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Phylogenetic Relationships Within the North American Hydrobiid Snail Genus Tgonia: Taxonomic and Biogeographic Implications

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Phylogenetic Relationships Within the North American Hydrobiid Snail Genus Tgonia: Taxonomic and Biogeographic Implications Phylogenetic Relationships Within the North American Hydrobiid Snail Genus Tgonia: Taxonomic and Biogeographic Implications Robert Hershleri , Hsiu-Ping Liu2, and Margaret Mulvey3 'Department of Invertebrate Zoology, National Museum of Natural History, Smithsonian Institution, Washington, D.C. 20560; 2Department of Biology, Olin Hall, Colgate University Hamilton, NY 13346; 3Savannah River Ecology Laboratory, P.O. Drawer E, Aiken, South Carolina 29802. Introduction The aquatic biota of western North America is of interest from the standpoint of evolutionary biology and biogeography because elements often are profoundly isolated by inhospitable deserts and mountain ranges, live in extremely restricted and/or harsh environments, and present distributional and phylogenetic patterns which have been molded by the extremely complex and dynamic(Cenozoi physical history of the region. Biotic distributions and evolutionary relationships may also provide clues as to early regional drainage relationships for which geological evidence often/has been obscured by subsequent deposition, deformation and erosion. Whereas early regional biogeographic treatments of fishes (e.g., Hubbs and Miller 1948; Hubbs 1974) focused on dispersal opportunities afforded by a highly integrated late Pleistocene "pluvial" drainage, Minckley et al. (1986) accepted great antiquity (Oligocene- Miocene) of this fauna and consequently emphasized the complex role of geological events in effecting vicariance, and the likelihood that fishes have been introduced to and/or transferred within the region by rafting on allochthonous terranes, intra-continental microplates, and other tectonically displaced or extended crustal fragments. The limited phylogenetic data then available for western American fishes demonstrated partial congruence with hypotheses for historical area relationships advanced by these authors, although they emphasized the need for additional Sich studies. While this work seemingly set the stage for a new era in biogeographic study of western American fishes and other aquatic biota, few pertinent phylogenetic hypotheses have since been generated, and these have focused almost exclusively on one group, fishes (e.g., Echelle and Dowling 1992; Smith 1992; but also see Hendrickson 1986). Freshwater mollusks have figured prominently in the development of provocative, albeit non-phylogenetic hypotheses for western American aquatic biogeography (e.g., Taylor 1985). Few elements of this biota have as much potential for evolutionary and biogeographic inquiry as the family Hydrobiidae, which is the most diverse group of freshwater snails in North America2' with about 35 genera and 285 described species (Turgeon et al. In Press). Hydrobiids are ubiquitous and locally abundant in many freshwater ecosystems of the West. These small benthic snails are obligately aquatic and disperse but slowly, features which link them tightly with drainage history (Taylor and Bright 1987) and, together with their antiquity (the regional age of the family is minimally Paleogene; Taylor 1985), make them ideal tools Col evaluating biotic response to vicariance. \Howeveta paucity of rigorously proposed phylogenetic hypotheses has i:trevented use of hydrobiids in such studies. One of the most speciose groups of western hydrobiids is the genus Tryonia, which is composed of at least 22 Recent species (Hershler and Thompson 1992). Most of these snails are locally endemic in major drainages of the Southwest and sympatry of congeners is rare, suggesting that the phylogeny of Tryonia may be informative with respect to regional historical biogeography. The Great Basin contains eight unique congeners, while smaller numbers of species are endemic to the Pecos River-Rio Grande (six), Gila River (one), and Colorado River (one) drainages. The uniquely parthenogenetic T. protea (unpublished) lives in both the Great Basin and Colorado River drainage, while additional species live along the Pacific (T. imitator) and Gulf of California (T. quitobaquitae) coasts. Tryonia also is represented by two broadly disjunct species in peninsular Florida, and a poorly known fauna in northern Mexico, whose sole described representative, T. hertleini, went extinct several decades ago following drying of the springs at its type locality. The possibility that congeners early ranged into Central America and northern South America is suggested by regional Neogene fossils (Taylor 1966; also see Wesselingh 1996; Wesselingh et al. 1996), although allocations of these to Tryonia are controversial (Nuttall 1990). Tryonia typically lives in inland, thermal springs, and