Phylogenomics reveals deep molluscan relationships (original) (raw)
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.
References
- Passamaneck, Y. J., Schander, C. & Halanych, K. M. Investigation of molluscan phylogeny using large-subunit and small-subunit nuclear rRNA sequences. Mol. Phylogenet. Evol. 32, 25–38 (2004)
Article CAS Google Scholar - Giribet, G. et al. Evidence for a clade composed of molluscs with serially repeated structures: Monoplacophorans are related to chitons. Proc. Natl. Acad. Sci. USA 103, 7723–7728 (2006)
Article ADS CAS Google Scholar - Wilson, N. G., Rouse, G. W. & Giribet, G. Assessing the molluscan hypothesis Serialia (Monoplacophora+ Polyplacophora) using novel molecular data. Mol. Phylogenet. Evol. 54, 187–193 (2010)
Article Google Scholar - Haszprunar, G. Is the Aplacophora monophyletic? A cladistic point of view. Am. Malacol. Bull. 15, 115–130 (2000)
Google Scholar - Dunn, C. W. et al. Broad phylogenomic sampling improves resolution of the animal tree of life. Nature 452, 745–749 (2008)
Article ADS CAS Google Scholar - Haszprunar, G., Schander, C. & Halanych, K. M. In Phylogeny and Evolution of the Mollusca (eds Ponder, W. & Lindberg, D. R. ) 19–32 (Univ. of California Press, 2008)
Google Scholar - Todt, C., Okusu, A., Schander, C. & Schwabe, E. In Phylogeny and evolution of the Mollusca (eds Ponder, W. & Lindberg, D. R. ) 105–141 (Univ. of California Press, 2008)
Google Scholar - Scheltema, A. H. Aplacophora as progenetic aculiferans and the coelomate origin of mollusks as the sister taxon of Sipuncula. Biol. Bull. 184, 57–78 (1993)
Article CAS Google Scholar - Salvini-Plawen, L. On the phylogenetic significance of the aplacophoran Mollusca. Iberus 21, 67–97 (2003)
Google Scholar - Meyer, A., Todt, C., Mikkelson, N. & Lieb, B. Fast evolving 18S rRNA sequences from Solenogastres (Mollusca) resist standard PCR amplification and give new insights into mollusk substitution rate heterogeneity. BMC Evol. Biol. 10, 70 (2010)
Article Google Scholar - Struck, T. H. et al. Phylogenomic analyses unravel annelid evolution. Nature 471, 95–98 (2011)
Article ADS CAS Google Scholar - Sigwart, J. D. & Sutton, M. D. Deep molluscan phylogeny: synthesis of palaeontological and neontological data. Proc. R. Soc. B 274, 2413–2419 (2007)
Article Google Scholar - Scheltema, A. H. & Ivanov, D. L. An aplacophoran postlarva with iterated dorsal groups of spicules and skeletal similarities to Paleozoic fossils. Invertebr. Biol. 121, 1–10 (2002)
Article Google Scholar - Nielsen, C., Haszprunar, G., Ruthensteiner, B. & Wanninger, A. Early development of the aplacophoran mollusc Chaetoderma. Acta Zool. 88, 231–247 (2007)
Article Google Scholar - Todt, C. & Wanninger, A. Of tests, trochs, shells, and spicules: Development of the basal mollusk Wirenia argentea (Solenogastres) and its bearing on the evolution of trochozoan larval key features. Front. Zool. 7, 6 (2010)
Article Google Scholar - Scheltema, A. H. & Schander, C. Exoskeletons: tracing molluscan evolution. Venus 65, 19–26 (2006)
Google Scholar - Meyer, A., Witek, A. & Lieb, B. Selecting ribosomal protein genes for invertebrate phylogenetic inferences: how many genes to resolve the Mollusca? Method. Ecol. Evol. 2, 34–42 (2011)
Article Google Scholar - Wanninger, A. & Haszprunar, G. Muscle development in Antalis entalis (Mollusca, Scaphopoda) and its significance for scaphopod relationships. J. Morphol. 254, 53–64 (2002)
Article Google Scholar - Lundin, K., Schander, C. & Todt, C. Ultrastructure of epidermal cilia and ciliary rootlets in Scaphopoda. J. Molluscan Stud. 75, 69–73 (2008)
Article Google Scholar - Moroz, L. L. On the independent origins of complex brains and neurons. Brain Behav. Evol. 74, 177–190 (2009)
Article Google Scholar - Simone, L. R. L. Filogenia das superfamílias de Caenogastropoda (Mollusca) com base em morfologia comparativa. PhD thesis, Univ. São Paulo. (2000)
Google Scholar - Jörger, K. M. et al. On the origin of Acochlidia and other enigmatic euthyneuran gastropods, with implications for the systematics of Heterobranchia. BMC Evol. Biol. 10, 323 (2010)
Article Google Scholar - Caron, J. B., Scheltema, A., Schander, C. & Rudkin, D. A soft-bodied mollusc with radula from the Middle Cambrian Burgess Shale. Nature 442, 159–163 (2006)
Article ADS CAS Google Scholar - Scheltema, A. H., Kerth, K. & Kuzirian, A. M. Original molluscan radula: comparisons among Aplacophora, Polyplacophora, Gastropoda, and the Cambrian fossil Wiwaxia corrugata. J. Morphol. 257, 219–245 (2003)
Article Google Scholar - Forment, J. et al. EST2uni: an open, parallel tool for automated EST analysis and database creation, with a data mining web interface and microarray expression data integration. BMC Bioinformatics 9, 5 (2008)
