A phylogenetic backbone for Bivalvia: an RNA-seq approach

Bivalves are an ancient and ubiquitous group of aquatic invertebrates with an estimated 10 000–20 000 living species. They are economically significant as a human food source, and ecologically important given their biomass and effects on communities. Their phylogenetic relationships have been studied for decades, and their unparalleled fossil record extends from the Cambrian to the Recent. Nevertheless, a robustly supported phylogeny of the deepest nodes, needed to fully exploit the bivalves as a model for testing macroevolutionary theories, is lacking. Here, we present the first phylogenomic approach for this important group of molluscs, including novel transcriptomic data for 31 bivalves obtained through an RNA-seq approach, and analyse these data with published genomes and transcriptomes of other bivalves plus outgroups. Our results provide a well-resolved, robust phylogenetic backbone for Bivalvia with all major lineages delineated, addressing long-standing questions about the monophyly of Protobranchia and Heterodonta, and resolving the position of particular groups such as Palaeoheterodonta, Archiheterodonta and Anomalodesmata. This now fully resolved backbone demonstrates that genomic approaches using hundreds of genes are feasible for resolving phylogenetic questions in bivalves and other animals.

[1]  R. Cutler,et al.  An Analytical Study , 2016 .

[2]  Vanessa L. González,et al.  A multilocus phylogeny of archiheterodont bivalves (Mollusca, Bivalvia, Archiheterodonta) , 2015 .

[3]  G. Giribet,et al.  Phylogenomic Analysis of Spiders Reveals Nonmonophyly of Orb Weavers , 2014, Current Biology.

[4]  Mark Howison,et al.  Phylogenomic analyses of deep gastropod relationships reject Orthogastropoda , 2014, bioRxiv.

[5]  P. Sharp,et al.  Investigating the Bivalve Tree of Life – an exemplar-based approach combining molecular and novel morphological characters , 2014, Invertebrate Systematics.

[6]  Antonio G. Checa,et al.  Early Stage Biomineralization in the Periostracum of the ‘Living Fossil’ Bivalve Neotrigonia , 2014, PloS one.

[7]  Alexandros Stamatakis,et al.  Decisive Data Sets in Phylogenomics: Lessons from Studies on the Phylogenetic Relationships of Primarily Wingless Insects , 2013, Molecular biology and evolution.

[8]  K. Kocot,et al.  Phylogenomics supports Panpulmonata: opisthobranch paraphyly and key evolutionary steps in a major radiation of gastropod molluscs. , 2013, Molecular phylogenetics and evolution.

[9]  Felipe Zapata,et al.  Agalma: an automated phylogenomics workflow , 2013, BMC Bioinformatics.

[10]  I. Stöger,et al.  Mitogenomics does not resolve deep molluscan relationships (yet?). , 2013, Molecular phylogenetics and evolution.

[11]  Elizabeth E. Boyle,et al.  Into the deep: a phylogenetic approach to the bivalve subclass Protobranchia. , 2013, Molecular phylogenetics and evolution.

[12]  Colin N. Dewey,et al.  De novo transcript sequence reconstruction from RNA-seq using the Trinity platform for reference generation and analysis , 2013, Nature Protocols.

[13]  Daniel Stubbs,et al.  PhyloBayes MPI: phylogenetic reconstruction with infinite mixtures of profiles in a parallel environment. , 2013, Systematic biology.

[14]  Gaston H. Gonnet,et al.  Inferring Hierarchical Orthologous Groups from Orthologous Gene Pairs , 2013, PloS one.

[15]  C. A. Soares,et al.  Boronated tartrolon antibiotic produced by symbiotic cellulose-degrading bacteria in shipworm gills , 2013, Proceedings of the National Academy of Sciences of the United States of America.

[16]  Nicholas H. Putnam,et al.  Insights into bilaterian evolution from three spiralian genomes , 2012, Nature.

