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On Bivalve Phylogeny: a High-Level Analysis of the Bivalvia (Mollusca) Based on Combined Morphology and DNA Sequence Data

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On Bivalve Phylogeny: a High-Level Analysis of the Bivalvia (Mollusca) Based on Combined Morphology and DNA Sequence Data Invertebrate Biology 12 I(4): 27 1-324. 0 2002 American Microscopical Society, Inc. On bivalve phylogeny: a high-level analysis of the Bivalvia (Mollusca) based on combined morphology and DNA sequence data Gonzalo Giribet'%aand Ward Wheeler2 ' Department of Organismic and Evolutionary Biology, Museum of Comparative Zoology, Harvard University; 16 Divinity Avenue, Cambridge, Massachusetts 021 38, USA Division of Invertebrate Zoology, American Museum of Natural History, Central Park West at 79th Street, New York, New York 10024, USA Abstract. Bivalve classification has suffered in the past from the crossed-purpose discussions among paleontologists and neontologists, and many have based their proposals on single char- acter systems. More recently, molecular biologists have investigated bivalve relationships by using only gene sequence data, ignoring paleontological and neontological data. In the present study we have compiled morphological and anatomical data with mostly new molecular evi- dence to provide a more stable and robust phylogenetic estimate for bivalve molluscs. The data here compiled consist of a morphological data set of 183 characters, and a molecular data set from 3 loci: 2 nuclear ribosomal genes (1 8s rRNA and 28s rRNA), and 1 mitochondria1 coding gene (cytochrome c oxidase subunit I), totaling -3 Kb of sequence data for 76 rnollu bivalves and 14 outgroup taxa). The data have been analyzed separately and in combination by using the direct optimization method of Wheeler (1 996), and they have been evaluated under 1 2 analytical schemes. The combined analysis supports the monophyly of bivalves, paraphyly of protobranchiate bivalves, and monophyly of Autolamellibranchiata, Pteriomorphia, Hetero- conchia, Palaeoheterodonta, and Heterodonta s.I., which includes the monophyletic taxon An- omalodesmata. These analyses strongly support the conclusion that Anomalodesmata should not receive a class status, and that the heterodont orders Myoida and Veneroida are not mono- phyletic. Among the most stable results of the analysis are the monophyly of Palaeoheterodonta, grouping the extant trigoniids with the freshwater unionids, and the sister-group relationship of the heterodont families Astartidae and Carditidae, which together constitute the sister taxon to the remaining heterodont bivalves. Internal relationships of the main bivalve groups are dis- cussed on the basis of node support and clade stability. Additional key words: Moll~sca,Bivalvia, Palaeoheterodonta, Heteroconchia, Heterodonta, 18s rRNA, 28s rRNA, cytochrome c oxidase I, morphology, direct optimization, scnsitivity analysis Bivalve molluscs are characterized by a laterally ciliated labial palps connect the ctenidia to the mouth, compressed body with an external bivalved shell that and direct food particles into it. The extensible foot is is hinged dorsally. The valves are connected by a par- either elongated or laterally compressed. tially calcified elastic ligament and are held together These modifications from the plesiomorphic mol- by 1 or 2 adductor muscles. There is no buccal or luscan condition have made it difficult to establish a radular apparatus, and the mantle lobes are either phylogenetic scheme of the group. The problems arise joined or free ventrally. The spacious mantle cavity from the difficulty in homologizing certain structures extends upwards on each side of the visceral mass and useful for bivalve taxonomy that are not present in the contains a pair of ctenidia suspended laterally. The cte- other molluscan classes. Paleontologists and neontol- nidia may be enlarged, lamellate and plicate. The ogists have disputed the monophyly and phylogenetic mouth and anus are located at opposite ends of the position of many groups, such as Anomalodesmata, body and the gut is typically convoluted. A pair of Protobrdnchia, and Palaeoheterodonta, while others us- ing molecular sequence data have openly questioned a Author for correspondence. the monophyly of Heterodonta, as well as the orders E-mail: ggiribet @ oeb.harvard.edu Veneroida and Myoida. 