Fast-Evolving Mitochondrial DNA in Ceriantharia: A Reflection of Hexacorallia Paraphyly?

The low evolutionary rate of mitochondrial genes in Anthozoa has challenged their utility for phylogenetic and systematic purposes, especially for DNA barcoding. However, the evolutionary rate of Ceriantharia, one of the most enigmatic “orders” within Anthozoa, has never been specifically examined. In this study, the divergence of mitochondrial DNA of Ceriantharia was compared to members of other Anthozoa and Medusozoa groups. In addition, nuclear markers were used to check the relative phylogenetic position of Ceriantharia in relation to other Cnidaria members. The results demonstrated a pattern of divergence of mitochondrial DNA completely different from those estimated for other anthozoans, and phylogenetic analyses indicate that Ceriantharia is not included within hexacorallians in most performed analyses. Thus, we propose that the Ceriantharia should be addressed as a separate clade.

[1]  M. Siddall,et al.  Higher level relationships of leeches (Annelida: Clitellata: Euhirudinea) based on morphology and gene sequences. , 1999, Molecular phylogenetics and evolution.

[2]  A. Vandamme.  The Phylogenetic Handbook: Basic concepts of molecular evolution , 2009 .

[3]  R. Lanfear,et al.  Partitionfinder: combined selection of partitioning schemes and substitution models for phylogenetic analyses. , 2012, Molecular biology and evolution.

[4]  B. Rho,et al.  A phylogenetic study of the Anthozoa (phylum Cnidaria) based on morphological and molecular characters , 2001, Coral Reefs.

[5]  P. Stadler,et al.  Accurate and efficient reconstruction of deep phylogenies from structured RNAs , 2009, Nucleic acids research.

[6]  Kazutaka Katoh,et al.  Multiple alignment of DNA sequences with MAFFT. , 2009, Methods in molecular biology.

[7]  A. Collins,et al.  Evaluating hypotheses of basal animal phylogeny using complete sequences of large and small subunit rRNA , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[8]  Simon P. Wilson,et al.  The Magnitude of Global Marine Species Diversity , 2012, Current Biology.

[9]  T. Cavalier-smith,et al.  Mitochondrial DNA of the coral sarcophyton glaucum contains a gene for a homologue of bacterial muts: A possible case of gene transfer from the nucleus to the mitochondrion , 1998, Journal of Molecular Evolution.

[10]  L. Moroz,et al.  Rapid evolution of the compact and unusual mitochondrial genome in the ctenophore, Pleurobrachia bachei. , 2012, Molecular Phylogenetics and Evolution.

[11]  Pablo A. Goloboff,et al.  TNT, a free program for phylogenetic analysis , 2008 .

[12]  A. Wilson,et al.  Mitochondrial DNA evolution in mice. , 1983, Genetics.

[13]  M. Stoneking,et al.  Mitochondrial DNA and two perspectives on evolutionary genetics , 1985 .

[14]  J. Claverie,et al.  Two new subfamilies of DNA mismatch repair proteins (MutS) specifically abundant in the marine environment , 2011, The ISME Journal.

[15]  Maxim Teslenko,et al.  MrBayes 3.2: Efficient Bayesian Phylogenetic Inference and Model Choice Across a Large Model Space , 2012, Systematic biology.

[16]  James Lyons-Weiler,et al.  Evolutionary origin, diversification and specialization of eukaryotic MutS homolog mismatch repair proteins. , 2000, Nucleic acids research.

[17]  R. DeSalle,et al.  Class-level relationships in the phylum Cnidaria: molecular and morphological evidence. , 1995, Molecular biology and evolution.

[18]  O. Gascuel,et al.  Survey of Branch Support Methods Demonstrates Accuracy, Power, and Robustness of Fast Likelihood-based Approximation Schemes , 2011, Systematic biology.

[19]  W. Wheeler,et al.  Systematics of the Damon variegatus group of African whip spiders (Chelicerata: Amblypygi): Evidence from behaviour, morphology and DNA , 2005 .

[20]  W. Wheeler,et al.  POY version 4: phylogenetic analysis using dynamic homologies , 2010, Cladistics : the international journal of the Willi Hennig Society.