[17]  Stefan Grünewald,et al.  SuperQ: Computing Supernetworks from Quartets , 2013, IEEE/ACM Transactions on Computational Biology and Bioinformatics.

[18]  Federico Plazzi,et al.  The complete mitochondrial genome of Solemya velum (Mollusca: Bivalvia) and its relationships with Conchifera , 2013, BMC Genomics.

[19]  Zhengwei Zhu,et al.  CD-HIT: accelerated for clustering the next-generation sequencing data , 2012, Bioinform..

[20]  P. Sharma,et al.  Phylogenetic analysis of four nuclear protein-encoding genes largely corroborates the traditional classification of Bivalvia (Mollusca). , 2012, Molecular phylogenetics and evolution.

[21]  Hideo Aoki,et al.  Draft Genome of the Pearl Oyster Pinctada fucata: A Platform for Understanding Bivalve Biology , 2012, DNA research : an international journal for rapid publication of reports on genes and genomes.

[22]  M. Taviani,et al.  A Molecular Phylogeny of Bivalve Mollusks: Ancient Radiations and Divergences as Revealed by Mitochondrial Genes , 2011, PloS one.

[23]  Stephen A. Smith,et al.  Resolving the evolutionary relationships of molluscs with phylogenomic tools , 2011, Nature.

[24]  L. Moroz,et al.  Phylogenomics reveals deep molluscan relationships , 2011, Nature.

[25]  N. Friedman,et al.  Trinity: reconstructing a full-length transcriptome without a genome from RNA-Seq data , 2011, Nature Biotechnology.

[26]  Federico Plazzi,et al.  Towards a molecular phylogeny of Mollusks: bivalves' early evolution as revealed by mitochondrial genes. , 2010, Molecular phylogenetics and evolution.

[27]  D. Kay,et al.  Safe Management of Shellfish and Harvest Waters , 2010 .

[28]  M. Martindale,et al.  Assessing the root of bilaterian animals with scalable phylogenomic methods , 2009, Proceedings of the Royal Society B: Biological Sciences.

[29]  D. Stallknecht,et al.  Filter-feeding bivalves can remove avian influenza viruses from water and reduce infectivity , 2009, Proceedings of the Royal Society B: Biological Sciences.

[30]  E. Glover,et al.  Phylogenetic position of the bivalve family Cyrenoididae-removal from (and further dismantling of) the superfamily Lucinoidea , 2009 .

[31]  Gaston H. Gonnet,et al.  Algorithm of OMA for large-scale orthology inference , 2008, BMC Bioinformatics.

[32]  J. Rougemont,et al.  A rapid bootstrap algorithm for the RAxML Web servers. , 2008, Systematic biology.

[33]  O. Gascuel,et al.  An improved general amino acid replacement matrix. , 2008, Molecular biology and evolution.

[34]  Kazutaka Katoh,et al.  Recent developments in the MAFFT multiple sequence alignment program , 2008, Briefings Bioinform..

[35]  J. W. Valentine,et al.  Species–genus ratios reflect a global history of diversification and range expansion in marine bivalves , 2008, Proceedings of the Royal Society B: Biological Sciences.

[36]  David Q. Matus,et al.  Broad phylogenomic sampling improves resolution of the animal tree of life , 2008, Nature.

[37]  E. Glover,et al.  A molecular phylogeny of heterodont bivalves (Mollusca: Bivalvia: Heterodonta): new analyses of 18S and 28S rRNA genes , 2007 .

[38]  Alexandros Stamatakis,et al.  RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models , 2006, Bioinform..

[39]  J. W. Valentine,et al.  Assessing the fidelity of the fossil record by using marine bivalves. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[40]  D. Huson,et al.  Application of phylogenetic networks in evolutionary studies. , 2006, Molecular biology and evolution.

[41]  Gerhard Steiner,et al.  What can 18S rDNA do for bivalve phylogeny? , 1996, Journal of Molecular Evolution.

