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Phylogenetic Relationships of the Cochliopinae (Rissooidea: Hydrobiidae): an Enigmatic Group of Aquatic Gastropods Hsiu-Ping Liu,* Robert Hershler,†,1 and Fred G

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Phylogenetic Relationships of the Cochliopinae (Rissooidea: Hydrobiidae): an Enigmatic Group of Aquatic Gastropods Hsiu-Ping Liu,* Robert Hershler,†,1 and Fred G Molecular Phylogenetics and Evolution Vol. 21, No. 1, October, pp. 17–25, 2001 doi:10.1006/mpev.2001.0988, available online at http://www.idealibrary.com on Phylogenetic Relationships of the Cochliopinae (Rissooidea: Hydrobiidae): An Enigmatic Group of Aquatic Gastropods Hsiu-Ping Liu,* Robert Hershler,†,1 and Fred G. Thompson‡ *Department of Biology, Southwest Missouri State University, 901 South National Avenue, Springfield, Missouri 65804-0095; †Department of Systematic Biology, National Museum of Natural History, Smithsonian Institution, Washington, DC 20560-0118; and ‡Florida Museum of Natural History, University of Florida, Gainesville, Florida 32611-7800 Received July 24, 2000; revised March 27, 2001 shler, 1993) have not been well tested as there is no Phylogenetic analysis based on a partial sequence of rigorously proposed analysis of relationships that in- the mitochondrial cytochrome c oxidase subunit I cludes more than a trivial sampling of this large group gene was performed for 26 representatives of the (e.g., Altaba, 1993; Ponder et al., 1993; Ponder, 1999). aquatic gastropod subfamily Cochliopinae, 6 addi- Phylogenetic reconstructions of these animals have tional members of the family Hydrobiidae, and out- been hampered by a paucity of apparent synapomor- group species of the families Rissoidae and Pomatiop- phies (Thompson, 1984), putatively extensive ho- sidae. Maximum-parsimony analysis yielded a single moplasy (Davis, 1988; Hershler and Thompson, 1992), shortest tree which resolved two monophyletic and difficulties in reconciling homology (Hershler and groups: (1) a clade containing all cochliopine taxa with Ponder, 1998). Whereas a recent survey and reassess- the exception of Antroselates and (2) a clade composed of Antroselates and the hydrobiid genus Amnicola. The ment of characters (Hershler and Ponder, 1998) may clade containing both of these monophyletic groups pave the way for more fruitful analyses that use mor- was depicted as more closely related to members of the phological criteria, the study of hydobiid phylogeny family Pomatiopsidae than to other hydrobiid snails clearly would benefit from infusion of additional data which were basally positioned in our topology. New sets, and we are utilizing DNA sequences of mitochon- anatomical evidence supports recognition of the coch- drial genes for this purpose. liopine and Antroselates–Amnicola clades, and struc- One of our goals is to assess the phylogenetic rela- ture within the monophyletic group of cochliopines is tionships of the major groups of hydrobiid snails. In largely congruent with genitalic characters. However, this paper we focus on the subfamily Cochliopinae, the close relationship between the Pomatiopsidae and which is composed of 34 genera and more than 260 these clades is in conflict with commonly accepted species and is distributed within tropical and temper- classifications and suggests that a widely accepted ate America and several regions of the Old World (Her- scenario for genitalic evolution in these snails is in shler and Thompson, 1992; Altaba, 1993; Hershler and need of further study. © 2001 Academic Press Velkovrh, 1993; Hershler, 1999). The Cochliopinae was early conceived as a small group of squat-shelled hy- drobiids (Taylor, 1966; Starobogatov, 1970). More re- INTRODUCTION cently, Hershler and Thompson (1992) reconstituted the subfamily as a larger group of diverse-shelled taxa The cosmopolitan gastropod family Hydrobiidae is diagnosed primarily by the partial or complete separa- the largest group of freshwater mollusks, with several tion of the sperm-conducting channel (sperm tube) thousand species placed in more than 300 genera (Ka- from the female glandular oviduct and the absence of a bat and Hershler, 1993). Despite the ubiquity and eco- glandular duct within the male penis. However, mono- logical importance of these small, locally abundant phyly of the cochliopines was not established in this snails, the biology of few species has been thoroughly nonphylogenetic treatment and was considered sus- investigated and the systematics of the group remains pect because these diagnostic characters are not unstable at all ranks. The divergent classifications that have been offered for the hydrobiids (Kabat and Her- unique in the Hydrobiidae—amnicolines share with cochliopines a diaulic arrangement of the female gen- italia (Hershler and Thompson, 1988) and most hydro- 1 To whom correspondence and reprint requests should be ad- dressed at Department of Systematic Biology, National Museum of biids lack an accessory glandular duct in the penis. The Natural History, Smithsonian Institution, Washington, DC 20560- phylogenetic relationships of the cochliopines also are 0118. Fax: (202) 357-2343. E-mail: [email protected]. uncertain. Several other rissooidean families have di- 17 1055-7903/01 $35.00 Copyright © 2001 by Academic Press All rights of reproduction in any form reserved. 