[21]  Derrick J. Zwickl.  Genetic algorithm approaches for the phylogenetic analysis of large biological sequence datasets under the maximum likelihood criterion , 2006 .

[22]  P. Stadler,et al.  Mitogenomics and metazoan evolution. , 2013, Molecular phylogenetics and evolution.

[23]  The Phylogenetic Handbook: Testing tree topologies , 2009 .

[24]  A. Wilson,et al.  DNA sequences from the quagga, an extinct member of the horse family , 1984, Nature.

[25]  M. Oppen,et al.  Slow mitochondrial DNA sequence evolution in the Anthozoa (Cnidaria) , 2002, Molecular ecology.

[26]  Marymegan Daly,et al.  Systematics of the Hexacorallia (Cnidaria: Anthozoa) , 2003 .

[27]  R. Meier,et al.  Slow Mitochondrial COI Sequence Evolution at the Base of the Metazoan Tree and Its Implications for DNA Barcoding , 2008, Journal of Molecular Evolution.

[28]  A. Morandini,et al.  Evolutionary Diversification of Banded Tube-Dwelling Anemones (Cnidaria; Ceriantharia; Isarachnanthus) in the Atlantic Ocean , 2012, PloS one.

[29]  T. Molodtsova.  On the taxonomy and presumable evolutionary pathways of planktonic larvae of Ceriantharia (Anthozoa, Cnidaria) , 2004, Hydrobiologia.

[30]  D. Miller,et al.  Systematic relationships within the Anthozoa (Cnidaria: Anthozoa) using the 5'-end of the 28S rDNA. , 1995, Molecular phylogenetics and evolution.

[31]  W. Brown,et al.  Rapid evolution of animal mitochondrial DNA. , 1979, Proceedings of the National Academy of Sciences of the United States of America.

[32]  A. Collins,et al.  Cnidarian phylogenetic relationships as revealed by mitogenomics , 2013, BMC Evolutionary Biology.

[33]  John D. Kececioglu,et al.  Multiple alignment by aligning alignments , 2007, ISMB/ECCB.

[34]  M. S. Lee,et al.  Partitioned likelihood support and the evaluation of data set conflict. , 2003, Systematic biology.

[35]  S. France,et al.  A molecular phylogenetic analysis of the Octocorallia (Cnidaria: Anthozoa) based on mitochondrial protein-coding sequences. , 2006, Molecular phylogenetics and evolution.

[36]  P. Stadler,et al.  Genetic aspects of mitochondrial genome evolution. , 2013, Molecular phylogenetics and evolution.

[37]  Patrick Kück,et al.  Parametric and non-parametric masking of randomness in sequence alignments can be improved and leads to better resolved trees , 2010, Frontiers in Zoology.

[38]  R. Glor.  Phylogenetic Insights on Adaptive Radiation , 2010 .

[39]  Benjamin D. Redelings,et al.  BAli-Phy: simultaneous Bayesian inference of alignment and phylogeny , 2006, Bioinform..

[40]  Tal Pupko,et al.  State-of the art methodologies dictate new standards for phylogenetic analysis , 2012, BMC Evolutionary Biology.

[41]  J. Townsend,et al.  PhyDesign: an online application for profiling phylogenetic informativeness , 2011, BMC Evolutionary Biology.

[42]  R. Cruickshank.  Molecular markers for the phylogenetics of mites and ticks , 2002 .

[43]  A. Collins,et al.  Evolution of Linear Mitochondrial Genomes in Medusozoan Cnidarians , 2011, Genome biology and evolution.

[44]  Matthias Bernt,et al.  A comprehensive analysis of bilaterian mitochondrial genomes and phylogeny. , 2013, Molecular phylogenetics and evolution.

[45]  T. Cavalier-smith,et al.  A coral mitochondrial mutS gene , 1995, Nature.

[46]  Robert C. Edgar,et al.  Multiple sequence alignment. , 2006, Current opinion in structural biology.

[47]  M. Dawson.  Renaissance taxonomy: integrative evolutionary analyses in the classification of Scyphozoa , 2005, Journal of the Marine Biological Association of the United Kingdom.

