Downloaded from http://sp.lyellcollection.org/ at CAPES on July 12, 2013 Geological Society, London, Special Publications On becoming cemented: evolutionary relationships among the genera in the freshwater bivalve family Etheriidae (Bivalvia: Unionoida) Arthur E. Bogan and Walter R. Hoeh Geological Society, London, Special Publications 2000, v.177; p159-168. doi: 10.1144/GSL.SP.2000.177.01.09 Email alerting click here to receive free e-mail alerts when service new articles cite this article Permission click here to seek permission to re-use all or request part of this article Subscribe click here to subscribe to Geological Society, London, Special Publications or the Lyell Collection Notes © The Geological Society of London 2013 Downloaded from http://sp.lyellcollection.org/ at CAPES on July 12, 2013 On becoming cemented: evolutionary relationships among the genera in the freshwater bivalve family Etheriidae (Bivalvia: Unionoida) ARTHUR E. BOGAN 1 & WALTER R. HOEH 2 INorth Carolina State Museum of Natural Sciences, Research Laboratory, 4301 Reedy Creek Road, Raleigh, NC 27607, USA (e-mail: arthur.bogan @ncmail, net) 2Department of Biological Sciences, Kent State University, Kent, 0H44242, USA Abstract: A robust phylogeny for the Unionoida is emerging and presumed relationships of some major clades are being questioned. The Etheriidae or freshwater oysters has been a distinct family for over 160 years and currently contains three cemented genera: Acostaea (Columbia, South America), Pseudomulleria (India) and Etheria (Africa and Madagascar). Starobogatov (1970, Nauka, 1-372), Mansur and da Silva (1990, Amazoniana, 11(2), 147-166) and Bonetto (1997, Bioci~ncias, 5, 113-142) present conflicting testable hypotheses regarding the evolution of these taxa. Using cytochrome c oxidase subunit I DNA sequences the evolutionary relationships of these three genera has been examined, by comparing them to representatives of 30 other unionoid taxa from around the world. These analyses place Acostaea and Etheria within the Mycetopodidae while Pseudomulleria falls within the Unionidae. A monophyletic Etheriidae, composed of cemented freshwater bivalves, is not supported by the present analyses. Furthermore, the analyses indicate that cementation in the Unionoida has evolved at least twice. In a paper which discusses the evolution of been debated (see Discussion). Most malacologists cementing bivalves, Yonge (1979) identified the recognize three cemented genera in the variety, origin and problems of convergence in Etheriidae: Acostaea (Columbia, South America), them, finding that over 20 families of bivalves have Pseudomulleria (India) and Etheria (Africa and become cemented. This paper focuses on a group of Madagascar). bivalves which has become cemented in freshwater, Prashad (1931) examined the convergence in the namely, the freshwater oysters (Unionoida: forms of the freshwater bivalve fauna of Southeast Etheriidae). Asia and compared it with similar fauna from South Bivalves found in freshwater environments America. At that time, he felt that the Unionoidea represent families from most of the major bivalve was polyphyletic and the Mutelidae with a taxodont subclasses (Bogan 1993). The greatest diversity in hinge was derived from the Arcidae. He suggested freshwater bivalves is found in the radiation of the that the Etheriidae relationships were undoubtedly Unionoida. Currently this order is divided into two with the Unionidae and that they were not related to superfamilies, six families and, it is estimated here, the Mutelidae. Prashad also noted the similarities of approximately 180 genera. The two major modern Etheria, Acostaea and Pseudomulleria but felt they unionoid radiations occurred in the southeastern all belonged to distinct genera with independent United States (Bogan 1993, 1998; Williams et al. origins and observed that 'the Etheriidae present 1993) and China (Liu 1979). Our understanding of the most noteworthy examples of the parallel evolutionary relationships within the Unionoida is evolution of similar forms from distinct ancestral based primarily on comparative anatomy (e.g. types, living under identical conditions in widely Simpson 1900, 1914; Ortmann 1912; Parodiz & separated countries.' Prashad's ideas represent the Bonetto 1963; Heard & Guckert 1970). multiple origins hypothesis for the evolution of The family Etheriidae has been recognized as a cementation in the Unionoida. distinct taxon for well over 160 years (e.g. In contrast, Yonge (1978, p. 446), in discussing Deshayes 1830; Tryon 1884; Fischer 1886; Thiele Acostaea and the evolution of the Etheriidae, 1934; Starobogatov 1970) but the evolutionary posited, 'Certainly Acostaea and Pseudomulleria relationships of this family to other unionoid must have arisen from a common dimyarian stock; families, and among its constituent genera, have the mode of growth and of assumption of the From: HARPER,E. M., TAYLOR, J. D. & CRAME,J. A. (eds) The Evolutionary Biology of the Bivalvia. Geological Society, London, Special Publications, 177, 159-168. 