some species are salt tolerant: T. sauna, for instance, lives in Cottonball Marsh in Death Valley, in which salinities range up to several times that of seawater (LaBounty and Deacon 1972). Floridian species live in lakes as well as springs (Thompson 1968) while T. imitator lives in coastal strand habitats and tolerates a 2 broad range of salinity regimes (Kellogg 1985). Tryonia also is of interest because it closely parallels patterns of distribution and endemism documented for one of the better studied groups of western fishes, the genus Cyprinodon (pupfish; Miller 1981). As with the overwhelming majority of the Hydrobiidae, scope and content of Tryonia have not been established within a phylogenetic context. In a recent review of the hydrobiid subfamily Cochliopinae (Hershler and Thompson 1992), Tryonia was placed in the informal "Littoridina group" along with 12 other New World genera in which males have glandular papillae on the penis; Mexipyrgus, locally endemic in northern Mexico, was conjectured as its closest relative. Tryonia has been loosely defined on the basis of a few distinctive (but not demonstrably synapomorphic) shell and genitalic features (Taylor 1966; Hershler and Thompson 1992), and even these details have not been published for most of the species currently allocated to the genus. Specific hypotheses of congener relationships have been proposed on the basis of patterns of penial ornament (Taylor 1985, 1987; Hershler 1989). The cosmopolitan distribution of the Cochliopine suggests that this group arose during the late Mesozoic and main sub-groups diverged prior to late Triassic to early Jurassic break-up of Laurasia (Hershler and Thompson 1992). The fossil record of Tryonia, although not overly useful given the weak phylogenetic signal provided by hydrobiid shells (Taylor 1987), nevertheless suggests a minimal Miocene age for the genus, based on fossils from the Mint Canyon Formation (southwest California) identified as T. imitator (Kew 1924; Oakenshott 1958). The possibility of an even more ancient origin is suggested by high-spired shells resembling Tryonia in early post-Laramide lake beds of the West (e.g., Paleocene-Eocene Flagstaff Formation; La Rocque 1960), although affinities of these are uncertain (Taylor 1975) and in need of more study. Taylor (1987) conjectured that extant species of Tryonia are generally of Miocene age. In order to provide a robust framework for biogeographical analysis of Tryonia, we are examining the monophyly and evolutionary structure of the genus using mitochondrial DNA seqUences. In a preliminary study, sequences from the cytochrome c oxidase subunit I (COI) gene were used to generate a robust phylogeny for species of the Death Valley system, (Hershler et al. submitted). Herein we analyze DNA sequence variation for this gene for the remaining congeners. We evaluate monophyly of Tryonia, propose a hypothesis of phylogenetic 3 relationships within the genus, and evaluate congruence of Tryonia biogeography with historical area relationships implied by geological history of the West. Materials and Methods Specimens Sequence data for species from the Death Valley region are from Hershler et al. (submitted). We also analyzed all other species currently allocated to Tryonia, as well as three undescribed species (two from the Great Basin and on:-.) fiom the coastal plain of Alabama) conforming to the genus in general features. Effort to collect suitable material proved unsuccessful only in the case of T. brunei, which we were unable to find at its single known locality in wesei'exasA (Taylor 1987). In order to test monophyly of Tryonia, we also analyzed other members of the "Littoridina group" (Aphaostracon, Littoridinops, Mexipyrgus, Onobops, Pyrgophorus) as well as representatives of the presumably more distantly related "Heleobia group" (Heleobia, Heleobops). Australasian taxa (Ascorhis, Phrantela) considered among the more plesiomorphic hydrobiids (Ponder and Clark 1988; Ponder et al. 1993) were used as outgroups (trees were rooted with Phrantela). Multiple samples were analyzed for several species of Tryonia (including the more widespread congeners) to evaluate intra-specific variation. Taxa and localities are listed in Table 1 and sampling localities for Tryonia are in Figure 1. All analyzed specimens were live-collected in the field, and either placed directly into concentrated ethanol or flash-frozen in a portable liquid nitrogen cannister. Voucher material from these samples is reposited in the Recent mollusk collection of the National Museum of Natural History (USNM). Laboratory Methods Genomic DNA was extracted from entire frozen snails using the Chelex method of Walsh et al. (1991), while the CTAB extraction method (Bucklin 1992) was used for ethanol-preserved specimens. A 710 base pair segment of mitochondrial gene was amplified via polymerase chain reaCtion (PCR) using primers COIL 1490 and COIH
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