The ''Naked Coral'' Hypothesis revisited - evidence for and against scleractinian monophyly

PLoS ONE

Volumn 9, Issue 4, 2014, Pages

  Kitahara, Marcelo V ^a,b   Lin, Mei Fang ^c,d   Forê T, Sylvain ^c,e   Huttley, Gavin ^f   Miller, David J ^c   Chen, Chaolun Allen ^d,g,h  

^a FEDERAL UNIVERSITY OF SÃO PAULO   (Brazil)

^b UNIVERSITY OF SÃO PAULO   (Brazil)

^c JAMES COOK UNIVERSITY   (Australia)

^d BIODIVERSITY RESEARCH CENTER   (Taiwan)

^e AUSTRALIAN NATIONAL UNIVERSITY   (Australia)

^f Australian National University   (Australia)

^g NATIONAL TAIWAN UNIVERSITY   (Taiwan)

^h ACADEMIA SINICA   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

MITOCHONDRIAL DNA; TRANSFER RNA; AMINO ACID; CODON; METHIONINE TRANSFER RNA; MITOCHONDRIAL PROTEIN; RIBOSOME RNA; RNA 16S; RNA, RIBOSOMAL, 12S; TRYPTOPHAN TRANSFER RNA; ARGININE; CYCLOOXYGENASE 1; CYCLOOXYGENASE 2; CYCLOOXYGENASE 3; NUCLEOTIDE; TYROSINE;

AMINO ACID COMPOSITION; AMINO ACID SEQUENCE; ARTICLE; CODON USAGE; CONTROLLED STUDY; CORAL; CORALLIMORPHARIA; DNA BASE COMPOSITION; DNA REPAIR; GENE DUPLICATION; GENOME SIZE; MITOCHONDRIAL GENOME; MONOPHYLY; NONHUMAN; NUCLEOTIDE SEQUENCE; PARAPHYLY; PHYLOGENY; SCLERACTINIA; ANIMAL; ANTHOZOA; CHEMISTRY; CLASSIFICATION; CODON; DNA SEQUENCE; GENETICS; SPECIES DIFFERENCE; AMINO ACID SUBSTITUTION; ATP6 GENE; ATP8 GENE; CELL LINEAGE; COB GENE; COX 1 GENE; COX 2 GENE; COX 3 GENE; DNA CONTENT; DNA EXTRACTION; GENE; GENE SEQUENCE; HEXACORALLIAN; NAD1 GENE; NAD2 GENE; NAD3 GENE; NAD4 GENE; NAD4L GENE; NAD5 GENE; NAD6 GENE; NAKED CORAL;

AMINO ACIDS; ANIMALS; ANTHOZOA; BASE COMPOSITION; CODON; DNA, MITOCHONDRIAL; GENOME, MITOCHONDRIAL; MITOCHONDRIAL PROTEINS; PHYLOGENY; RNA, RIBOSOMAL; RNA, RIBOSOMAL, 16S; RNA, TRANSFER, MET; RNA, TRANSFER, TRP; SEQUENCE ANALYSIS, DNA; SPECIES SPECIFICITY;

EID: 84925556597     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0094774.g001     Document Type: Article

References (93)

