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The Indo-Pacific Gemmula Species in the Subfamily Turrinae: Aspects of Field Distribution, Molecular Phylogeny, Radular Anatomy and Feeding Ecology

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The Indo-Pacific Gemmula Species in the Subfamily Turrinae: Aspects of Field Distribution, Molecular Phylogeny, Radular Anatomy and Feeding Ecology ARTICLE THE INDO-PACIFIC GEMMULA SPECIES IN THE SUBFAMILY TURRINAE: ASPECTS OF FIELD DISTRIBUTION, MOLECULAR PHYLOGENY, RADULAR ANATOMY AND FEEDING ECOLOGY FRANCISCO M. HERALDE III1*, YURI I. KANTOR2, MARY ANNE Q. ASTILLA3, ARTURO O. LLUISMA3, ROLLAN GERONIMO3, PORFIRIO M. ALIÑO3, MAREN WATKINS4, PATRICE SHOWERS CORNELI5, BALDOMERO M. OLIVERA5, AMEURFINA D. SANTOS1, AND GISELA P. CONCEPCION3 1 National Institute of Molecular Biology and Biotechnology, University of the Philippines, Diliman,Quezon City 1101, Philippines 2 A. N. Severtzov Institute of Ecology and Evolution, Russian Academy of Sciences, Leninski Prospect 33, Moscow 119071, Russia 3 Marine Science Institute, University of the Philippines, Diliman, Quezon City 1101, Philippines 4 Department of Pathology, University of Utah, 421 Wakara Way, Suite 3323, 84108, U.S.A 5 Department of Biology, 257 S 1400 E, Room 201, University of Utah, Salt Lake City, Utah, 84112, U.S.A. he biology, feeding ecology and phylogenetic much more abundant at one site but not at the other sites. relationships of marine snails in the family Turridae Molecular phylogenetic analysis based on 16S sequences remain poorly understood. Here we report our study correlated with previously reported 12S sequences and revealed on four deep-water species in the genus Gemmula, a that the four species all belong to a well-supported Gemmula major group in this family. The four species G. clade within the subfamily Turrinae; and that this clade appeared Tspeciosa (Reeve 1843), G. sogodensis (Olivera 2005), G. kieneri more closely related to the clades Xenuroturris, Turris and (Doumet 1940) and G. diomedea (Powell 1964) were collected Lophiotoma than to the other clades in the subfamily at five different sites in the Philippines, and their pattern of (i.e.,Turridrupa, Unedogemmula and Polystira). Morphological distribution in the sites, their feeding behavior as well as their analysis of the radula of both G. speciosa and G. sogodensis phylogenetic relationships with each other and with other revealed that the radulae of the two species were similar but members of the subfamily Turrinae were investigated. The differed from the other turrids, Lophiotoma acuta and radular morphology (of two Gemmula species) and potential Unedogemmula bisaya, by the presence of central teeth, prey (for one Gemmula species) were also examined. Actual consistent with the separation of the Gemmula clade from the feeding observations were also conducted for Gemmula speciosa Lophiotoma and Unedogemmula clade. and compared with two turrids from other genera. To identify the polychaete group that is targeted as prey by All four Gemmula species showed strikingly different species of Gemmula, analysis of regurgitated food fragments patterns of distribution; each species was found to be relatively was made; phylogenetic analysis of an mtCOI gene fragment that was PCR-amplified from the regurgitated tissue of one *Corresponding Author specimen (G. diomedea) indicated close affinity of the prey to Current address: Department of Biochemistry and the terebellid polychaete Amphitritides. Specimens of Gemmula Molecular Biology, College of Medicine,University of the speciosa, when challenged with the terebellid polychaete Philippines, Manila 1000, Philippines Loimia sp., were observed to attack the worm suggesting that Tel/Fax: +632-526-4197 Gemmula species feed on terebellid polychaetes. Lophiotoma Email: [email protected] acuta were also observed to feed on the same species of Subm itted: December 3, 2009 Revised: February 6, 2010 terebellid but were usually group-feeding in contrast to the Accepted: February 9, 2010 solitary feeding of G. speciosa. Unedogemmula bisaya did not Published: March 5, 2010 feed on the terebellid which also supports the separation of the Editor-in-Charge: Eduardo A. Padlan Gemmula and Unedogemmula clade. The 16S-based clustering Vol.3 | No.1 | 2010 Philippine Science Letters 21 prediction of a likely terebellid foodtype for the molecular phylogeny have been carried out on Conus (Duda and Gemmula/Lophiotoma clade was validated by the feeding Palumbi 1999; Duda et al. 2001; Espiritu et al. 2001; Monje et challenge experiments in contrast with the central teeth pattern al. 1999); phylogenetic relationships for the vast biodiversity of of the radula. turrids (Powell 1964; Taylor et al. 1993; Bouchet et al. 2002; Two lines of proof (i.e. the molecular phylogenetic analysis and Puillandre et al. 2008) are still poorly understood. So far, and the feeding challenge) supporting the toxin homology only one study has been carried out (Heralde