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Investigating the Bivalve Tree of Life – an Exemplar-Based Approach Combining Molecular and Novel Morphological Characters

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Investigating the Bivalve Tree of Life – an Exemplar-Based Approach Combining Molecular and Novel Morphological Characters CSIRO PUBLISHING Invertebrate Systematics, 2014, 28,32–115 http://dx.doi.org/10.1071/IS13010 Investigating the Bivalve Tree of Life – an exemplar-based approach combining molecular and novel morphological characters Rüdiger Bieler A,N, Paula M. Mikkelsen B, Timothy M. Collins C, Emily A. Glover D, Vanessa L. González E, Daniel L. GrafG, Elizabeth M. HarperH, John Healy A,I, Gisele Y. Kawauchi E, Prashant P. SharmaF, Sid Staubach A, Ellen E. StrongJ, John D. Taylor D, Ilya TëmkinJ,K, John D. ZardusL, Stephanie Clark A, Alejandra Guzmán E,M, Erin McIntyre E, Paul Sharp C and Gonzalo Giribet E AInvertebrates, Field Museum of Natural History, 1400 South Lake Shore Drive, Chicago, IL 60605, USA. BPaleontological Research Institution, 1259 Trumansburg Road, and Department of Ecology & Evolutionary Biology, Cornell University, Ithaca, NY 14850, USA. CDepartment of Biological Sciences, AHC 1 Bldg, Rm 319C, Florida International University, Miami, FL 33199, USA. DDepartment of Life Sciences, The Natural History Museum, London SW7 5BD, UK. EMuseum of Comparative Zoology & Department of Organismic and Evolutionary Biology, Harvard University, 26 Oxford Street, Cambridge, MA 02138, USA. FAmerican Museum of Natural History, Division of Invertebrate Zoology, 200 Central Park West, New York City, NY 10024, USA. GUniversity of Wisconsin-Stevens Point, Biology Department, 800 Reserve Street, Stevens Point, WI 54481, USA. HDepartment of Earth Sciences, University of Cambridge, Downing Street, Cambridge, CB2 3EQ, UK. IQueensland Museum, PO Box 3300, South Brisbane, Qld 4101, Australia. JDepartment of Invertebrate Zoology, National Museum of Natural History, Smithsonian Institution, PO Box 37012, MRC 163, Washington, DC 20013, USA. KBiology Department, Northern Virginia Community College, 4001 Wakefield Chapel Road, Annandale, VA 22003, USA. LDepartment of Biology, The Citadel, 171 Moultrie Street, Charleston, SC 29409, USA. MStanford University, 300 Pasteur Drive, Stanford, CA 94305, USA. NCorresponding author. Email: rbieler@fieldmuseum.org Abstract. To re-evaluate the relationships of the major bivalve lineages, we amassed detailed morpho-anatomical, ultrastructural and molecular sequence data for a targeted selection of exemplar bivalves spanning the phylogenetic diversity of the class. We included molecular data for 103 bivalve species (up to five markers) and also analysed a subset of taxa with four additional nuclear protein-encoding genes. Novel as well as historically employed morphological characters were explored, and we systematically disassembled widely used descriptors such as gill and stomach ‘types’. Phylogenetic analyses, conducted using parsimony direct optimisation and probabilistic methods on static alignments (maximum likelihood and Bayesian inference) of the molecular data, both alone and in combination with morphological characters, offer a robust test of bivalve relationships. A calibrated phylogeny also provided insights into the tempo of bivalve evolution. Finally, an analysis of the informativeness of morphological characters showed that sperm ultrastructure characters are among the best morphological features to diagnose bivalve clades, followed by characters of the shell, including its microstructure. Our study found support for monophyly of most broadly recognised higher bivalve taxa, although support was not uniform for Protobranchia. However, monophyly of the bivalves with protobranchiate gills was the best-supported hypothesis with incremental morphological and/or molecular sequence data. Autobranchia, Pteriomorphia, Heteroconchia, Palaeoheterodonta, Archiheterodonta, Euheterodonta, Anomalodesmata and Imparidentia new clade ( = Euheterodonta excluding Anomalodesmata) were recovered across analyses, irrespective of data treatment or analytical framework. Another clade supported by our analyses but not formally recognised in the literature includes Palaeoheterodonta and Archiheterodonta, which emerged under multiple analytical conditions. The origin and diversification of each of these major clades is Cambrian or Ordovician, except for Archiheterodonta, which diverged Journal compilation Ó CSIRO 2014 www.publish.csiro.au/journals/is Investigating the Bivalve Tree of Life Invertebrate Systematics 33 from Palaeoheterodonta during the Cambrian, but diversified during the Mesozoic. Although the radiation of some lineages was shifted towards the Palaeozoic (Pteriomorphia, Anomalodesmata), or presented a gap between origin and diversification (Archiheterodonta, Unionida), Imparidentia showed steady diversification through the Palaeozoic and Mesozoic. Finally, a