1. Roberts JM, Wheeler AJ, Freiwald A, Cairns SD (2009) Cold-water corals: the biology and geology of deep-sea coral habitats. Cambridge: Cambridge University Press. xvi+334 p.
2. Dower JF, Perry RI (2001) High abundance of larval rockfish over Cobb Seamount, an isolated seamount in the Northeast Pacific. Fish Oceanogr 10: 268-374.
3. Fischer E, Jones G (2012) Atmospheric dimethysulphide production from corals in the Great Barrier Reef and links to solar radiation, climate and coral bleaching. Biogeochemistry 110: 31-46.
4. Kleypas JA, Danabasoglu G, Laugh JM (2008) Potential role of the ocean thermostat in determining regional differences in coral reef bleaching events. Geophys Res Lett 35: L03613.
5. Reaka-Kudla ML (1997) Biodiversity II: understanding and protecting our biological resources. In: Reaka-Kudla ML, Wilson DE, Wilson EO editors. Washington DC: Joseph Henry Press. pp. 83-108.
6. Reed JK (2002) Deep-water Oculina coral reefs of Florida: biology, impacts, and management. Hydrobiologia 471: 43-55. (Pubitemid 34791758)
7. Rogers AD (1999) The biology of Lophelia pertusa (Linnaeus, 1758) and other deep-water reef-forming corals and impacts from human activities. Hydrobiologia 84: 315-406. (Pubitemid 29407492)
8. Barbeitos M, Romano S, Lasker HR (2010) Repeated loss of coloniality and symbiosis in scleractinian corals. Proc Natl Acad Sci USA 26: 11877-11882.
9. Fukami H, Chen CA, Budd AF, Collins A, Wallace C, et al. (2008) Mitochondrial and nuclear genes suggest that stony corals are monophyletic but most families of stony corals are not (Order Scleractinia, Class Anthozoa, Phylum Cnidaria). PLoS One 3: e3222.
10. Kitahara MV, Cairns SD, Miller DJ (2010a) Monophyletic origin of the Caryophyllia (Scleractinia; Caryophylliidae), with description of six new species. Syst Biodivers 8: 91-118.
11. Kitahara MV, Cairns SD, Stolarski J, Blair D, Miller DJ (2010b) A comprehensive phylogenetic analysis of the Scleractinia (Cnidaria, Anthozoa) based on mitochondrial CO1 sequence data. PloS One 5: e11490.
12. Kitahara MV, Cairns SD, Stolarski J, Miller DJ (2012a) Deltocyathiidae, an early-diverging family of Robust corals (Anthozoa, Scleractinia). Zool Scr 42: 201-212.
13. Kitahara MV, Stolarski J, Cairns SD, Benzoni F, Stake JL, et al. (2012b) The first modern solitary Agariciidae (Anthozoa, Scleractinia) revealed by molecular and microstructural analysis. Invertebr Syst 26: 303-305.
14. Le Goff-Vitry MC, Rogers AD, Baglow D (2004) A deep-sea slant on the molecular phylogeny of the Scleractinia. Mol Phylogenet Evol 30: 167-177. (Pubitemid 38097779)
15. Romano SL, Cairns SD (2000) Molecular phylogenetic hypotheses for the evolution of scleractinian corals. Bull Mar Sci 67: 1043-1068.
16. Romano SL, Palumbi SR (1996) Evolution of scleractinian corals inferred from molecular systematics. Science 271: 640-642.
17. Stolarski J, Kitahara MV, Miller DJ, Cairns SD, Mazur M, et al. (2011) The ancient evolutionary origins of Scleractinia revealed by azooxanthellate corals. BMC Evol Biol 11: 2-15.
18. Fukami H, Budd AF, Paulay G, Sole-Cava A, Chen CA, et al. (2004) Conventional taxonomy obscures deep divergence between Pacific and Atlantic corals. Nature 427: 832-835. (Pubitemid 38297743)
19. Huang D, Licuanan WY, Baird AH, Fukami H (2011) Cleaning up the "Bigmessidae" : molecular phylogeny of scleractinian corals from Faviidae, Merulinidae, Pectiniidae and Trachyphylliidae. BMC Evol Biol 11: 37.
20. Huang D (2012) Threatened reef corals of the world. PLoS ONE 7: e34459.
21. Stanley GD Jr, Fautin DG (2001) The origin of modern corals. Science 291: 1913-1914.
22. Fine M, Tchernov D (2007) Scleractinian coral species survive and recover from decalcification. Science 315: 1811. (Pubitemid 46580132)
23. Rodolfo-Metalpa R, Martin S, Ferrier-Pages C, Gattuso JP (2011) Response of the temperate coral Cladocora caespitosa to mid- and long-term exposure to pCO sub and temperature levels projected for the year 2100 AD. Biogeosciences 7: 289-300.
24. Medina M, Collins AG, Takaoka TL, Kuehl JV, Boore JL (2006) Naked corals: skeleton loss in Scleractinia. Proc Natl Acad Sci USA 103: 96-100.
