Phylogeny and Relationships of Pleurotomariid Gastropods (Mollusca: Gastropoda): an Assessment Based on Partial 18S Rdna and Cytochrome C Oxidase I Sequences
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¥A/ Molecular Marine Biology and Biotechnology (1997] 6(1), 1-20 Phylogeny and relationships of pleurotomariid gastropods (Mollusca: Gastropoda): an assessment based on partial 18S rDNA and cytochrome c oxidase I sequences M.G. Harasewych* V2 variable region of the 18S RNA. Relationships of Department of Invertebrate Zoology, National Museum the genera and species within Pleurotomariidae are of Natural History, Smithsonian Institution, fully resolved using "total molecular evidence" Waslvngton, DC 20560. U.S.A. consisting of partial sequences of 18S rDNA and COI and including data on length variation within S. Laura Adamkewicz the inserts. Department of Biology, George Mason University, Fairfax, Virginia 22030, U.S.A. Introduction Judith A. Blake, Deborah Saudek, Tracy Spriggs, and Carol J. Bult The superfamily Pleurotomarioidea is recorded The Institute for Genomic Research, Rockville, from Upper Cambrian deposits (Knight et al., 1960; Maryland 20850, U.S.A. Tracey et al., 1993) and comprises one of the oldest undisputed gastropod lineages. Its diversity at all taxonomic levels was greatest during the Paleozoic, Abstract when these animals were the most numerous, The phylogenetic position of the ancient family varied, and abundant of all gastropods. Pleurotoma- Pleurotomariidae within the Molluscan class Gas- rioideans were conspicuous components of shal- tropoda, as well as the relationships of its Recent low-water marine communities throughout the genera and species, were assessed using an iterative, Paleozoic and Mesozoic, but Cenozoic fossils are two-gene (18S rDNA and cytochrome c oxidase I) rare, occurring in deep-water facies (for review, see approach to phylogeny reconstruction. In order to Hickman, 1976). Of the approximately 1500 species orient the Pleurotomariidae within Gastropoda, par- that have been described, only 24, all members of tial 18S rDNA sequences were determined for 7 the family Pleurotomariidae, are living today. The pleurotomariid and 22 other gastropods that span Recent species are limited to tropical and temperate the major groups within the class as well as for latitudes, occurring along the margins of continen- one cephalopod and two polyplacophorans, which tal tectonic plates that bound the western shores of serve as outgroups. Cladistic analyses of a sequence the Atlantic, Pacific, and Indian Oceans as well as of approximately 450 base pairs (bp) near the 5' end along southeastern Asia, northwestern Australia, of the 18S rDNA support the monophyly of the and intervening islands (for review, see Anseeuw following higher gastropod taxa: Patellogastropoda, and Goto, 1996). All living species are members Vetigastropoda, Neritopsina, Apogastropoda, and of upper continental slope communities (approx. its subclades Caenogastropoda and Heterobranchia. 100-1000 m), most are restricted to hard substrates The 18S rDNA sequences and 579 bp of cytochrome and steep to vertical slopes, and tend to be the nu- c oxidase I (COI) analyzed separately and together, merically dominant, large gastropods in these habi- indicate that Pleurotomariidae are included within tats (Harasewych et al, 1988). Vetigastropoda but comprise a clade that is the sister Pleurotomarioideans are most readily identified group to the other families referred to this order. on the basis of having dextral, conispiral shells with Monophyly of the Pleurotomariidae is also sup- narrow, generally deep emarginations or "slits" ported by the unique presence of seven separate along their outer lips that give rise to a spiral band inserts (ranging in length from 1 to 68 bp) within the or selenizone along or near the periphery of the shell (Figure 1). The discovery of the first living pleurotomariid in 1856 prompted an era of intense '"'Correspondence should be sent to this author. anatomic scrutiny of these rare "living fossils," with *^ 1997 Blackwell Science, Inc. every new collection of specimens generating a se- // 2 M.G. Harasenych et al. Figure 1. Representatives of fossil and living Pleurotomariidae, (A) Pleurotomaria angUcus (Sowerby, 1818), type species of Pleurotomaria, lurassic. France. (B) Perotrochas quoyanus (Fischer and Bernai'di, 1856). Recent, Lesser Antilles. (C) En- teinnotrochus adansonianus (Crosse and Fischer, 1861), Recent, Lesser Antilles. Reproduced from Knight et al., 1960, pi. 131 (A) and from Ball, 1889, pi. 37 (B and C). ries of publications (for review, see Bayer, 1965). surellidae -I- Haliotidae -I- Fissurellidae), Cocculi- Pleurotomariids liave since been regarded almost noidea, Trochoidea, and the extinct Macluritoidea universally as the most primitive living gastropods and Murchinsinoidea, as well