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Phylogenomics reveals deep molluscan relationships

Abstract

Evolutionary relationships among the eight major lineages of Mollusca have remained unresolved despite their diversity and importance. Previous investigations of molluscan phylogeny, based primarily on nuclear ribosomal gene sequences1,2,3 or morphological data4, have been unsuccessful at elucidating these relationships. Recently, phylogenomic studies using dozens to hundreds of genes have greatly improved our understanding of deep animal relationships5. However, limited genomic resources spanning molluscan diversity has prevented use of a phylogenomic approach. Here we use transcriptome and genome data from all major lineages (except Monoplacophora) and recover a well-supported topology for Mollusca. Our results strongly support the Aculifera hypothesis placing Polyplacophora (chitons) in a clade with a monophyletic Aplacophora (worm-like molluscs). Additionally, within Conchifera, a sister-taxon relationship between Gastropoda and Bivalvia is supported. This grouping has received little consideration and contains most (>95%) molluscan species. Thus we propose the node-based name Pleistomollusca. In light of these results, we examined the evolution of morphological characters and found support for advanced cephalization and shells as possibly having multiple origins within Mollusca.

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Figure 1: Leading hypotheses of molluscan phylogeny.
Figure 2: Relationships among major lineages of Mollusca based on 308 genes.
Figure 3: Data matrix coverage.
Figure 4: Deep molluscan phylogeny as inferred in the present study.

Accession codes

Data deposits

Capillary sequence data are available from the NCBI EST database (http://www.ncbi.nlm.nih.gov/projects/dbEST) under accession numbers JG454968.1–JG456874.1 and 454 sequence data are available from the NCBI SRA database (http://www.ncbi.nlm.nih.gov/sra) accession number SRA030407.1. Matrices and trees from this study are available from TreeBASE (http://www.treebase.org) accession number S11762.

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Acknowledgements

We thank W. Jones and K. T. Fielman for help with cDNA library preparation, R. M. Jennings, N. Mikkelsen, and the crews of the RV Håkon Mosby, RV Hans Brattstrom and RV Laurence M. Gould for assistance collecting aplacophorans, and J. C. Havird, P. J. Krug, S. C. Kempf, D. R. Lindberg, M. V. Matz, L. R. Page and T. H. Struck for discussions. D. Speiser kindly shared the photo of Argopecten. F. W. Goetz, A. Gracey and M. L. Blaxter kindly provided sequence quality data for Dreissena rostriformis, Mytilus californianus and Lumbricus rubellus, respectively. We thank A. Di Cosmo, P. Burbach, V. Rehder, W. Wright and R. Gillette for providing samples of Octopus, Loligo, Helisoma, Dolabrifera and Pleurobranchaea as well as sharing some sequencing cost for these species. We also thank D. Young and the Alabama Supercomputer Authority for access to computational resources. The genomes of Capitella teleta, Helobdella robusta, Lottia gigantea and Nematostella vectensis were produced by the US Department of Energy Joint Genome Institute in collaboration with the user community. This work was supported by National Science Foundation (NSF) grants (0744649 and 0821622) to K.M.H., National Institute of Health (NIH) grants (1RO1NS06076, 1R01GM097502, R21 RR025699, R21DA030118) and the McKnight Brain Research Foundation to L.L.M., the Deep Metazoan Phylogeny (DMP) program of the German Science Foundation (Li 998/9-1) to B.L., and The University of Bergen (Norway) free researcher initiated project grant to C.T. (project no. 226270). This work represents contributions 82 and 4 to the Auburn University (AU) Marine Biology Program and Molette Biology Laboratory for Environmental and Climate Change Studies, respectively.

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Authors

Contributions

K.M.H., C.T., B.L., C.S. and K.M.K. conceived and designed this study. K.M.H., L.L.M., B.L. and C.T. supervised cDNA preparation and sequencing. L.L.M., A.B.K., K.M.K., J.T.C. and A.M. prepared and sequenced cDNA. K.M.K., J.T.C., S.R.S. and M.R.C. developed the bioinformatics pipeline. K.M.K. performed phylogenetic and ancestral state reconstruction analyses. K.M.K. and J.T.C. prepared the figures. C.S., C.T. and K.M.K. modified the morphological character matrix. A.B.K., K.M.K. and A.M. submitted sequences to GenBank. All authors contributed in preparing the Letter.

Corresponding authors

Correspondence to Kevin M. Kocot or Kenneth M. Halanych.

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The authors declare no competing financial interests.

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This file contains Supplementary Methods, Supplementary Results, Supplementary References, Supplementary Tables 1-7 and Supplementary Figures 1-16 with legends. (PDF 14738 kb)

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Kocot, K., Cannon, J., Todt, C. et al. Phylogenomics reveals deep molluscan relationships. Nature 477, 452–456 (2011). https://doi.org/10.1038/nature10382

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