25. Culligan KM, Meyer-Gauen G, Lyons-Weiler J, Hays JB (2000) Evolutionary origin, diversification and specialization of eukaryotic MutS homolog mismatch repair proteins. Nucl Acids Res 28: 463-471. (Pubitemid 30057985)
26. Stephenson TA (1921) On the classification of Actiniaria. Part II. Consideration of the whole group and its relationships, with special reference to forms not treated in part I. Quart J Micr Sci 65: 493-576.
27. Kayal E, Roure B, Philippe H, Collins AG, Lavrov DV (2013) Cnidarian phylogenetic relationships as revealed by mitogenomics. BMC Evol Biol 13: 5.
28. Stampar SN, Maronna MM, Kitahara MV, Reimer JD, Morandini AC (2014) Fast-evolving mitochondrial DNA in Ceriantharia: a reflection of Hexacorallia paraphyly? PLoS One 9: e86612.
29. Huang D, Meier R, Todd PA, Chou LM (2008) Slow mitochondrial COI sequence evolution at the base of the metazoan tree and its implications for DNA barcoding. J Mol Evol 66: 167-174.
30. Shearer TL, Coffroth MA (2008) DNA BARCODING: Barcoding corals: limited by interspecific divergence, not intraspecific variation. Mol Ecol Resour 8: 247-255. (Pubitemid 351224891)
31. Pont-Kingdon GA, Okada NA, Macfarlane JL, Beagley CT, Wolstenholme DR, et al. (1995) A coral mitochondrial MutS gene. Nature 375: 109-111.
32. Tseng CC, Wallace CC, Chen CA (2005) Mitogenomic analysis of Montipora cactus and Anacropora matthai (Cnidaria; Scleractinia; Acroporidae) indicates an unequal rate of mitochondrial evolution among Acroporidae corals. Coral Reefs 24: 502-508. (Pubitemid 41738384)
33. Cheng S, Higuchi R, Stoneking M (1994) Complete mitochondrial genome amplification. Nature Genet 7: 350-351.
34. Chen CA, Yu JK (2000) Universal primers for amplification of mitochondrial small subunit ribosomal RNA-encoding gene in scleractinian corals. Mar Biotechnol 2: 146-503.
35. Folmer O, Black M, Hoeh W, Lutz R, Vrijenhoek R (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol Mar Biol Biotechnol 3: 294-299.
36. Romano SL, Palumbi SR (1997) Molecular evolution of a portion of the mitochondrial 16S ribosomal gene region in scleractinian corals. J Mol Evol 45: 397-411. (Pubitemid 27425912)
37. Lin MF, Luzon KS, Licuanan WY, Ablan-Lagman CM, Chen AC (2011) Seventy-four universal primers for characterizing the complete mitochondrial genomes of scleractinian corals (Cnidaria; Anthozoa). Zool Stud 50: 513-524.
38. Wyman SK, Jansen RK, Boore JL (2004) Automatic annotation of organellar genomes with DOGMA. Bioinformatics 20: 3252-3255. (Pubitemid 39619219)
39. Stothard P (2000) The sequence manipulation suite: JavaScript programs for analyzing and formatting protein and DNA sequences. Biotechniques 28: 1102-1104.
40. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, et al. (2011) MEGA5: Molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28: 2731-2739.
41. Katoh K, Kuma K, Toh H, Miyata T (2005) MAFFT version 5: Improvement in accuracy of multiple sequence alignment. Nucleic Acids Res 33: 511-518. (Pubitemid 40360980)
42. Guindon S, Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52: 696-704. (Pubitemid 37365050)
43. Huelsenbeck JP, Ronquist F (2001) MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics Applications Note 17: 754-755. (Pubitemid 32851390)
44. Harrison GL, McLenachan PA, Phillips MJ, Slack KE, Cooper A, et al. (2004) Four new avian mitochondrial genomes help get to basic evolutionary questions in the late Cretaceous. Mol Biol Evol 21: 974-983. (Pubitemid 38658205)
45. Phillips MJ, Gibb GC, Crimp EA, Penny D (2010) Tinamous and moa flock together: mitochondrial genome sequence analysis reveals independent losses of flight among ratites. Syst Biol 59: 90-107.
46. Hrdy I, Hirt RP, Dolezal P, Bardonova L, Foster PG, et al. (2004). Trichomonas hydrogenosomes contain the NADH dehydrogenase module of mitochondrial complex I. Nature 432: 618-622. (Pubitemid 39626267)
47. Rodríguez-Ezpeleta N, Brinkmann H, Roure B, Lartillot N, Lang F, et al. (2007) Detecting and overcoming systematic errors in genome-scale phylogenies. Syst Biol 56: 389-399.
48. Boussau B, Gouy M (2006) Efficient Likelihood Computations with Non- Reversible Models of Evolution. Syst Biol 55: 756-68.
49. Knight R, Maxwell P, Birmingham A, Carnes J, Caporaso JG, et al. (2007) PyCogent: a toolkit for making sense from sequence. Genome Biol 8: R171.