as two other "early (e.g., Thiele, 1929; Taylor and Sohl, 1962; Boss, side-branches," the patellogastropod limpets and 1982; Vaught, 1989) and appeared as such in para- the Neritopsina. Following a rapid succession of digms of gastropod evolution (e.g., Bouvier, 1887; articles providing data on new suites of anatomic Yonge, 1947; Morton and Yonge, 1964; Graham, and ultrastructural characters as well as on newly 1985; Salvini-Plawen, 1985; Brusca and Brusca, discovered taxa, Haszprunar (1988) published a hy- 1990; for a detailed review, see Bieler, 1992). The pothesis of gastropod phylogeny in which he pro- combination in pleurotomarioideans of an asym- posed the successive emergence of 13 higher taxa metrically coiled shell and symmetrically paired (Figure 2A). More recently, Ponder and Lindberg palliai organs (including gills, auricles, kidneys, (1996, 1997) published parsimony-based phyloge- and hypobranchial glands) has been regarded as netic analyses of Gastropoda based on anatomic transitional between extinct, planispirally coiled, characters (Figure 2B) that differed from Haszpru- bilaterally symmetrical ancestors, generally be- nar's hypothesis in the composition and placement lieved to be bellerophonts, and asymmetrical mod- of several key families and orders, but concurred ern gastropods. in placing the patellogastropod limpets as the sister Interest in gastropod phylogeny has had a renais- taxon to the remaining gastropods and the pleuroto- sance over the past two decades, prompted in large mariids as closely related to the trochids. part by discoveries of primitive, previously un- Few DNA sequence-based phylogenies con- known groups, primarily from deep-sea hydrother- taining more than five gastropods have been pub- mal vents, and fueled by developments of molecular lished to date (Emberton et al., 1990; Tillier et al,, techniques and software for cladistic analysis, as 1992, 1994, 1996; Rosenberg et al., 1994, 1997), all well as by the more widespread application of the based on small portions (approx. 150-700 bp) from principles of phylogenetic systematics. The first of various domains within the large ribosomal mole- the major works to reassess gastropod evolution was cule (28S rRNA). Most focused on evolutionary rela- that of Golikov and Starobogatov (1975). These au- tionships of higher taxa within Gastropoda, but thors recognized that the patellogastropod limpets, several (Tillier et al., 1992, 1994; Rosenberg et al., together with some Paleozoic groups, manifested a 1994, 1997) spanned the class as a whole. These r series of archaic characters that were neither shared studies, for the most part, supported themonophyly with nor could be derived from other gastropods. of Vetigastropoda and Apogastropoda [sensu Pon- They placed these taxa in the subclass Cyclobran- der and Lindberg, 1997 - Caenogastropoda + Het- chia to segregate them as an earl}', monophyletic erobranchia), but differed in the placement of such offshoot fi-om the remaining gastropods, and consid- basal groups as the Neritopsina (with Bivalvia in ered the pleurotomarioideans to be the most primi- Rosenberg et al, 1994, 1997) and the patellogastro- tive of the Recent forms among the remaining pod limpets. Relationships of the patellogastropod gastropod taxa. limpets have proved especially difficult to resolve, Salvini-Plawen (1980) divided the basal gastro- as they emerge as a sister group to all other Gastro- pods into the Vetigastropoda, in which he included poda (Tillier et al., 1992), as a sister group to either the Pleurotomarioidea (Pleurotomariidae + Scis- Vetigastropoda, Neomphalina -I- Apogastropoda, Molecular phylogeny of pleurotomarüd gastropods 3 Figure 2. Recent morphologj'-basecl P*TELl.DaASTPOPail* - POLVPi-rtCOPHLWA hypotheses of gastropod phylogeny. Ci>]CULWIlOAE COCíUL íUfíf^MIft - ríAUílLOIDÉA TEIELLOIÜEA - CATEUOÜASTUDPOQA NEPiTOPSIHA (A) Phylogenetic reconstruction of - LfPÇTÏLUOlDEA 1 Haszprunar (1988, Figure 5), with no- - RSSüBELLOlDEA - PtEJPOTOWAfllCrtlEA uetlGASTBOPCOA menclature and taxon rank modified/ • PISSUHELLOIDEA - TTICCMIDAE . SCis5ur4ttb<lH ueTPGASrftûPD[>rt - S99<i<Kiz»doe J updated to be comparable with that - HÍLlOTO(DE> - NEmropsiHA of (B) Ponder and Lindberg (1996a, - PLEuADTOHAnoQ^ - OOCCHlNlQtó - Vlfil idrd Figure 11.3D). Taxa listed in upper- - CyyímN3r.duif case ai'e represented in the present - CEniTHllD4E CAZWOÜBTÍÍOPDUA CAEHDGAS1 Rf^POOA study (see Table 1). The "Hot Vent - MEDTÍE^IOQLOSSA C" limpets reported by Haszprunar - 10NNC}I[>LA APOGASTBOPOOA (1988) were subsequently described - KJfiJCOIDEA - COMQ<íl£A as family Neolepetopsidae by HFTEROElñArJGHIA iVicLean (1990) and included in Patel- HFl£ftOBA4NCHm l'rRAlJiPELtOlCftA - 0PISTHüBJlAí4L^t^|.-, logastropoda by Ponder and Lindberg EUtHYMEURA - Pm.fd<ííATA (1996, 1997), or Heterobranchia (Tillier et al., 1994), or within letic. Most