Hydrobiologia 485: 253–256, 2002. © 2002 Kluwer Academic Publishers. Printed in the Netherlands.
253
Short note
A proposal to regard the former family Naididae as a subfamily within Tubificidae (Annelida, Clitellata) Christer Ers´eus & Lena Gustavsson Department of Invertebrate Zoology, Swedish Museum of Natural History, Box 50007, SE-104 05 Stockholm, Sweden E-mail:
[email protected] Received 24 June 2002; accepted 12 July 2002
Key words: Clitellata, Oligochaeta, Tubificidae, Naididae, Naidinae, taxonomy, classification
Abstract Following recent phylogenetic assessments using DNA data, the aquatic oligochaete family Naididae (=Naidina Ehrenberg, 1828) is proposed to be treated as a subfamily, Naidinae, within Tubificidae Vejdovský, 1876. [A complication of this proposal is that the family-group name Naididae is older than Tubificidae, and thus, according to the International Code of Zoological Nomenclature, should have precedence over the latter; this will be dealt with in a separate application to the International Commission of Zoological Nomenclature.] Naidinae appears to be closely related to taxa currently placed in another tubificid subfamily, Rhyacodrilinae, but it is argued that, while Naidinae is likely to be a natural group, Rhyacodrilinae is most probably not, neither with nor without the inclusion of the naidines. It is thus predicted that future revisions will involve splitting of Rhyacodrilinae rather than a drastic change in the circumscription of Naidinae.
Introduction About one-third of the over 22 000 known species of segmented worms (Annelida; Blake & Erséus, 1994) belong to Clitellata, the members of which develop a glandular clitellum around a part of the body at sexual maturity. Moreover, all sexually reproducing clitellates are hermaphrodites. Clitellata is traditionally divided into Oligochaeta (earthworms, sludge worms, etc.), Hirudinea (leeches) and two other leech-like taxa (Acanthobdellida and Branchiobdellida), all groups being well represented in aquatic habitats. Recent analyses of DNA sequences, however, corroborate that leeches and their allies are derived oligochaetes (Martin, 2001; Siddall et al., 2001), and thus Oligochaeta could be referred to as the same group as Clitellata. None of these two names has priority over the other (ICZN, 1999), but Clitellata may be preferred as it was originally meant to include Hirudinea too (Martin, 2001; de Queiroz & Gauthier, 1990, 1992).
As a matter of analogy to Hirudinea/Oligochaeta, various independent data now strongly support that Naididae, long regarded as one of several aquatic clitellate families, is a phylogenetic member of another such family, Tubificidae (Erséus, 1990; Brinkhurst, 1994; Christensen & Theisen, 1998; Erséus et al., 2000, 2002). For this reason, Erséus et al. (2002) suggested that the name Naididae should be formally suppressed as a synonym of Tubificidae. That is, all genera and species formerly regarded as naidids should be considered as tubificids. The further taxonomic consequences of this, however, were previously not elucidated. In this note, we propose that all former naidids are treated as a subfamily, Naidinae, within Tubificidae. In the following, we discuss the justification of this proposal, as well as the complication that it now proves that the name Naididae, which is the equivalent of the original family-group name Naidina Ehrenberg, 1828, is older than the name Tubificidae Vejdovský, 1876.
254 Thus, following ICZN (1999), all former tubificids should rather be regarded as naidids.
Classification and natural groups Hennig (1950) argued that only groups that include all the descendants of a common ancestor represent ‘natural’ units (monophyletic groups) in a classification system, and this has become the dogma of phylogenetic systematics. Thus, for taxon Tubificidae to be a natural group, all former Naididae should be regarded as part of it. By the same token, for all former naidids to remain a single taxon (regardless of its name), they should also comprise a monophyly.
The subfamilial classification of Tubificidae Currently, five other tubificid subfamilies are recognized, Tubificinae, Telmatodrilinae, Phallodrilinae, Limnodriloidinae, and Rhyacodrilinae (Erséus, 1990). Erséus et al. (2002) analysed the phylogenetic status of all of these except Telmatodrilinae on the basis of the 18S rRNA gene data, which provide some support for Tubificinae, while Phallodrilinae and Rhyacodrilinae appear non-monophyletic, and Limnodriloidinae is unresolved. This DNA study, however, corroborated that the naidids are nested among genera today assembled in the Rhyacodrilinae, a position already suggested by morphology (Erséus, 1990; Brinkhurst, 1994). As is characteristic of rhyacodrilines, a majority of the former naidids have coelomocytes, and diffuse prostate glands (Erséus, 1990). At least for Rhyacodrilus coccineus, Monopylephorus rubroniveus (both Rhyacodrilinae), and Stylaria lacustris (former Naididae), which have been studied in more detail, these prostate glands have a mesodermal origin and are probably homologous (Gustavsson & Erséus, 1997, 1999). It is thus evident that few of the already existing subfamilies are natural groups, and even if the naidids were included in Rhyacodrilinae, this latter taxon is likely to remain non-monophyletic. For the time being, we consider treating Naidinae as a subfamily within Tubificidae as the best solution. Future phylogenetic work will certainly result in further revisions of the subfamilial classification of Tubificidae, but this may involve splitting of Rhyacodrilinae (e.g., into several subfamilies) rather than a drastic change in the circumscription of Naidinae.
