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Envall Et Al Molecular Phylogenetics and Evolution 40 (2006) 570–584 www.elsevier.com/locate/ympev Molecular evidence for the non-monophyletic status of Naidinae (Annelida, Clitellata, TubiWcidae) Ida Envall a,b,c,¤, Mari Källersjö c, Christer Erséus d a Department of Zoology, Stockholm University, SE-106 91 Stockholm, Sweden b Department of Invertebrate Zoology, Swedish Museum of Natural History, Box 50007, SE-104 05 Stockholm, Sweden c Laboratory of Molecular Systematics, Swedish Museum of Natural History, Box 50007, SE-104 05 Stockholm, Sweden d Department of Zoology, Göteborg University, Box 463, SE-405 30 Göteborg, Sweden Received 24 October 2005; revised 9 February 2006; accepted 15 March 2006 Available online 8 May 2006 Abstract Naidinae (former Naididae) is a group of small aquatic clitellate annelids, common worldwide. In this study, we evaluated the phylo- genetic status of Naidinae, and examined the phylogenetic relationships within the group. Sequence data from two mitochondrial genes (12S rDNA and 16S rDNA), and one nuclear gene (18S rDNA), were used. Sequences were obtained from 27 naidine species, 24 species from the other tubiWcid subfamilies, and Wve outgroup taxa. New sequences (in all 108) as well as GenBank data were used. The data were analysed by parsimony and Bayesian inference. The tree topologies emanating from the diVerent analyses are congruent to a great extent. Naidinae is not found to be monophyletic. The naidine genus Pristina appears to be a derived group within a clade consisting of several genera (Ainudrilus, Epirodrilus, Monopylephorus, and Rhyacodrilus) from another tubiWcid subfamily, Rhyacodrilinae. These results dem- onstrate the need for a taxonomic revision: either Ainudrilus, Epirodrilus, Monopylephorus, and Rhyacodrilus should be included within Naidinae, or Pristina should be excluded from this subfamily. Monophyly of four out of six naidine genera represented by more than one species is supported: Chaetogaster, Dero, Paranais, and Pristina, respectively. © 2006 Elsevier Inc. All rights reserved. Keywords: Naidinae; Naididae; Rhyacodrilinae; TubiWcidae; 12S rDNA; 16S rDNA; 18S rDNA; Phylogeny; Taxonomy 1. Introduction Naidids are capable of reproducing asexually, by bud- ding (paratomy) or fragmentation (architomy) (Brinkhurst Naidid worms are small aquatic clitellate annelids, com- and Jamieson, 1971; Sperber, 1948). Paratomic Wssion is mon worldwide. About 180 species have been described most usual. This is a peculiar process in which a new head, (Erséus, 2005), and 24 genera are currently recognized and in front of this a new tail, is intercalated in the middle (Table 1). Most species inhabit freshwater, but some are of the original worm’s body. In this way, a transient linked adapted to brackish or marine habitats (Sperber, 1948). chain of individuals may be formed (Bely and Wray, 2001, They are primarily found in superWcial sediment layers, or 2004; Dehorne, 1916). Partly because of this vegetative at the surface of aquatic vegetation, and some species are mode of reproduction, which makes it possible for a worm even active swimmers (Erséus, 2005). Most species are detri- to produce many oVspring in a short time, naidid popula- tivorous, but carnivory and parasitism exist (Brinkhurst tions may increase rapidly under favorable conditions (e.g., and Jamieson, 1971). Armendáriz, 2000; Loden, 1981). Naidids also periodically reproduce sexually (e.g., Erséus, 2005; Sperber, 1948). Naididae was long regarded as a separate family within the clitellate order TubiWcida. However, several studies, * Corresponding author. Fax: +46 8 5195 5181. both morphological (Brinkhurst, 1994; Erséus, 1987, 1990) E-mail address: [email protected] (I. Envall). and molecular, based on 28S rDNA (but referred to as 1055-7903/$ - see front matter © 2006 Elsevier Inc. All rights reserved. doi:10.1016/j.ympev.2006.03.021 I. Envall et al. / Molecular Phylogenetics and Evolution 40 (2006) 570–584 571 Table 1 Naidinae, within TubiWcidae, and from now on we will use The genera within Naididae sensu Brinkhurst and Jamieson (1971) (plus the proposed subfamily name Naidinae (sensu Erséus and the two genera Bratislavia Kosel, 1976, and Rhopalonais Dzwillo and Gustavsson, 2002) in this paper. [Erséus et al. (2005) has Grimm, 1974 later described) asked the International Commission of Zoological Nomen- Allonais Sperber, 1948 • • clature to conserve the usage of the family group name Amphichaeta Tauber, 1879 W Arcteonais Piguet, 1928 Tubi cidae, despite that it is younger than the family group Branchiodrilus Michaelsen, 1900 name Naididae.] Bratislavia Kosel, 1976 In addition to Naidinae, Wve tubiWcid subfamilies are rec- Chaetogaster von Baer, 1827 • ognized: Limnodriloidinae, Phallodrilinae, Rhyacodrilinae, • Dero