50. Goldman N (1993) Statistical tests of models of DNA substitution. J Mol Evol 36: 182-198. (Pubitemid 23056380)
51. Gil M, Zanetti MS, Zoller S, Anisimova M (2013) CodonPhyML: fast maximum likelihood phylogeny estimation under codon substitution models. Mol Biol Evol 30: 1270-1280.
52. Yap VB, Lindsay H, Easteal S, Huttley G (2010) Estimates of the effect of natural selection on protein-coding content. Mol Biol Evol 27: 726-734.
53. Lartillot N, Lepage T, Blanquart S (2009) PhyloBayes 3: a Bayesian software package for phylogenetic reconstruction and molecular dating. Bioinformatics 25: 2286-2288.
54. Shimodaira H, Hasegawa M (2001) CONSEL: for assessing the confidence of phylogenetic tree selection. Bioinformatics 17: 1246-1247. (Pubitemid 33735360)
55. Rosenberg MS, Kumar S (2003) Heterogeneity of nucleotide frequencies among evolutionary lineages and phylogenetic inference. Mol Biol Evol 20: 610-621. (Pubitemid 36437911)
56. Phillips MJ, Penny D (2003) The root of the mammalian tree inferred from whole mitochondrial genomes. Mol Phylogenet Evol 28: 171-185. (Pubitemid 37446823)
57. Riemann-Zürneck K, Iken K (2003) Corallimorphus profundus in shallow Antarctic habitats: bionomics, histology, and systematics (Cnidaria: Hexacorallia). Zool Verh Leiden 345: 367-386.
58. Stolarski J (1995) Ontogenetic development of the thecal structures in Caryophylliinae scleractinian corals. Acta Palaeontol Pol 40: 19-44.
59. Chen C, Dai CF, Plathong S, Chiou CY, Chen CA (2008a) The complete mitochondrial genomes of needle corals, Seriatopora spp. (Scleractinia: Pocilloporidae): an idiosyncratic atp8, duplicated trnW gene, and hypervariable regions used to determine species phylogenies and recently diverged populations. Mol Phylogenet Evol 46: 19-33. (Pubitemid 350278673)
60. Park E, Song J, Won Y (2011) The complete mitochondrial genome of Calicogorgia granulosa (Anthozoa:Octocorallia): potential gene novelty in unidentified ORFs formed by repeat expansion and segmental duplication. Gene 486: 81-87.
61. Chen C, Chiou CY, Dai CF, Chen CA (2008b) Unique mitogenomic features in the scleractinian family Pocilloporidae (Scleractinia: Astrocoeniina). Mar Biotechnol 10: 538-553.
62. Fukami H, Knowlton N (2005) Analysis of complete mitochondrial DNA sequences of three members of the Montastraea annularis species complex (Cnidaria, Anthozoa, Scleractinia). Coral Reefs 24: 410-417. (Pubitemid 41738367)
63. Park E, Hwang DS, Lee JS, Song JI, Seo TK, et al. (2012) Estimation of divergence times in cnidarian evolution based on mitochondrial protein-coding genes and the fossil record. Mol Phylogenet Evol 62: 329-345.
64. van Oppen MJ, Catmull J, McDonald BJ, Hislop NR, Hagerman PJ, et al. (2000) The mitochondrial genome of Acropora tenuis (Cnidaria; Scleractinia) contains a large group I intron and a candidate control region. J Mol Evol 55: 1-13. (Pubitemid 34634355)
65. Lin MF, Kitahara MV, Tachikawa H, Fukami H, Miller DJ, et al. (2012) Novel organization of the mitochondrial genome in the deep-sea coral, Madrepora oculata (Hexacorallia, Scleractinia, Oculinidae) and its taxonomic implications. Mol Phylogenet Evol 65: 323-328.
66. Tamura K, Nei M (1993) Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol Biol Evol 10: 512-526. (Pubitemid 23157236)
67. Hasegawa M, Kishino H, Yano T (1985) Dating of the human-ape splitting by a molecular clock of mitochondrial DNA. J Mol Evol 22: 160-174. (Pubitemid 16227864)
68. Jones DT, Taylor WR, Thornton JM (1992) The rapid generation of mutation data matrices from protein sequences. Comput Appl Biosci 8: 275-282.
69. Whelan S, Goldman N (2001) A general empirical model of protein evolution derived from multiple protein families using a maximum-likelihood approach. Mol Biol Evol 18: 691-699. (Pubitemid 32372940)
70. Dayhoff M, Schwartz R, Orcutt B (1978) A model of evolutionary change in protein. In: Dayhoff MO editor. Atlas of protein sequences and structure. Washington, DC: National Biomedical Research Foundation. pp. 345-351.
71. van Den Bussche RA, Baker RJ, Huelsenbeck JP, Hillis DM (1998) Base compositional bias and phylogenetic analyses: a test of the "flying DNA" hypothesis. Mol Phylogenet Evol 13: 408-416. (Pubitemid 128349347)
