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A New Deepwater Species of Stauromedusae, Lucernaria Janetae

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A New Deepwater Species of Stauromedusae, Lucernaria Janetae Reference: Biol. Bull. 208: 221–230. (June 2005) © 2005 Marine Biological Laboratory A New Deepwater Species of Stauromedusae, Lucernaria janetae (Cnidaria, Staurozoa, Lucernariidae), and a Preliminary Investigation of Stauromedusan Phylogeny Based on Nuclear and Mitochondrial rDNA Data ALLEN G. COLLINS1,* AND MARYMEGAN DALY2 1NMFS, National Systematics Laboratory, National Museum of Natural History, MRC-153, Smithsonian Institution, P.O. Box 37012, Washington, DC 20013-7012; and 2Department of Evolution, Ecology and Organismal Biology, The Ohio State University, Columbus, Ohio 43210 Abstract. The deepwater stauromedusan Lucernaria jan- faunal taxa and kinds of communities. Among some of these etae n. sp is described from adult and juvenile specimens novel communities associated with areas of diffuse flow collected from the East Pacific Rise. Lucernaria janetae is near active vents are spectacular fields of “stalked jellyfish” the first species in the genus recorded from the Pacific (Stauromedusae) up to 10 cm in height (Lutz et al., 1998; Ocean, and differs from its congeners in size and morphol- Halanych et al., 1999). Stauromedusans are typically small ogy. Mitochondrial (16S) and nuclear (SSU) ribosomal and solitary, and live in shallow near-shore habitats of gene sequences from L. janetae were analyzed with those of temperate seas, highlighting the unusual nature of this deep- representative stauromedusan taxa to evaluate stauromedu- sea occurrence. Despite their benthic nature, members of san monophyly. Both genes recovered a strongly monophy- Stauromedusae have traditionally been grouped as an order letic Stauromedusae that is the sister group to all other within the cnidarian class Scyphozoa. However, recent phy- medusozoans. Support of these hypotheses is robust to logenetic analyses of Cnidaria based on morphology method of phylogenetic reconstruction and to outgroup se- (Marques and Collins, 2004) and molecular data (Collins, lection, buttressing the argument that Stauromedusae should 2002) suggest that Stauromedusae is not more closely re- be recognized as the class Staurozoa. The molecular mark- lated to the scyphozoan taxa Coronatae, Rhizostomeae, and ers used here favor the same topology of relationships Semaeostomeae (herein united as Scyphozoa, following among our samples and clearly distinguished between two Marques and Collins, 2004) than it is to Cubozoa or species, Haliclystus sanjuanensis and H. octoradiatus, that Hydrozoa. have been considered synonymous by many workers. A Evolutionary discussions of stauromedusans have largely stable systematic framework for Stauromedusae appears achievable through comprehensive study of both morpho- focused on their relationship to other groups of Cnidaria logical and sequence data. (e.g., Uchida, 1929, 1972; Thiel, 1966) rather than on the relationships among its component groups (but see Thiel, Introduction 1936; Uchida, 1972). Comparatively little effort has been put into determining the systematic relationships within Deep-sea hydrothermal vent communities have been in- Stauromedusae. As a result, families and genera are recog- tensively studied since their discovery (Ballard, 1977; nized by a mosaic of features, many of which are not Lonsdale, 1977), but continue to yield major new macro- exclusive, or which suggest contradictory groupings. As an example relevant to the findings reported here, Lucernaria Received 9 December 2004; accepted 19 April 2005. is often grouped with Haliclystus to the exclusion of Lucer- * To whom correspondence should be addressed. E-mail: [email protected] nariopsis because both the former have muscles in the 221 222 A. G. COLLINS AND M. DALY peduncle. However, both Lucernaria and Lucernariopsis corded because these data may be useful for future system- lack perradial anchors and have a single-chambered pedun- atic studies of Stauromedusae. cle, whereas Haliclystus has anchors and a four-chambered The Invisorb extraction kit (Invitek GmbH, Berlin) was peduncle. The taxonomy of Stauromedusae is further hin- used to obtain DNA from one specimen each of Lucernaria dered by the fact that many species are rarely encountered. janetae (FMNH 10329) preserved in 95% ethanol, Crater- The group is in need of a thorough systematic revision. olophus convolvulus (Johnston, 1835), Depastromorpha af- In November 2003, a camera sled towed by the R/V ricana Carlgren, 1935, and an undescribed species of Hali- Atlantis serendipitously captured footage of a stauromedu- clystus. From these DNA preparations, as well as those from san aggregation near 8° 37Ј North on the East Pacific Rise. Haliclystus octoradiatus Clark, 1863, and Haliclystus san- This was not the first