18 LIU, HERSHLER, AND THOMPSON aulic female genitalia (e.g., Pomatiopsidae, Stenothy- ment of the female genitalia. We also sampled four ridae) and a minority of workers have suggested that additional hydrobiids that include representatives of cochliopines are more closely related to these than to two other commonly accepted subfamilies (Litho- hydrobiids (Starobogatov, 1970; Ioganzen and Starobo- glyphinae, Nymphophilinae) and two putatively plesi- gatov, 1982; Starobogatov and Sitnikova, 1983). Others omorphic hydrobiids (Hydrobia and Phrantela). Trees have argued that diauly was independently evolved by were rooted with Rissoina, a representative of the the cochliopines within the Hydrobiidae (Davis et al., primitive marine rissooidean family Rissoidae ( fide 1982; Ponder, 1988; Hershler and Ponder, 1998) and Ponder, 1985, 1988, Fig. 4). We also utilized several this is reflected in most of the recent classifications of mtCOI sequences of pomatiopsids and rissoids re- these snails. The single detailed analysis of rissooidean ported by Davis et al. (1998). Taxa are listed in Table 1. phylogeny did not resolve this issue as its terminals Samples not assigned to species represent novelties were composite representations of individual families whose generic placements were based on our morpho- (Ponder, 1988), and a more recent analysis of a small logical study of voucher material. Voucher material number of taxa supports the latter hypothesis (Ponder, (UF, Florida Museum of Natural History, University of 1999). Florida; USNM, National Museum of Natural History, In a recent paper, which focused on analysis of phy- Smithsonian Institution) is cited in Table 1 for taxa logenetic relationships of species of the genus Tryonia whose sequences are newly provided herein. by use of partial sequences of the mitochondrial cyto- Laboratory Methods chrome c oxidase subunit I (COI) gene, eight cochlio- pine genera were shown to be a monophyletic group Snails were collected alive and placed directly in 90% relative to two Australian hydrobiid outgroups (Her- ethanol. Genomic DNA was extracted from these speci- shler et al., 1999). Here we analyze partial sequences of mens with the CTAB method (Bucklin, 1992). A segment this same gene from a broader spectrum of cochliopine of the mitochondrial cytochrome c oxidase subunit I gene and other taxa to more fully assess monophyly of the was amplified via polymerase chain reaction (PCR) with subfamily and to examine its relationships to other primer pairs COIL1490 and COIH2198 (Folmer et al., rissooidean snails. We also contrast phylogenetic struc- 1994) or COIL1492 and COIH2390. The COIL1492 ture within the cochliopines with previously proposed (5ЈTCA ACA AAT CAT AAA GAT ATT GGT AC3Ј)wasa morphological groupings (Hershler and Thompson, modification of COIL1490 that we developed for hydro- 1992) and briefly discuss biogeographic implications of biid snails. The COIH2390 (5ЈATA GTA GCC GCA GTA our data. AAA TAA GC3Ј) was based on published mtDNA se- quences of several mollusks (Cypraea, Katharina, and Mytilus; GenBank) and our unpublished sequences of MATERIALS AND METHODS hydrobiid snails. Approximately 100 ng of genomic DNA was used as Specimens a template for double-stranded PCRs in a 25-␮l reac- For this study we utilized partial mtCOI sequences tion solution containing each dNTP at 125 ␮M, each of 26 cochliopine species placed in 18 genera. Ten of primer at 0.5 ␮M, 0.5 unit Taq polymerase (Applied these sequences are newly reported herein and others Biosystems, Inc.), and 5 ␮l5ϫ optimizer kit buffer F were previously reported by Hershler et al. (1999). We (Invitrogen, Inc.). Reactions were amplified for 40 cy- have sampled cochliopines from all of the major geo- cles at 94°C for 1 min, 55°C for 1 min, and 72°C for 2 graphic regions where these snails occur except tropi- min. The PCR product was incubated at 37°C for 15 cal Africa (to which the genus Lobogenes is endemic), min and then at 85°C for another 15 min with 0.5 unit and we included in our analysis two or more represen- shrimp alkaline phosphatase (SAP; Amersham) and 5 tatives of each of the three subgroups of cochliopines unit exonuclease I (ExoI; Amersham) to remove re- proposed by Hershler and Thompson (1992). For 17 of maining primers and nucleotides. Approximately the cochliopine genera we analyzed 1 or 2 species and 30–70 ng of cleaned PCR product served as a template 7 species were analyzed for Tryonia to encompass the in a cycle sequencing reaction that used the Big Dye phylogenetic diversity of these snails previously re- Terminator Cycle Sequencing Ready
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