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(Hydrozoa, Anthomedusae) and the Use of 16S Rdna Sequences for Unpuzzling Systematic Relationships in Hydrozoa*

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(Hydrozoa, Anthomedusae) and the Use of 16S Rdna Sequences for Unpuzzling Systematic Relationships in Hydrozoa* SCI. MAR., 64 (Supl. 1): 117-122 SCIENTIA MARINA 2000 TRENDS IN HYDROZOAN BIOLOGY - IV. C.E. MILLS, F. BOERO, A. MIGOTTO and J.M. GILI (eds.) Sarsia marii n. sp. (Hydrozoa, Anthomedusae) and the use of 16S rDNA sequences for unpuzzling systematic relationships in Hydrozoa* BERND SCHIERWATER1,2 and ANDREA ENDER1 1Zoologisches Institut der J. W. Goethe-Universität, Siesmayerstr. 70, D-60054 Frankfurt, Germany, E-mail: [email protected] 2JTZ, Ecology and Evolution, Ti Ho Hannover, Bünteweg 17d, D-30559 Hannover, Germany. SUMMARY: A new hydrozoan species, Sarsia marii, is described by using morphological and molecular characters. Both morphological and 16S rDNA data place the new species together with other Sarsia species near the base of a clade that developed‚ “walking” tentacles in the medusa stage. The molecular data also suggest that the family Cladonematidae (Cladonema, Eleutheria, Staurocladia) is monophyletic. The taxonomic embedding of Sarsia marii n. sp. demonstrates the usefulness of 16S rDNA sequences for reconstructing phylogenetic relationships in Hydrozoa. Key words: Sarsia marii n. sp., Cnidaria, Hydrozoa, Corynidae, 16S rDNA, systematics, phylogeny. INTRODUCTION Cracraft, 1991; Schierwater et al., 1994; Swofford et al., 1996). Nevertheless molecular data are especial- Molecular data and parsimony analysis have ly useful or even indispensable in groups where become powerful tools for the study of phylogenet- other characters, like morphological data, are limit- ic relationships among extant animal taxa. In partic- ed or hard to interpret. ular, DNA sequence data have added important and One classical problem to animal phylogeny is the surprising information on the phylogenetic relation- evolution of cnidarians and the groups therein ships at almost all taxonomic levels in a variety of (Hyman, 1940; Brusca and Brusca, 1990; Bridge et animal groups (for references see Avise, 1994; al., 1992, 1995; Schuchert, 1993; Schierwater, 1994; DeSalle and Schierwater, 1998). We may not forget, Odorico and Miller, 1997). Particularly the system- however, that inferring phylogenetic relationships atic relationships within the Hydrozoa represent one from molecular data is neither trivial nor a final of the most difficult and long-standing problems to solution to systematics, since the molecular option evolutionary biologists. In lack of fossil records and can be prone to a large number of pitfalls and mis- a sufficient number of unambiguous morphological understandings (for refs. see Miyamoto and characters, neither the phylogenetic relationships between nor within the orders have been understood *Received February 17, 1999. Accepted May 10, 1999. and are still subject of controversial debates (see for EMBEDDING A NEW HYDROZOAN SPECIES BY 16S DATA 117 example, Petersen, 1979, 1990; Cunningham and (Hamburg, Germany), of Sarsia reesi by Alvaro Buss, 1993; Schuchert, 1996). Historically, hydroid Esteves Migotto (São Sebastião, Brazil), and of systematics has been hindered by problems of decid- Thecocodium quadratum by Stefan Berking ing the importance of polyp versus medusoid char- (Cologne, Germany). acters (Rees, 1957; Naumov, 1960; Boero, 1980; Hydroids of Eleutheria dichotoma, Cladonema Bouillon, 1981; Boero and Bouillon, 1987). Since in radiatum and Sarsia marii n. sp. were collected by most hydroids the medusa stage has been reduced to the authors from the green alga Ulva lactuca, sessile gonophores, reconstructions of phylogenetic obtained 10-50 cm under the water surface at the relationships have mainly been based upon morpho- rocky shore of the Laboratoire Arago, Banyuls sur logical characters of the hydroid stage and the Mer, France. Single polyps were isolated from the assumption of a progressive reduction of the medu- algae and grown in small finger bowls in the lab soid stage (Werner, 1984; Boero and Sarà, 1987). using our standard culturing conditions for hydro- Here, the arrangement of tentacles and the invento- zoans (Schierwater et al., 1992; Schierwater and ry of nematocysts have been two of the most impor- Hadrys, 1998). Polyps were maintained in artificial tant characters. The morphological simplicity and seawater (30‰ salinity) at 19-21°C and fed ad libi- plasticity of hydroids, however, makes morphologi- tum two times weekly on 3-4 day old brine shrimp cal homoplasy likely to be common in this group. larvae (Artemia salina). Under these conditions We suggest that molecular characters must be added polyps of all three species, including Sarsia marii, to morphological and life cycle characters in order grew into colonies of polyps connected by a hori- to resolve