sighting of stauromedusans in the deep juanensis Hyman, 1940 (see Table 1 for locality data for all East Pacific (e.g., Lutz et al., 1998; Halanych et al., 1999), samples), a 530–560-bp region of mitochondrial 16S was but two subsequent dives in the DSV Alvin allowed for amplified, using the forward primer from Cunningham and these animals to be collected and examined in detail. Our Buss (1993) combined with the reverse primer from Schroth samples include individuals at several ontogenetic stages, et al. (2002). Products of the polymerase chain reaction allowing us to describe the morphology of both adults and (PCR) were purified and sequenced in both directions by juveniles. On the basis of our examinations, we find that using a Megabace 500 automated sequencer. Similarly, these specimens belong to a new species, described here as nearly complete sequences of the gene coding for SSU (or Lucernaria janetae. This is the first species of Lucernaria 18S) were obtained (except for H. sanjuanensis, which described from the Pacific Ocean. In addition, we extracted had already been sequenced for a prior study; Collins, 2002) DNA from a specimen of L. janetae and amplified two by using standard PCR and sequencing primers (Medlin et genes, one coding for the complete small subunit of the al., 1988). Edited 16S sequences were aligned by using nuclear ribosome (SSU), the other for a region of the ClustalW and then improved by eye with the software mitochondrial large ribosomal subunit (16S). Combining SeaView (Galtier et al., 1996) along with sequences from these data with data from five other species of Staurome- two stauromedusans and six representatives of outgroup dusae, we assess the usefulness of these markers for reveal- taxa obtained from GenBank; edited SSU sequences were ing historical relationships within Stauromedusae and aligned by eye into a dataset (derived from that used in present an initial investigation of stauromedusan phylogeny. Collins, 2002) comprising more than 150 other cnidarian species. All alignments used in this study are available upon Materials and Methods request. Phylogenetic analyses were carried out on three datasets Footage from a camera sled towed by the R/V Atlantis of using PAUP* 4.0 (Swofford, 2002). The first data set con- the Woods Hole Oceanographic Institution in November tains 230 characters of 16S that are hypothesized to be 2003 revealed dense aggregations of large stauromedusans homologous across our stauromedusan samples and the six in a previously undocumented area of weak hydrothermal outgroup taxa representing Anthozoa, Cubozoa, Hydrozoa, activity at 8° 36.745ЈN, 104° 12.740ЈW. During two dives and Scyphozoa. For the SSU sequences, we excluded re- (3935, 3927) in the submersible Alvin, the extent of the gions that could not be reliably aligned across Stauromedu- aggregations was determined, populations were docu- sae and the eight outgroup taxa; the resulting alignment is mented with still digital photography and video, and several 1746 bases. The third dataset comprises both 16S and SSU specimens were collected by using suction samplers. data from Stauromedusae; narrowing the taxonomic focus Live material was photographed and examined and then allowed us to include an additional 233 characters from 16S fixed in 20% formalin or 95% ethanol. Formalin-fixed ma- rDNA. For each dataset, we searched for optimal trees by terial was transferred to 70% ethanol after 2 weeks. Addi- using the criteria of maximum parsimony (MP) and maxi- tional material was frozen for molecular or isotopic analy- ses. All specimens have been deposited at the Field Museum of Natural History, Chicago, Illinois. Preserved specimens Table 1 were examined whole and in dissection; some material was Stauromedusans sampled for molecular data processed for histology with standard paraffin techniques. Histological slides were stained in Masson’s trichrome Species Locality of collection (Presnell and Schreibman, 1997). Pieces of tissue from Craterolophus convolvulus Helgoland, Germany tentacles, subumbrellar vesicles, and gastric filaments were Depastromorpha africana False Bay, South Africa smeared on a slide; nematocysts in these smears were ex- Haliclystus octoradiatus Northern Germany amined using differential interference contrast microscopy Haliclystus sanjuanensis Washington State, USA at 100ϫ magnification. Cnidae terminology follows Mar- Haliclystus sp. Los Molinos (near Valdivia), Chile Ј iscal (1974). Nematocyst type, size, and location are re- Lucernaria janetae 8° 37 North on the East Pacific Rise NEW SPECIES OF DEEP-SEA STAUROMEDUSAE 223 mum likelihood (ML), with 500 and 100 replicate searches, respectively, and with sequences added randomly to the starting topology. Gaps were treated as missing data. We used likelihood ratio tests employed by ModelTest ver. 3.6 (Posada and Crandall, 1998) to determine
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