Oken, 1815 Telmatodrilinae, and TubiWcinae (Erséus, 1990), although it Haemonais Bretscher, 1900 Homochaeta Bretscher, 1896 is not probable that all these groups are natural (Erséus, Nais Müller, 1773 • 1990; Erséus and Ferraguti, 1995; Erséus and Gustavsson, Neonaisa Sokolskaya, 1962 2002; Erséus et al., 2000, 2002; Sjölin et al., 2005). There are Ophidonais Gervais, 1838 • indications that Naidinae is closely related to Rhyacodrili- • Paranais Czerniavsky, 1880 nae. It has been placed close to, or even nested within, Rhya- Piguetiella Sperber, 1939 • Pristina (including Pristinella)b Ehrenberg, 1828 • codrilinae in several phylogenetic studies (Brinkhurst, 1994; Rhopalonais Dzwillo and Grimm, 1974 Christensen and Theisen, 1998; Erséus, 1990; Erséus et al., Ripistes Dujardin, 1842 • 2000, 2002; Sjölin et al., 2005). However, in these studies the Slavina Vejdovský, 1883 • number of taxa from the two groups has been insuYcient to • Specaria Sperber, 1939 enable any detailed conclusions. Stephensoniana Cernosvitov, 1938 Stylaria Lamarck, 1816 • Three morphology-based hypotheses on the naidine phy- Uncinais Levinsen, 1884 • logeny have been formulated in the last century (Lastobkin, Vejdovskyella Michaelsen, 1903 • 1924; Nemec and Brinkhurst, 1987; Sperber, 1948). The two Wapsac Marcus, 1965 oldest of these were not based on explicit phylogenetic prin- A bullet indicates that the genus is represented in this study ciples, but rather on mere morphological similarity. The a A genus which remains inadequately described (Brinkhurst and Jamie- three hypotheses are fundamentally diVerent in several son, 1971). respects, probably at least partly because of the low number b Brinkhurst (1985) divided Pristina into Pristina and Pristinella, but the two groups were reunited, since species with a mix of Pristina and of independent morphological characters. According to Las- Pristinella characters were described by Collado and Schmelz (2000). tobkin (1924) there are two groups within “Naididae”, i.e., c Wapsa is today regarded as a synonym of Paranais (Brinkhurst and Pristininae (Pristina) and Naidinae (sensu Lastobkin) (all Coates, 1985). other genera). Sperber (1948) identiWed four subfamilies: Pristininae (Pristina), Paranaidinae (Paranais), Chaetogas- “23S”) in combination with the COI gene (Christensen and trinae (Chaetogaster and Amphichaeta), and Naidinae (sensu Theisen, 1998), 18S rDNA (Erséus et al., 2002; Erséus and Sperber) (all remaining genera). According to Nemec and Källersjö, 2004), and 18S rDNA combined with 16S rDNA Brinkhurst (1987), Wnally, there are two subfamilies within (Sjölin et al., 2005), support that the naidids should be “Naididae”: Stylarinae and Naidinae (sensu Nemec and treated as an ingroup of another family, TubiWcidae. The Brinkhurst, 1987). Stylarinae consists of the genera Stylaria, genitalia have a more anterior position in naidids (in seg- Arcteonais, Ripistes, Vejdovskyella, Slavina, Stephensoniana ments IV–V to VII–VIII) compared to in tubiWcids (seg- (incertae sedis), and Piguetiella (incertae sedis). Naidinae ments X–XI), and this condition, together with the ability (sensu Nemec and Brinkhurst, 1987) consists of all the of Wssion, have been the main reasons assigning Naididae remaining genera, divided into four tribes: Naidini, Derini, family status. Sometimes, Naididae has in fact been Pristinini, and Chaetogastrini. regarded as a “primitive” clitellate group, not even closely In a recent study, Bely and Wray (2004) used molecular related to TubiWcidae (Omodeo, 1998), because of a com- data (COI) in the attempt to reconstruct the naidine phy- paratively simple circulatory system, and a somewhat leech- logeny. The result from this study suggests two groups: one like embryology. However, the morphology of the genitalia comprising the genus Pristina, and the other comprising all of TubiWcidae and Naididae, respectively, is similar, with other genera sampled. prostate glands directly associated with the atrium (which The aim of the present study was to evaluate the mono- is a part of the male eVerent duct). Moreover, the reproduc- phyly of Naidinae sensu Erséus and Gustavsson (2002), tive structures are located in two consecutive segments in with special emphasis on its relationship to Rhyacodrilinae, both groups (although in diVerent segment pairs), with the and to Wnd a hypothesis about the phylogeny within the Wrst segment containing one pair of testes and one pair of group. 18S rDNA sequences have been used several times spermathecae, and the other segment containing one pair of before, dealing with clitellate phylogenies (Apakupakul ovaries and one pair of male eVerent ducts. Furthermore, et al., 1999; Erséus et al., 2000, 2002; Erséus and Källersjö, the spermatozoa exhibit ultrastructural
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