72. Galtier N, Gouy M (1998) Inferring pattern and process: Maximum-likelihood implementation of a nonhomogeneous model of DNA sequence evolution for phylogenetic analysis. Mol Biol Evol 15: 871-879. (Pubitemid 28321885)
73. Peden J (2005) CodonW version 1. 4. 2. Available: http://codonw. sourceforge. net/ culong. html#License
74. Lartillot N. Philippe H (2004) A Bayesian mixture model for across-site heterogeneities in the amino-acid replacement process. Mol Biol Evol 21: 1095-1109. (Pubitemid 38658218)
75. Lartillot N, Brinkmann H, Philippe H (2007) Suppression of long-branch attraction artefacts in the animal phylogeny using a site-heterogeneous model. BMC Evol Biol (Suppl 1): S4.
76. Shearer TL, van Oppen MJH, Romano SL, Worheide G (2002) Slow mitochondrial DNA sequence evolution in the Anthozoa (Cnidaria). Mol Ecol 11: 2475-2487. (Pubitemid 35436670)
77. Aranda M, DeSalvo MK, Bayer T, Medina M, Voolstra C (2012) Evolutionary insights into scleractinian corals using comparative genomic hybridizations. BMC Genomics 13: 501.
78. Beagley CT, Okimoto R, Wolstenholme DR (1998) The mitochondrial genome of the sea anemone Metridium senile (Cnidaria): introns, a paucity of tRNA genes, a near-standard genetic code. Genetics 148: 1091-1108. (Pubitemid 28169021)
79. Shinzato C, Shoguchi E, Kawashima T, Hamada M, Hisata K, et al. (2011) Using the Acropora digitifera genome to understand coral responses to environmental change. Nature 476: 320-323.
80. van Oppen MJH, Hislop NR, Hagerman PJ, Miller DJ (1999) Gene content and organization in a segment of the mitochondrial genome of the scleractinian coral Acropora tenuis: major differences in gene order within the anthozoan subclass Zoantharia. Mol Biol Evol 16: 1812-1215.
81. Knight RD, Freeland SJ, Landweber LF (2001) A simple model based on mutation and selection explains trends in codon and amino-acid usage and GC composition within and across genomes. Genome Biol 2: 4.
82. Barry D, Hartigan JA (1987) Statistical analysis of Hominoid molecular evolution. Stat Sci 2: 191-207.
83. Kosiol C (2006) Markov models for protein sequence evolution. [Ph. D. thesis]. EMBL-European Bioinformatics Institute. Cambridge: University of Cambridge.
84. Huttley G (2009) Do genomic datasets resolve the correct relationship among the placental, marsupial and monotreme lineages? Austral J Zool 57: 167-174.
85. Sheffield NC, Song H, Cameron SL, Whiting MF (2009) Nonstationary evolution and compositional heterogeneity in beetle mitochondrial phylogenomics. Syst Biol 58: 381-394.
86. Beaton MJ, Roger AJ, Cavalier-Smith T (1998) Sequence analysis of the mitochondrial genome of Sarcophyton glaucum: conserved gene order among octocorals. J Mol Evol 47: 697-708. (Pubitemid 29008773)
87. Brugler MR, France SC (2007) The complete mitochondrial genome of the black coral Chrysopathes formosa (Cnidaria: Anthozoa: Antipatharia) supports classification of antipatharians within the subclass Hexacorallia. Mol Phylogenet Evol 42: 776-788. (Pubitemid 46330804)
88. Flot JF, Tillier S (2007) The mitochondrial genome of Pocillopora (Cnidaria: Scleractinia) contains two variable regions: the putative D-loop and a novel ORF of unknown function. Gene 401: 80-87. (Pubitemid 47379516)
89. Sinniger F, ChevaldonnéP, Pawlowski J (2007) Mitochondrial genome of Savalia savaglia (Cnidaria, Hexacorallia) and early metazoan phylogeny. J Mol Evol 64: 196-203. (Pubitemid 46147043)
90. Emblem A, Karlsen BO, Evertsen J, Johansen SD (2011) Mitogenome rearrangement in the cold-water scleractinian coral Lophelia pertusa (Cnidaria, Anthozoa) involves a long-term evolving group I intron. Mol Phylogenet Evol 61: 495-503.
91. Adachi J, Waddell PJ, Martin W, Hasegawa M (2000) Plastid genome phylogeny and a model of amino acid substitution for protein encoded by chloroplast DNA. J Mol Evol 50: 348-358. (Pubitemid 30429968)
92. Daly M, Fautin DG, Cappola VA (2003) Systematics of the Hexacorallia (Cnidaria: Anthozoa). Zool J Linn Soc-Lond 139: 419-437. (Pubitemid 37457858)
93. TavaréS. 1986 Some probabilistic and statistical problems in the analysis of DNA sequences. Lectures Math Life Sci 17: 57-86.