[42]  W. Wheeler,et al.  On bivalve phylogeny: a high‐level analysis of the Bivalvia (Mollusca) based on combined morphology and DNA sequence data , 2005 .

[43]  H. Philippe,et al.  Multigene analyses of bilaterian animals corroborate the monophyly of Ecdysozoa, Lophotrochozoa, and Protostomia. , 2005, Molecular biology and evolution.

[44]  N. Malchus Constraints in the ligament ontogeny and evolution of pteriomorphian Bivalvia , 2004 .

[45]  H. Philippe,et al.  A Bayesian mixture model for across-site heterogeneities in the amino-acid replacement process. , 2004, Molecular biology and evolution.

[46]  E. Glover,et al.  MOLECULAR PHYLOGENY OF THE LUCINOIDEA (BIVALVIA): NON‐MONOPHYLY AND SEPARATE ACQUISITION OF BACTERIAL CHEMOSYMBIOSIS , 2004 .

[47]  S. Carroll,et al.  Genome-scale approaches to resolving incongruence in molecular phylogenies , 2003, Nature.

[48]  M. Matsumoto Phylogenetic analysis of the subclass Pteriomorphia (Bivalvia) from mtDNA COI sequences. , 2003, Molecular phylogenetics and evolution.

[49]  S. Whelan,et al.  A general empirical model of protein evolution derived from multiple protein families using a maximum-likelihood approach. , 2001, Molecular biology and evolution.

[50]  Wei Qian,et al.  Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. , 2000, Molecular biology and evolution.

[51]  J. W. Valentine,et al.  Dissecting latitudinal diversity gradients: functional groups and clades of marine bivalves , 2000, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[52]  J. Cope A new look at early bivalve phylogeny , 2000, Geological Society, London, Special Publications.

[53]  B. Morton,et al.  Relationships between the extant Anomalodesmata: a cladistic test , 2000, Geological Society, London, Special Publications.

[54]  D. Campbell Molecular evidence on the evolution of the Bivalvia , 2000, Geological Society, London, Special Publications.

[55]  J. G. Carter,et al.  Cladistic perspectives on early bivalve evolution , 2000, Geological Society, London, Special Publications.

[56]  G. Steiner,et al.  Molecular phylogeny of the Bivalvia inferred from 18S rDNA sequences with particular reference to the Pteriomorphia , 2000, Geological Society, London, Special Publications.

[57]  J. Cope The early phylogeny of the class Bivalvia , 1997 .

[58]  L. Salvini-Plawen Synapomorphies and synplesiomorphies in higher classification of Mollusca , 1996 .

[59]  John Taylor,et al.  Origin and evolutionary radiation of the Mollusca , 1996 .

[60]  P. Tyler,et al.  Deep-Sea Biology: A Natural History of Organisms at the Deep-Sea Floor , 1991 .

[61]  B. Morton The bivalvia : proceedings of a memorial symposium in honour of Sir Charles Maurice Yonge (1899-1986) at the IXth International Malacological Congress, 1986, Edinburgh, Scotland, U.K. , 1990 .

[62]  R. Purchon Classification and Evolution of the Bivalvia: An Analytical Study , 1987 .

[63]  D. Walton,et al.  Fauna of Australia , 1987 .

[64]  T. Waller The Evolution of Ligament Systems in the Bivalvia , 1986 .

[65]  R. Purchon,et al.  An Analytical Approach to a Classification of the Bivalvia , 1978 .

[66]  R. D. Turner,et al.  Classification of Bivalvia , 1969 .

[67]  C. R. Stasek Synopsis and discussion of the association of ctenidia and labial palps in the bivalved Mollusca , 1963 .

[68]  R. Purchon 4. PHYLOGENETIC CLASSIFICATION OF THE LAMELLIBRANCHIA, WITH SPECIAL REFERENCE TO THE PROTOBRANCHIA , 1959 .