classification system with six major monophyletic lineages is proposed to comprise modern Bivalvia: Protobranchia, Pteriomorphia, Palaeoheterodonta, Archiheterodonta, Anomalodesmata and Imparidentia. Additional keywords: Bivalvia, evolution, gills, labial palps, Mollusca, phylogeny, shell microstructure, sperm ultrastructure, stomach. Received 15 March 2013, accepted 17 November 2013, published online 20 March 2014 Introduction (which was variously placed as Cryptodonta or Lipodonta). Bivalves constitute a commercially and ecologically important Consensus developed to break down the Autobranchia into group of molluscs related to gastropods and scaphopods (Kocot Pteriomorphia (with or without the Mytilida – the latter also et al. 2011; Smith et al. 2011) and are the second most species- classified separately as Isofilibranchia), Palaeoheterodonta rich molluscan class after Gastropoda. Their membership in the (including Trigoniida and Unionida among extant taxa), phylum Mollusca is undisputed and bivalve monophyly, Heterodonta (a large group of bivalves including Venerida and although challenged in early molecular analyses, has found Myida), as well as the Anomalodesmata (comprising an array support in more recent studies using large datasets. Bivalve of strange and highly specialised marine bivalves with mostly species have become the focus of numerous lines of prismato-nacreous shells and modified eulamellibranchiate interdisciplinary research, including the recent publication of or septibranch ctenidia that include Pholadomyida and the the draft genomes of two pteriomorphian species (Takeuchi previously mentioned Septibranchia) (e.g. Newell 1965; Amler et al. 2012; Zhang et al. 2012) and new transcriptomic 1999). The advent of cladistic methodology and molecular resources (Clark et al. 2010; Kocot et al. 2011; Milan et al. techniques allowed for reinvestigation of hypothesised 2011; Smith et al. 2011; Coppe et al. 2012). Translational medical taxa and their interrelationships. Among the new results was studies on bivalves include aging research (Ungvari et al. 2011) the recognition of Anomalodesmata as a clade nested and the discovery of new antibiotics produced by the bacterial within Heterodonta, rendering the latter subclass paraphyletic gill symbionts of shipworms (Elshahawi et al. 2013). Bivalves (e.g. Giribet and Wheeler 2002; Harper et al. 2006). have also been used as models for understanding diversification Anomalodesmata constitutes the most-basal clade of in the deep sea (Etter et al. 2005, 2011; Rex et al. 2005; Sharma Euheterodonta – an unranked clade introduced by Giribet and et al. 2013), and their rich fossil record has emerged as one of Distel (2003) for the heterodonts excluding Carditoidea and the most powerful tools for explaining global ecological and Crassatelloidea. Other previously unrecognised clades within biogeographical patterns (Jablonski et al. 2006; Mittelbach Heterodonta were also supported, such as Neoheterodontei – an et al. 2007; Krug et al. 2009; Roy et al. 2009; summarised unranked group erected by Taylor et al.(2007b) that includes by Bieler et al. 2013). Nevertheless, composition and Sphaerioidea,Myida,Gaimardioidea,Mactroidea,Ungulinoidea, interrelationships of its constituent clades have remained a Cyrenoidea ( = Corbiculoidea), Chamoidea and Veneroidea. matter of heated debate. Archiheterodonta was introduced by Giribet (2008); the name Hypotheses about the higher-level internal structure of was used by Taylor et al.(2007b) citing ‘Giribet (in press)’ for the Bivalvia have, of course, changed over time, driven by members of the superfamilies Carditoidea and Crassatelloidea corroborating and conflicting signals from character systems (the order Carditida sensu Bieler et al. 2010), which form a well derived from shell morphology (especially hinge teeth and supported clade, not nested within the more traditional muscle scars that are also recognisable in the rich fossil heterodont group, both in molecular as well as morphological record), and organisational patterns of the gills or stomachs. analyses, and are united most notably by the presence of Numerous classifications have been proposed (summarised intracellular haemoglobin and sperm ultrastructure. and compared, for example, by Newell 1965; Beesley et al. Two recent family-level classifications have attempted to 1998; Amler et al. 2000; Schneider 2001). Among the provide synopses of the bivalve system, arranging the more commonly recognised subgroups are Protobranchia (‘primitive’ than 1000 family-group names for extant and extinct Bivalvia bivalves with plesiomorphic ctenidia with a solely respiratory into a classification informed by shell-morphology, anatomy function) and Autobranchia (formerly Autolamellibranchiata and other knowledge gathered from the published literature. or Autolamellibranchia; bivalves with hypertrophied gills The two classifications differ substantially,
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