hydrozoan systematics. zontal net of stolons (the latter grew attached to the By applying molecular data to previously unde- glass surface of the finger bowl). While medusae of scribed species we might in many cases be able to Eleutheria dichotoma and Cladonema radiatum are resolve their relative taxonomic position even in the found regularly year round, Sarsia marii medusae absence of morphological or developmental data. were found only once in spring 1998. Since the lat- This approach promises valuable results if molecu- ter stayed alive just for a few days, morphological lar data from closely related taxa are available for traits could be observed on subadult medusae only. comparative analyses. We present an example from The original polyp was found on a thallus of the a new athecate hydroid species which we assign to green alga Ulva lactuca collected on 5 April 1997 at the genus Sarsia based on both morphological and the Laboratoire Arago, Banyuls sur Mer, France, molecular data. 42°29’N, 3°08’E. DNA extraction, amplification and sequencing MATERIALS AND METHODS Small samples of hydroid tissue were homoge- Animal material nized in HOM buffer (100mM Tris-HCL, 10mM EDTA, 100mM NaCl, 0.5% SDS, pH 8.0), and Based on morphological characters we used the extracted once with phenol-chloroform-isoamyl following closely related species of the infra-order alcohol (25:24:1). DNA was precipitated by addi- Capitata (Werner, 1984) for embedding the new tion of two volumes ethanol and 1/10 volume 5M species into a taxonomic framework: Stauridiosar- NH4Ac, and after a single centrifugation and wash- sia producta Wright (1858), Sarsia tubulosa Sars ing step resuspended in TE buffer (1mM Tris-HCL, (1835), Sarsia reesi Vannucci (1956) (all members 0.1mM EDTA, pH 7.5) (for details see Schierwater of the family Corynidae), Staurocladia bilateralis and Ender, 1993). For PCR amplification of part of Edmondson (1930), Staurocladia oahuensis the 16S rRNA mitochondrial large subunit, hydro- Edmondson (1930), Cladonema radiatum Dujardin zoan specific primers were used (Cunningham and (1843) (Cladonematidae), and Eleutheria Buss, 1993). The amplified region corresponds to dichotoma Quatrefages (1842) (Eleutheriidae). The the 5´-end of the 16S rRNA gene and revealed Filifera Thecocodium quadratum Werner (1965) between 588 bp (Eleutheria dichotoma) and 595 bp served as an outgroup. Animal material of Stauro- (Cladonema radiatum). Amplification reactions cladia bilateralis and S. oahuensis were provided were carried out with 10-20ng of DNA in a total vol- by Yayoi Hirano (Awagun, Japan), of Stauridiosar- ume of 25 µL using a 9.600 thermocycler from sia producta and Sarsia tubulosa by Gerhard Jarms Perkin Elmer and the following temperature profile: 118 B. SCHIERWATER and A. ENDER FIG. 1. – Drawings of live specimens of Sarsia marii n. sp. raised in the laboratory. A polyp with a well developed medusa bud above the aboral tentacle whorl and a four-day-old medusa are shown. Explanations are given in the text. 10 cycles (92°C/50 s, 45°C/50 s, ramp 3 s/1°C, RESULTS 72°C/1 min) followed by 40 cycles (92°C/50 s, 50°C/1 min, ramp 3 s/1°C, 72°C/1 min); finally Sarsia marii n. sp. fragments were elongated at 72°C for 5 min. DNA cloning and sequencing were performed as The morphology of Sarsia marii polyps and described in Ender et al. (1996). medusae (Fig. 1) suggests relationships to the Cladonematidae and Corynidae (cf. Werner, 1984; DNA sequence alignment and phylogenetic Petersen, 1990). The polyp of S. marii looks rather analyses similar to a Cladonema radiatum polyp and exhibits in addition to the oral whorl of capitate tentacles a 16S rDNA sequences were aligned with the aid second whorl of 4 filiform sensory tentacles. The of CLUSTAL (Higgins and Sharp, 1989) and number of capitate tentacles was always four, with ambiguous regions (often surrounding variable each 10-11 endodermal cells (Table 1). The medusa loops) were deleted. Since computer based align- looks like a typical Sarsia medusa and lacks any ment programs did not reveal consistent alignments, Cladonema typical tentacle branching patterns, sug- sequences were controlled by eye and compared to a gesting that Sarsia marii is related to the genus Sar- secondary structure model of the Eleutheria sia. Here the new species appears to be very similar dichotoma 16S rRNA molecule (Ender, 1997). A to S. reesi (synonym: Dipurena reesi Vannucci, detailed description of the 16S rDNA data collection 1956; Brinkmann-Voss and Petersen, 1960), both in and analyses will be given elsewhere (together with the polyp and medusa generation (Table 1). The typ- a larger hydrozoan tree; Ender and Schierwater, in ical long manubrium of S. reesi medusae, however, prep.). For tree inference by maximum parsimony or was not found in the immature medusae of S. marii. neighbor-joining data were analyzed using PAUP The most striking difference
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