergodrilidae but correctly gave prior- Bois-Reymond Marcus, 1948: 8, footnote) favoured ity to the latter name, and the redefined family, Meyer's view. following the dismemberment of the taxon Archian- In the meantime, another minute annelid, Stygo- nelida (Beklemischev, 1958), he now placed un- had been the capitella subterranea Knollner, 1934, der Polychaeta Sedentaria, at an intermediate discovered from littoral subsoil waters in the Kiel level between the Drilomorpha and the Nerillidae. Bay, Germany. In spite of its homonomous seg- Interestingly, in the Grasse volume on Annelida, mentation, the lack of dorsal chaetal bundles and Parergodrilus was ‘for practical reasons’ still re- the aberrant ventral location of its sexual opening, ferred to the archiannelids (Beauchamps, 1959), the it was attributed to polychaete family Capitel- but treated also under the enchytraeids (Avel, 1959). lidae, In 1955, Tor Karling collectedS. subterranea in spite of subsequent research, a more precise has on the coast of Scania, Sweden, and immediately classification of the Parergodrilidae not as yet perceived its intriguing resemblance to P. heideri. been possible. Dales (1962, 1963), in consideration Karling (1958) carried out a detailed anatomical of the structure of the pharyngeal organ, suggested ndn- to study of the two taxa, adding support to the the ‘curious little stygocapitellids’ be an early clilellate nature of Parergodrilus and substantiat- offshoot from the ancestral stock of which the ing its affinities with Stygocapitella. He regarded ‘archiannelids’ of today are specialized survivors. maintainedtheir but the position of S. subterranea in the Capitellidae He position as uncertain some- untenable its how close the and as and pointed out similarity (in gen- to Cirratulidae Ctenodrilidae the order eral appearance, gut anatomy, possession of a car- (the three families were grouped in diac body) with the Ctenodrilidae, although a close Cirratulida). Fauchald (1977), followed by Peltibone kinship with the latter was ruled out because of (1982), George & Hartmann-Schroder (1985) and the exclusively sexual and gonochoristic reproduc- Barnes & Harrison (1992), classified the Cteno- tion drilidae and in the order ofStygocapitella. Karling found even greater Parergodrilidae together of similarities (in segmentation, arrangement me- Ctenodrilida, but, influenced by Wilfcrt (1973), senteries, circulatory system, alimentary canal, male assigned the Cirratulidae to a different order. To and female reproductive organs) with the ‘archian- the Ctenodrilida Fauchald (1977) gave no particu- nelid’ the lack of family Nerillidae, although con- lar position, but recognized them as simple bod- Contributions to Zoology, 70 (3) - 2001 129 in of the animal led forms like those included the Orbiniida, description nor indicated the local- Psammodrilida, Cossurida, Spionida, Capitellida ity of the finding. The species was independently and Opheliida. He refused to group these orders discovered in South Bohemia and thoroughly stud- under the old concept Drilomorpha as “these forms ied by light microscopy by Pizl & Chalupsky (1984). are about as far apart as any other grouping of Contrary to Parergodrilus and Stygocapitella, polychaetes that might be proposed, judging from Hrabeiella has a dorsal pharyngeal organ and is differences in tagmatization, parapodial develop- hermaphroditic, in these respects resembling an its lack ment and setal distribution” (op.cit.: 9). oligochaete. However, of a clitellum and Bunke noted that the ventral its overall of the internal (1967) pharyngeal arrangement organs pre- the annelidPotamodrilus clude the Pizl organ of freshwater flu-
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