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Resolving the evolutionary relationships of molluscs with phylogenomic tools

Nature volume 480, pages 364–367 (2011)Cite this article

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A Corrigendum to this article was published on 28 November 2012

This article has been updated

Abstract

Molluscs (snails, octopuses, clams and their relatives) have a great disparity of body plans and, among the animals, only arthropods surpass them in species number. This diversity has made Mollusca one of the best-studied groups of animals, yet their evolutionary relationships remain poorly resolved1. Open questions have important implications for the origin of Mollusca and for morphological evolution within the group. These questions include whether the shell-less, vermiform aplacophoran molluscs diverged before the origin of the shelled molluscs (Conchifera)2,3,4 or lost their shells secondarily. Monoplacophorans were not included in molecular studies until recently5,6, when it was proposed that they constitute a clade named Serialia together with Polyplacophora (chitons), reflecting the serial repetition of body organs in both groups5. Attempts to understand the early evolution of molluscs become even more complex when considering the large diversity of Cambrian fossils. These can have multiple dorsal shell plates and sclerites7,8,9,10 or can be shell-less but with a typical molluscan radula and serially repeated gills11. To better resolve the relationships among molluscs, we generated transcriptome data for 15 species that, in combination with existing data, represent for the first time all major molluscan groups. We analysed multiple data sets containing up to 216,402 sites and 1,185 gene regions using multiple models and methods. Our results support the clade Aculifera, containing the three molluscan groups with spicules but without true shells, and they support the monophyly of Conchifera. Monoplacophora is not the sister group to other Conchifera but to Cephalopoda. Strong support is found for a clade that comprises Scaphopoda (tusk shells), Gastropoda and Bivalvia, with most analyses placing Scaphopoda and Gastropoda as sister groups. This well-resolved tree will constitute a framework for further studies of mollusc evolution, development and anatomy.

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Figure 1: Selected hypotheses of extant molluscan relationships and relevant taxa.
Figure 2: Phylogram of the RAxML maximum likelihood analysis of the big matrix (216,402 amino acids) under the WAG+Γ model.

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Accession codes

Primary accessions

Sequence Read Archive

Data deposits

Illumina and 454 reads have been deposited in the National Center for Biotechnology Information (NCBI) Sequence Read Archive under accession number SRA044948. Sanger reads for Laevipilina hyalina have been deposited in the NCBI Trace Archive under the sequencing centre name BUDL with TI range 2317135955-2317139410. The assembled data, matrices and trees have been deposited in Dryad (http://dx.doi.org/10.5061/dryad.24cb8).

Change history

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Acknowledgements

This research was supported by the US National Science Foundation through the Systematics Program (awards 0844596, 0844881 and 0844652), the AToL Program (EF-0531757), EPSCoR (Infrastructure to Advance Life Sciences in the Ocean State, 1004057) and the iPlant Collaborative (0735191). Support was also provided by the Scripps Institution of Oceanography, the University of California Ship Funds and the Museum of Comparative Zoology. Collecting in Greenland was supported by the Carlsberg Foundation. A. Riesgo and J. Harasewych provided tissue samples of Octopus and Perotrochus, respectively. E. Röttinger assisted with Nautilus. C. Palacín allowed us to use an Octopus vulgaris photograph. At Brown University, Illumina sequencing was enabled by the Genomics Core Facility, and computational analyses were facilitated by L. Dong and the Center for Computing and Visualization. At Harvard University, Illumina sequencing was enabled by the Bauer Core in the Faculty of Arts and Sciences (FAS) Center for Systems Biology, and analyses were supported by the staff of the Research Computing cluster Odyssey facility in the FAS.

Author information

Authors and Affiliations

  1. Department of Ecology and Evolutionary Biology, Brown University, Providence, 02912, Rhode Island, USA

    Stephen A. Smith, Freya E. Goetz, Caitlin Feehery & Casey W. Dunn

  2. Heidelberg Institute for Theoretical Studies, Heidelberg D-69118, Germany,

    Stephen A. Smith

  3. The Australian Museum, Sydney, 2010, New South Wales, Australia

    Nerida G. Wilson

  4. Scripps Institution of Oceanography, University of California San Diego, La Jolla, 92093, California, USA

    Nerida G. Wilson, Caitlin Feehery & Greg W. Rouse

  5. Department of Organismic and Evolutionary Biology, Museum of Comparative Zoology, Harvard University, Cambridge, 02138, Massachusetts, USA

    Sónia C. S. Andrade & Gonzalo Giribet

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  1. Stephen A. Smith
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Contributions

C.W.D., G.G. and N.G.W. conceived of and oversaw the study. S.A.S. and C.W.D. designed and implemented the data analyses. N.G.W., G.G. and G.W.R. collected the specimens. F.E.G., S.C.S.A. and C.F. prepared the specimens for sequencing. S.A.S., C.W.D., G.G., G.W.R. and N.G.W. wrote the manuscript. All authors read and provided input into the manuscript and approved the final version.

Corresponding authors

Correspondence to Nerida G. Wilson, Gonzalo Giribet or Casey W. Dunn.

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The authors declare no competing financial interests.

Supplementary information

Supplementary Information

The file contains Supplementary Figures 1-9 with legends and Supplementary Table 1. This file contains updated versions of Supplementary Figures 2-9 and was replaced online on 28 November 2012 (see Corrigendum doi:10.1038/nature11736 for details). (PDF 489 kb)

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Smith, S., Wilson, N., Goetz, F. et al. Resolving the evolutionary relationships of molluscs with phylogenomic tools. Nature 480, 364–367 (2011). https://doi.org/10.1038/nature10526

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