et al. 2007) which findings previously reported, provide consistent evidence that defined clades in the subfamily Turrinae. Gemmula is a distinct clade of worm-hunting Turrinae that feeds To further discriminate the species, we examined and on Terebellidae. compared the foregut anatomy, i.e., radula, of three species. Because their habitats are inaccessible, little is also known of their feeding biology. Although turrids in general are known to KEYWORDS feed on polychaetes, there are no available data on which species of polychaetes are preyed on by Gemmula (or any Gemmula ecology, Turrinae taxonomy, molecular phylogeny, turrid) species. We therefore collected new data on feeding 16S clustering, central teeth, terebellid foodtype, feeding behavior and potential prey preferences. challenge, regurgitate analysis MATERIALS AND METHODS INTRODUCTION Sample Collection Marine snails belonging to the family Turridae (the Snails were purchased from local fishermen as by-catch in “turrids”) comprise a large and highly diverse subgroup within trawl nets along the mouth of Manila Bay (from Bataan to the superfamily Conoidea, a group consisting of venomous Cavite and Batangas) and tangle nets in the seas of Cebu and marine gastropods. In fact, turrids comprise the largest family of Bohol. Live snails were kept in seawater until they were deep-sea gastropods (Rex et al. 2000) and account for the vast processed for anatomical or molecular work. The relative majority of conoidean biodiversity (Bouchet et al. 2002). distribution and abundance of Gemmula speciosa along the However, the biology, ecology, and species-level phylogenetic periphery of Manila Bay was initially assessed by monitoring relationships of these organisms are still poorly known. A the collections per trawl of selected boats in August 2005 and number of factors contribute to the difficulty of studying these from October 2005 to January 2006. The abundance in all the organisms, such as high morphological similarity among sampling sites was monitored from the snails collected by the species, poor accessibility of their habitats (50 -500 m depth), fishermen from February to May 2006. their small size, and their nocturnal and burrowing behavior. Recent studies have started to shed light on the biochemistry, Specimen Preparation and DNA Extraction toxinology and toxin gene expression of this group, revealing its The snails were segregated by putative species and pre- potential as a source of bioactive peptides (López-Vera et al. served for various uses. The snails were cracked and tissue sam- 2004; Watkins et al. 2006; Heralde et al. 2008). Understanding ples (hepatopancreas and foot) were obtained and preserved in the ecology, i.e., feeding behavior, and genetic diversity of these approximately 10 volumes of RNALater. Voucher specimens organisms will therefore be of interest to marine biologists as were kept in 70% ethanol. DNA extraction was performed in well as marine biotechnologists. fifty mg tissue samples (hepatopancreas or foot) using the Pure- As part of an initial effort to characterize this group, this gene DNA kit (Invitrogen) or the DNeasy tissue kit (Qiagen) study focuses on the genus Gemmula (the “gem turrids”). The and aliquots were prepared.. members of this genus largely occur in deeper tropical waters (at depths of 50-500 meters) and comprise a major group in the Gene amplification subfamily Turrinae (Powell 1964). Other genera conventionally The 16S mitochondrial rRNA gene was amplified using the included in this subfamily are Turris, Lophiotoma, primers 16SL (5’-GTTTACCAAAAACATGGCTTC-3’) and Unedogemmula, Turridrupa and Polystira (Heralde et al. 2007; 16SH (5’-CCGGTCTGAACTCAGATCACGT-3’) with uracil Powell 1964; Taylor et al. 1993). Several species of Gemmula adaptor sequences. A PCR mix containing 20-40 ng genomic have been collected in relatively large numbers in Philippine DNA, 2μM of each primer, 2μM of dNTP and 2μM of Taq waters. In this study, we particularly focused on four deep-water Polymerase was prepared and cycled with the following profile: Gemmula species, namely, G. speciosa (Reeve 1843) (the 95oC 1 min initial denaturation; 40 cycles of 95oC 20 sec “splendid gem turrid”), G. sogodensis (Olivera 2004), G. denaturation, 55oC 20 sec annealing and 72oC 30 sec extension; diomedea (Powell 1964), and G. kieneri (Doumet 1840) (Figure and 72oC 5 min final extension. The PCR product was ligated to 1). We investigated their distribution and phylogeny, as pNEB206A (USER Friendly Cloning, New England Biolabs) information on the pattern of their distribution is scant and the and introduced into E. coli (DH5a) through chemical phylogeny of these species has not yet been elucidated. In the transformation. Plasmids from transformants with inserts were superfamily Conoidea, most previous investigations of sequenced through the ABI 377 DNA Sequencer or submitted to 22 Philippine Science Letters Vol.3 | No.1 | 2010
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