1-86239-076-2/00/$15.00 9 The Geological Societyof London 2000. Downloaded from http://sp.lyellcollection.org/ at CAPES on July 12, 2013 160 A.E. BOGAN & W. R. HOEH monomyarian condition are too remarkable for was originally described in Mulleria F6russac, convergence to be contemplated.' Yonge (1978) 1823 [non Leach 1814] and subsequently moved to claimed that Acostaea, Etheria and Pseudomulleria Acostaea Orbigny, 1851. Acosmea is known from were, in fact, each others closest relatives and so a the Rio Magdalena in Columbia, South America. monophyletic Etheriidae was supported. This is the Arteaga Sogamoso (1994) discovered that the single origin hypothesis for the genesis of larvae ofAcosataea rivoli is a lasidium which, from cementation in the Unionoida. the diagnoses of the family Mycetopodidae, would argue that Acostaea belongs in this family. The anatomy of Etheria elliptica Lamarck, 1807 has been reported, illustrated and discussed by Development of a unionoid phylogeny Rang & Cailliaud (1834) and Anthony (1905, Recent work on the evolutionary relationships 1907). Heard & Vail (1976) examined the anatomy among unionoid higher taxa has progressed from of Etheria elliptica and suggested that it belongs in the efforts of Parodiz & Bonetto (1963) and Heard the South American family Mycetopodidae. & Guckert (1970) to the immunoelectrophoretic Etheria elliptica is widespread in Africa: the basins analyses of Davis & Fuller (1981). The cladistic of the Nile, Lake Tanganyika and Lake Victoria; the analysis of 16S DNA and morphology data sets basins of the Chad, Zaire, Niger and Senegal; part presented by Lydeard et al. (1996) has clarified of the rivers in Angola and north Madagascar phylogenetic relationships among a number of (Daget 1998); and it is known from the Miocene of North American unionoid genera, but did not northeast Zaire (Gautier 1965; Gautier & Van include potentially closely related taxa from other Damme 1973). continents or a suitable outgroup taxon. Specimens of Pseudomulleria dalyi (Smith Hoeh et al. (1998b) examined the higher level 1898), from the Budra Drainage, Kadur district, relationships of the Unionoida based on cyto- State of Mysore, southern India, were initially chrome c oxidase subunit I (COI) sequences and placed in the genus Mulleria and in the family supported the hypothesis that Neotrigonia Etheriidae. Smith (1898) observed that P. dalyi was (Trigonioida: Trigoniidae) is the sister group to a cemented by either the right or the left valves. monophyletic Unionoida. These conclusions Woodward (1898), in the same volume, carefully support the monophyly of the Palaeoheterodonta described the anatomy of Pseudomulleria dalyi, (Trigonioida + Unionoida) as proposed by Waller reported the monomyarian condition and noted that (1990, 1998), Hoeh et al. (1998a) presented a COI the rectum no longer passed through the heart. sequence-based phylogeny for the Unionoida Woodward (1898) presented a cross-section including 30 taxa representing five families diagram of the anatomy and figured the coiling of (excluding representatives of the Etheriidae). Their the intestine. The intestinal coiling, as figured by analyses suggest that the hyriids, not margariti- Woodward, appears very similar to the intestinal ferids, are a product of the most basal cladogenic coiling of examined North American Unionidae event within the Unionoida and that the glochidial (AEB, personal observations). Woodward (1898) larvae is the ancestral larval type. The margariti- concluded '... the details of the gills, the mantle ferids, mycetopodids, iridinids and hyriids were all lobes, and the kidney, Mulleria [= Pseudomulleria] depicted as monophyletic groups, with the approximates to the Unionidae.' However, Preston Unionidae being paraphyletic. Hoeh et al. (2001) (1915) placed Mulleria dalyi in the Etheriidae and have expanded on the data presented in Hoeh et al. cited extensively from Woodward on the anatomy. (1998a) by adding a morphological data set of 28 The most recent coverage of the freshwater characters and produced a total evidence-based molluscan fauna of India by Subba Rao (1989) phylogeny for the Unionoida. The total evidence follows the taxonomy of the family put forward by analysis supported the earlier phylogeny and Thiele (1934), recognizing Pseudomulleria as a character evolution hypotheses of Hoeh et al. subgenus of Acostaea. (1998a). If it is assumed that the tree based on the Yonge (1953) recognized a single genus
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