Invertebrate Systematics Invertebrate Systematics Society
Systematics, phylogeny and biogeography
RESEARCH ARTICLE (Open Access)

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. Graf G , Elizabeth M. Harper H , John Healy A I , Gisele Y. Kawauchi E , Prashant P. Sharma F , Sid Staubach A , Ellen E. Strong J , John D. Taylor D , Ilya Tëmkin J K , John D. Zardus L , Stephanie Clark A , Alejandra Guzmán E M , Erin McIntyre E , Paul Sharp C and Gonzalo Giribet E

A Invertebrates, Field Museum of Natural History, 1400 South Lake Shore Drive, Chicago, IL 60605, USA.

B Paleontological Research Institution, 1259 Trumansburg Road, and Department of Ecology & Evolutionary Biology, Cornell University, Ithaca, NY 14850, USA.

C Department of Biological Sciences, AHC 1 Bldg, Rm 319C, Florida International University, Miami, FL 33199, USA.

D Department of Life Sciences, The Natural History Museum, London SW7 5BD, UK.

E Museum of Comparative Zoology & Department of Organismic and Evolutionary Biology, Harvard University, 26 Oxford Street, Cambridge, MA 02138, USA.

F American Museum of Natural History, Division of Invertebrate Zoology, 200 Central Park West, New York City, NY 10024, USA.

G University of Wisconsin-Stevens Point, Biology Department, 800 Reserve Street, Stevens Point, WI 54481, USA.

H Department of Earth Sciences, University of Cambridge, Downing Street, Cambridge, CB2 3EQ, UK.

I Queensland Museum, PO Box 3300, South Brisbane, Qld 4101, Australia.

J Department of Invertebrate Zoology, National Museum of Natural History, Smithsonian Institution, PO Box 37012, MRC 163, Washington, DC 20013, USA.

K Biology Department, Northern Virginia Community College, 4001 Wakefield Chapel Road, Annandale, VA 22003, USA.

L Department of Biology, The Citadel, 171 Moultrie Street, Charleston, SC 29409, USA.

M Stanford University, 300 Pasteur Drive, Stanford, CA 94305, USA.

N Corresponding author. Email: rbieler@fieldmuseum.org

Invertebrate Systematics 28(1) 32-115 http://dx.doi.org/10.1071/IS13010
Submitted: 15 March 2013  Accepted: 17 November 2013   Published: 20 March 2014

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 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.


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