Article Google Scholar - Ebersberger, I., Strauss, S. & Von Haeseler, A. HaMStR: Profile hidden markov model based search for orthologs in ESTs. BMC Evol. Biol. 9, 157 (2009)
Article Google Scholar - Stamatakis, A. RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22, 2688–2690 (2006)
Article CAS Google Scholar - Lartillot, N. & Philippe, H. A Bayesian mixture model for across-site heterogeneities in the amino-acid replacement process. Mol. Biol. Evol. 21, 1095–1109 (2004)
Article CAS Google Scholar - Smith, S. A. & Dunn, C. W. Phyutility: a phyloinformatics tool for trees, alignments and molecular data. Bioinformatics 24, 715–716 (2008)
Article CAS Google Scholar - Shimodaira, H. An approximately unbiased test of phylogenetic tree selection. Syst. Biol. 51, 492–508 (2002)
Article Google Scholar - Chou, H. H. & Holmes, M. H. DNA sequence quality trimming and vector removal. Bioinformatics 17, 1093–1104 (2001)
Article CAS Google Scholar - Huang, X. & Madan, A. CAP3: a DNA sequence assembly program. Genome Res. 9, 868–877 (1999)
Article CAS Google Scholar - Lottaz, C., Iseli, C., Jongeneel, C. V. & Bucher, P. Modeling sequencing errors by combining Hidden Markov models. Bioinformatics 19, (2003)
- O’Brien, K. P., Remm, M. & Sonnhammer, E. L. Inparanoid: a comprehensive database of eukaryotic orthologs. Nucleic Acids Res. 33, D476–D480 (2005)
Article Google Scholar - Katoh, K., Kuma, K., Toh, H. & Miyata, T. MAFFT version 5: improvement in accuracy of multiple sequence alignment. Nucleic Acids Res. 33, 511–518 (2005)
Article CAS Google Scholar - Misof, B. & Misof, K. A Monte Carlo approach successfully identifies randomness in multiple sequence alignments: a more objective means of data exclusion. Syst. Biol. (2009)
- Roure, B., Rodriguez-Ezpeleta, N. & Philippe, H. SCaFoS: a tool for selection, concatenation and fusion of sequences for phylogenomics. BMC Evol. Biol. 7, (2007)
- Okusu, A. & Giribet, G. New 18S rRNA sequences from neomenioid aplacophorans and the possible origin of persistent exogenous contamination. J. Molluscan Stud. 69, 385–387 (2003)
Article Google Scholar - Price, M. N., Dehal, P. S. & Arkin, A. P. FastTree 2 – approximately maximum-likelihood trees for large alignments. PLoS ONE 5, (2010)
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.
Author information
Authors and Affiliations
- Department of Biological Sciences, Auburn University, 101 Rouse Life Sciences, Auburn, 36849, Alabama, USA
Kevin M. Kocot, Johanna T. Cannon, Scott R. Santos & Kenneth M. Halanych - Department of Biology and Centre for Geobiology, University of Bergen, P.O. Box 7800, NO-5020 Bergen, Norway
Christiane Todt & Christoffer Schander - The Whitney Laboratory for Marine Bioscience, University of Florida, 9505 Ocean Shore Blvd., St. Augustine, 32080, Florida, USA
Mathew R. Citarella, Andrea B. Kohn & Leonid L. Moroz - Institute of Zoology, Johannes Gutenberg University, Müllerweg 6, D-55099 Mainz, Germany
Achim Meyer & Bernhard Lieb - Department of Neuroscience, University of Florida, Gainesville, 32611, Florida, USA
Leonid L. Moroz
Authors
- Kevin M. Kocot
You can also search for this author inPubMed Google Scholar - Johanna T. Cannon
You can also search for this author inPubMed Google Scholar - Christiane Todt
You can also search for this author inPubMed Google Scholar - Mathew R. Citarella
You can also search for this author inPubMed Google Scholar - Andrea B. Kohn
You can also search for this author inPubMed Google Scholar - Achim Meyer
You can also search for this author inPubMed Google Scholar - Scott R. Santos
You can also search for this author inPubMed Google Scholar - Christoffer Schander
You can also search for this author inPubMed Google Scholar - Leonid L. Moroz
You can also search for this author inPubMed Google Scholar - Bernhard Lieb
You can also search for this author inPubMed Google Scholar - Kenneth M. Halanych
You can also search for this author inPubMed Google Scholar
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 toKevin M. Kocot or Kenneth M. Halanych.
Ethics declarations
Competing interests
The authors declare no competing financial interests.
Supplementary information
Supplementary Information
This file contains Supplementary Methods, Supplementary Results, Supplementary References, Supplementary Tables 1-7 and Supplementary Figures 1-16 with legends. (PDF 14738 kb)
PowerPoint slides
Rights and permissions
About this article
Cite this article
Kocot, K., Cannon, J., Todt, C. et al. Phylogenomics reveals deep molluscan relationships.Nature 477, 452–456 (2011). https://doi.org/10.1038/nature10382
- Received: 23 February 2011
- Accepted: 22 July 2011
- Published: 04 September 2011
- Issue Date: 22 September 2011
- DOI: https://doi.org/10.1038/nature10382