[48]  A. Couloux,et al.  Molecular phylogenetics of Thecata (Hydrozoa, Cnidaria) reveals long-term maintenance of life history traits despite high frequency of recent character changes. , 2009, Systematic biology.

[49]  R. Vrijenhoek,et al.  DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. , 1994, Molecular marine biology and biotechnology.

[50]  C. McFadden,et al.  The Mitochondrial Genome of Paraminabea aldersladei (Cnidaria: Anthozoa: Octocorallia) Supports Intramolecular Recombination as the Primary Mechanism of Gene Rearrangement in Octocoral Mitochondrial Genomes , 2012, Genome biology and evolution.

[51]  M. Youngbluth,et al.  DNA Barcoding the Medusozoa using mtCOI , 2010 .

[52]  Anne-Mieke Vandamme,et al.  The Phylogenetic Handbook: A Practical Approach to Phylogenetic Analysis and Hypothesis Testing , 2009 .

[53]  O. Gascuel,et al.  New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. , 2010, Systematic biology.

[54]  Y. Won,et al.  Estimation of divergence times in cnidarian evolution based on mitochondrial protein-coding genes and the fossil record. , 2012, Molecular phylogenetics and evolution.

[55]  P. Keeling,et al.  Gene Conversion Shapes Linear Mitochondrial Genome Architecture , 2013, Genome biology and evolution.

[56]  M. Nei,et al.  MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. , 2011, Molecular biology and evolution.

[57]  T. Kocher,et al.  DNA sequence variation of mitochondrial large-subunit rRNA provides support for a two-subclass organization of the Anthozoa (Cnidaria). , 1996, Molecular marine biology and biotechnology.

[58]  Des Higgins,et al.  The Phylogenetic Handbook: Multiple sequence alignment , 2009 .

[59]  B. Schierwater,et al.  Mitogenomics at the base of Metazoa. , 2013, Molecular phylogenetics and evolution.

[60]  B. Schierwater,et al.  Speciation and phylogeography in the cosmopolitan marine moon jelly, Aurelia sp , 2002, BMC Evolutionary Biology.

[61]  S. Degnan,et al.  A unique horizontal gene transfer event has provided the octocoral mitochondrial genome with an active mismatch repair gene that has potential for an unusual self-contained function , 2011, BMC Evolutionary Biology.

[62]  Andrea Ender,et al.  Placozoa – no longer a phylum of one , 2004, Current Biology.

[63]  J. Mullikin,et al.  Extreme mitochondrial evolution in the ctenophore Mnemiopsis leidyi: Insight from mtDNA and the nuclear genome , 2011, Mitochondrial DNA.

[64]  M. Coffroth,et al.  DNA BARCODING: Barcoding corals: limited by interspecific divergence, not intraspecific variation , 2008, Molecular ecology resources.

[65]  B. Schierwater,et al.  Medusozoan phylogeny and character evolution clarified by new large and small subunit rDNA data and an assessment of the utility of phylogenetic mixture models. , 2006, Systematic biology.

[66]  P. L. Chang,et al.  Structure, Transcription, and Variability of Metazoan Mitochondrial Genome: Perspectives from an Unusual Mitochondrial Inheritance System , 2013, Genome biology and evolution.

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

[68]  P. Hebert,et al.  Barcoding animal life: cytochrome c oxidase subunit 1 divergences among closely related species , 2003, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[69]  Serita M. Nelesen,et al.  SATe-II: very fast and accurate simultaneous estimation of multiple sequence alignments and phylogenetic trees. , 2012, Systematic biology.

[70]  L. Buss,et al.  Molecular evidence for multiple episodes of paedomorphosis in the family Hydractiniidae , 1993 .

[71]  O. Gascuel,et al.  Approximate likelihood-ratio test for branches: A fast, accurate, and powerful alternative. , 2006, Systematic biology.

[72]  B. Schierwater,et al.  Mitochondrial genome of Trichoplax adhaerens supports placozoa as the basal lower metazoan phylum. , 2006, Proceedings of the National Academy of Sciences of the United States of America.