272 Giribet & Whceler There have been several concerted attempts to re- laeotaxodonta (= Nuculoidea and Nuculanoidea), solve the contradictory systems of classification of bi- Cryptodonta (= Solemyoida), Pteriomorphia, Palaeo- valves proposed by paleontologists and neontologists. heterodonta, Heterodonta, and Anomalodesmata. Pur- C.M. Yonge and T.E. Thompson organized the sym- chon (1978) compiled a data matrix of 9 characters for posium Evolutionary Systematics of Bivalve Molluscs, 40 taxa (superfamilies) of bivalves that was analyzed which was published in 1978 (Phil. Trans. R. Soc. using a phenetic computer algorithm. Following an ex- Lond. B 284: 199-436). Two decades later, paleon- panded analysis (Purchon 1987b), bivalves werc di- to I ogi sts, neontol og ists, and molecular biologists pro- vided into 2 subclasses, Protobranchia and Lamelli- vided additional insights into bivalve phylogeny at the branchia, the latter containing 4 orders: Pteriomorphia, International Symposium on the Paleobiology and Mesosyntheta (= Trigonioida and Unionoida [includ- Evolution of the Bivalvia (Johnston & Haggart 1998) ing also Crassatelloidea, Carditoidea, and Leptonoi- and at a meeting on The Biology and Evolution of the deal), Anomalodesmata, and Gastropempta (= Bivalvia (Harper et al. 2000b).These efforts have not Heterodonta) (Fig. 1A). yet produced a single combination of morphological For the purposes of the present study, we lollow thc and molecular data, and conflicting hypotheses of bi- classification system of Beesley et al. (1998). Thus, a valve evolution remain. It is our aim to investigate classification system of 5 subclasses is followed prior previously proposed hypotheses by analyzing morpho- to the phylogenetic analyses. This classification is gen- logical and molecular characters of all the extant erally corroborated by the morphological analysis oc bivalve orders in a total-evidence framework. Waller (1998). Taxon names currently in use in the literature are noted where needed. This classification Previous classification systems of bivalves includes the following subclasses; representatives used in this study are listed in Table 2. Comparative anatomical studies of living bivalves Subclass Protobranchia. The classification of the have led to several classification schemes. Cox (1960) Protobranchia is unstable (Reid 1998). Nuculoidea and provided an excellent historical review of early at- Nuculanoidea are considered superfamilies of the or- tempts to classify the bivalves. Ridewood (1 903) rec- der Nuculoida by several authors, although certain ognized 3 orders of bivalves (Protobranchia, Eleuth- phylogenetic studies have suggested non-monophyly erorhabda, and Synaptorhabda) based on gill structure. of Nuculoida (Waller 1990, 1998; Morton 1996). Pelseneer (1906, 19 1 1) developed another system of Therefore, we have used the superfamilies Solemy- classification based on 5 grades of gill structure and oidea (2 species of Solemya), Nuculoidea (4 species of assigned ordinal status to each grade: Protobranchia, Nuculidae), and Nuculanoidea (2 species of Nuculan- Filibranchia, Pseudolamellibranchia, Eulamellibran- idae, 2 species of Yoldiidae, and 1 of Neilonellidae). chia, and Septibranchia. Iredale (1939) added the order Subclass Pteriomorphia (= Filibranchia). Five Isofilibranchia to distinguish the mytiloids, which he orders are recognized in this classification: Mytiloida, considered to differ sufficiently in gill structure from Arcoida, Pterioida, Limoida, and Ostreoida. Pojeta the other members of Filibranchia. Atkins (1 938) de- 978) separated mytiloids as a distinct subclass (Iso- scribed two types of latero-frontal ciliation on gill fil- (I aments and proposed division of the class into 2 filibranchia), but Waller (1 998) recognized the cate- groups, the Macrociliobranchia and Microciliobran- gory Pteriomorphia, regarding Mytiloida as the sister chia. Later workers proposed that other structures be group to the other pteriomorphs. Representatives of the used in classifying bivalves (stomach: Purchon 1960, 5 orders have been examined in this study. 1963, 1968; ctenidial-labial palp associations: Stasek Subclass Palaeoheterodonta. This group is com- 1963). Scarlato & Starobogatov (1975, 1978, 1979) posed of 2 orders, Trigonioida and Unionoida. How- and Starobogatov (1992) recognized 3 superorders of ever, some authors do not support the monophyly of bivalves, the Nuculiformii (= Protobranchia), Mytili- the group (e.g., Salvini-Plawen & Steiner 1996). Our forniii, and Conocardiiformii (= Anomalodesmata). In study includes representatives of both orders (2 this new classification, Mytiliformii contained unionids and 2 trigoniids). pteriomorphs, palaeoheterodonts, and heterodonts. Subclass Heterodonta. Classification of Hetero- Classifications based on single-character systems donta has not been resolved, even at the ordinal level have been criticized (Cox 1960; Newell 1965, 1969). (Prezant 1998). Heterodonta (as accepted by Vokes Newell (1965, 1969) summarized the available evi- 1968; Cox 1969; Newell 1969; Beesley et al. 1998) dence on shell structure and anatomy and presented a consists of 3 orders: the extinct Hippuritoida and the classification of Bivalvia that is now generally in use. extant Veneroida and Myoida. The large order Vene- In his scheme, 6 subclasses were recognized: the Pa- roida comprises - I8 superfamilies, of which IS are On bivalve phylogeny 27 3 Nuculoidca Nucincllidae Nuculanoidea
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