Proposed classification Family TUBIFICIDAE Vejdovský, 1876 Subfamily NAIDINAE Ehrenberg, 1828 (new rank) Subfamily TUBIFICINAE Vejdovský, 1876 Subfamily TELMATODRILINAE Eisen, 1885 Subfamily LIMNODRILOIDINAE Erséus, 1982 Subfamily PHALLODRILINAE Brinkhurst, 1971 Subfamily RHYACODRILINAE Hrabe, 1963 Remarks. Various authorities have been associated with the older family-group names Tubificidae/Tubificinae and Naididae/Naidinae by different subsequent authors. For instance, Erséus et al. (2002) referred to ‘Naididae Benham, 1890’ and ‘Tubificidae Vejdovský, 1884’. However, already Ehrenberg (1828) established a family name (Naidina) that is a (latinized) “noun in the nominative plural formed from the stem of an available generic name [in this case, Nais Müller, 1774]” (ICZN, 1999:Article 11.7.1), which is sufficient to consider Ehrenberg as the author of Naididae. Vejdovský (already in 1876) introduced the family group-names ‘Tubificidae’ (based on Tubifex Lamarck, 1816), as well as ‘Naididae’, although he made no specific reference to Ehrenberg. Later, Vejdovský (1884) introduced a new taxon name, ‘family’ Naidomorpha, to which he referred Ehrenberg’s Naidina as well his own Naididae.
Discussion Monophyly of Tubificidae The analysis of the 18S sequences by Erséus et al. (2002, Fig. 1) demonstrates a strong support for a clade consisting of all the tubificids ‘s. str.’ (52 species) as well as former Naididae (seven species) sampled in the study. Morphologically, the tubificid/naidid worms also form a coherent group, inasmuch as their genital system is not only anatomically similar (in virtually all cases involving prostate glands in direct association with atrial structures in the male efferent ducts), but is also with few exceptions located in two consecutive segments, with one pair of testes and one pair of spermathecae in one segment, and one pair of ovaries and one pair of male efferent ducts in the following segment. Furthermore, spermatozoal ultrastructure shows great similarity in naidids and tubificids (Ferraguti et al., 1999).
255 Monophyly of Naidinae
Further subdivision of Naidinae
The members of Naidinae differ from the other tubificids in being adapted to an aquatic life out of the sediment (Christensen & Theisen, 1998). In many species this involves the evolution of eyes, and/or the ability to swim. Furthermore, all naidines are characterized by a forward shift of the genital organs (relative to the position in other tubificids), which seems to be coupled with their alternating sexual and asexual (clonal) reproduction (Sperber, 1948; Erséus et al., 2002). In more than one way, these worms thus seem to have entered a grade separate from that of all other tubificids, and as already mentioned, DNA analyses support that they are a part of Tubificidae (Christensen & Theisen, 1998; Erséus et al., 2000, 2002). This supports Stephenson’s (1930) conclusion that the reproductive characters of naidids are derived (apomorphic) traits, but is in contrast to the older opinion that Naididae is an ancestral oligochaete group (Michaelsen, 1900; recently also advocated by Omodeo, 1998). Considering morphological traits alone, monophyly of Naidinae seems to be the most parsimonious hypothesis: these worms all have their genital organs in a more anterior position as opposed to that characterizing all other tubificids as well as other microdrile families (Enchytraeidae, Phreodrilidae, Lumbriculidae, etc.; see Brinkhurst, 1994). However, the molecular phylogenetic analysis by Erséus et al. (2002) failed to find support for a group exclusively containing the seven former naidid species sampled. Instead, the 18S data suggest a sistergroup relationship between the ‘tubificid’ Monopylephorus rubroniveus and one of the ‘naidids’, Chaetogaster diastrophus (op. cit.: Fig. 1). It should be noted, however, that the 18S sequence of M. rubroniveus differs considerably from those of all other members of the tubificid-naidid clade (indicated by its long terminal branch; op. cit.: Fig. 2), and this species’ grouping with C. diastrophus (with jackknife support only 65) may be a bias due to mere chance. Moreover, there are no morphological characters suggesting that Monopylephorus is more closely related to Chaetogaster than to any of the other naidines. For the time being, the most reasonable hypothesis is that the Naidinae is a monophyletic group, positioned within the tubificid clade.
There have been various proposals to divide the former family Naididae into subfamilies. The early history of this was reviewed by Sperber (1948), who herself recognized four such taxa: Naidinae, Pristininae, Paranaidinae, and Chaetogastrinae. Subsequently, Nemec and Brinkhurst (1987) concluded that the family contains two major groups, Naidinae (further divided into four tribes) and Stylarinae. However, none of these studies were based on well supported hypotheses of monophyly. In our opinion, regardless of whether this whole group has familial (Naididae) or subfamilial rank (Naidinae), its internal phylogenetic resolution is yet not sufficient to justify any further subdivision. Such details must await more detailed studies, preferably based on a combination of gene sequences and morphological characters. Nomenclatural priority The fact that the family-group name Naididae/Naidinae is older than Tubificidae is in conflict with the proposal presented here, as the ICZN (1999) stipulates that Naididae then should rather be enlarged to include also all former tubificids. If the latter alternative is chosen, a further division of the Naididae into subfamilies could be the same as the one suggested above, but then only Tubificinae would be based on the genus name Tubifex. Telmatodrilinae, Limnodriloidinae, Phallodrilinae and Rhyacodrilinae, together encompassing close to 600 species previously attributed to Tubificidae, would all have to be relocated under another family name, Naididae. However, considering that there are only about 175 named ‘naidid’ species in the world (Erséus & Grimm, 1998), and that replacing ‘Naididae’ by ‘Naidinae’ for these species is merely a minor nomenclatural change, we will submit an application to the International Commission of Zoological Nomenclature regarding the conservation of the usage of the family-group name Tubificidae. In our opinion, such a ruling by the Commission would better promote stability in the classification of these widespread and abundant aquatic clitellates than a strict adherance to the priority rule.
Acknowledgements We are grateful to Dr Mikael Thollesson (Uppsala University) for valuable comments on the manuscript.
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