Species boundaries and phylogenetic relationships between Atlanto-Mediterranean shallow-water and deep-sea coral associated Hexadella species (Porifera, Ianthellidae)

Molecular Phylogenetics and Evolution

Volumn 56, Issue 1, 2010, Pages 104-114

  Reveillaud, Julie ^a   Remerie, Thomas ^a   van Soest, Rob ^b   Erpenbeck, Dirk ^c   Cárdenas, Paco ^d   Derycke, Sofie ^a   Xavier, Joana R ^e,f   Rigaux, Annelien ^a   Vanreusel, Ann ^a  

^a GHENT UNIVERSITY   (Belgium)

^b UNIVERSITY OF AMSTERDAM   (Netherlands)

^c UNIVERSITY OF MUNICH   (Germany)

^d UNIVERSITY OF BERGEN   (Norway)

^e CENTRO DE INVESTIGAÇÃO EM BIODIVERSIDADE E RECURSOS GENÉTICOS   (Portugal)

^f CENTRE D ESTUDIS AVANÇATS DE BLANES CEAB CSIC   (Spain)

Author keywords

Atlanto Mediterranean; COI; Cold water coral; Nuclear intron; Partial 28S rDNA; Phylogenetic resolution; Porifera

Indexed keywords

MITOCHONDRIAL DNA;

ANIMAL; ANTHOZOA; ARTICLE; ATLANTIC OCEAN; BAYES THEOREM; CELL NUCLEUS; CLASSIFICATION; DNA SEQUENCE; ECOSYSTEM; GENETIC VARIABILITY; GENETICS; MEDITERRANEAN SEA; METABOLISM; MOLECULAR EVOLUTION; PHYLOGENY; SEQUENCE ALIGNMENT; SPONGE (PORIFERA);

ANIMALS; ANTHOZOA; ATLANTIC OCEAN; BAYES THEOREM; CELL NUCLEUS; DNA, MITOCHONDRIAL; ECOSYSTEM; EVOLUTION, MOLECULAR; GENETIC VARIATION; MEDITERRANEAN SEA; PHYLOGENY; PORIFERA; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS, DNA;

ANTHOZOA; DEMOSPONGIAE; HEXADELLA; HEXADELLA PRUVOTI; IANTHELLIDAE; PORIFERA; VERONGIDA;

EID: 77953561432     PISSN: 10557903     EISSN: 10959513     Source Type: Journal    
DOI: 10.1016/j.ympev.2010.03.034     Document Type: Article

References (73)

1. Altschul S.F., Gish W., Miller W., Myers E.W., and Lipman D.J. Basic local alignment search tool. J. Mol. Biol. 215 (1990) 403-410
2. Ballard J.W.O., and Whitlock M.C. The incomplete natural history of mitochondria. Mol. Ecol. 13 (2004) 729-744
3. Bell J.J., Barnes D.K.A., and Turner J.R. The importance of micro and macro morphological variation in the adaptation of a sublittoral demosponge to current extremes. Mar. Biol. 140 (2002) 75-81
4. Bell J.J. The functional roles of marine sponges. Estuarine Coastal Shelf Sci. 79 (2008) 341-353
5. Bentlage B., and Wörheide G. Low genetic structuring among Pericharax heteroraphis (Porifera: Calcarea) populations from the Great Barrier Reef (Australia), revealed by analysis of nrDNA and nuclear intron sequences. Coral Reefs 26 (2007) 807-816
6. Bergquist P.R., and Cook S.D.C. Order Verongida Bergquist, 1978. In: Hooper J.N.A., and Van Soest R.W.M. (Eds). Systema Porifera, A Guide to the Classification of Sponges (2002), Kluwer Academic/Plenum Publishers, New York 1081-1096
7. Blanquer A., and Uriz M.J. Cryptic speciation in marine sponges evidenced by mitochondrial and nuclear genes: a phylogenetic approach. Mol. Phylogenet. Evol. 45 (2007) 392-397
8. Blanquer A., and Uriz M.J. 'A posteriori' searching for phenotypic characters to describe new cryptic species of sponges revealed by molecular markers (Dictyonellidae: Scopalina). Invertebr. Syst. 22 (2008) 489-502
9. Blanquer A., Uriz M.J., and Caujape-Castells J. Small-scale spatial genetic structure in Scopalina lophyropoda, an encrusting sponge with philopatric larval dispersal and frequent fission and fusion events. Mar. Ecol. Prog. Ser. 380 (2009) 95-102
10. Boury-Esnault N., Solé-Cava A.M., and Thorpe J.P. Genetic and cytological divergence between colour morphs of the Mediterranean sponge Oscarella lobularis Schmidt (Porifera, Demospongiae, Oscarellidae). J. Nat. Hist. 26 (1992) 271-284
11. Boury-Esnault N., Klautau M., Bezac C., Wulff J., and Solé-Cava A.M. Comparative study of putative conspecific sponge populations from both sides of the Isthmus of Panama. J. Mar. Biol. Assoc. UK 79 (1999) 39-50
12. Cairns S.D. Deep-water corals: an overview with special reference to diversity and distribution of deep-water Scleractinian corals. Bull. Mar. Sci. 81 (2007) 311-322
13. Calderón I., Ortega N., Duran S., Becerro M., Pascual M., and Turon X. Finding the relevant scale: clonality and genetic structure in a marine invertebrate (Crambe crambe, Porifera). Mol. Ecol. 16 (2007) 1799-1810
14. Carballo J.L., Avila E., Enriquez S., and Camacho L. Phenotypic plasticity in a mutualistic association between the sponge Haliclona caerulea and the calcareous macroalga Jania adherens induced by transplanting experiments. I: Morphological responses of the sponge. Mar. Biol. 148 (2006) 467-478
15. Cárdenas P., Xavier J., Tendal O.S., Schander C., and Rapp H.T. Redescription and resurrection of Pachymatisma normani (Demospongiae, Geodiidae), with remarks on the genus Pachymatisma. J. Mar. Biol. Assoc. UK 87 (2007) 1511-1525
16. Cárdenas P., Rapp H.T., Schander C., and Tendal O.S. Molecular taxonomy and phylogeny of the Geodiidae (Porifera, Demospongiae, Astrophorida) - combining phylogenetic and Linnaean classification. Zool. Scr. 39 (2010) 89-106
17. Cornish-Bowden A. IUPAC-IUB symbols for nucleotide nomenclature. Nucleic Acids Res. 13 (1985) 3021-3030
18. De Mol B., Henriet J.P., and Canals M. Development of coral banks in Porcupine Seabight: do they have Mediterranean ancestors?. In: Freiwald A., and Roberts J.M. (Eds). Cold-Water Corals and Ecosystems (2005), Springer, Heidelberg 515-533
19. Duran S., Pascual M., and Turon X. Low levels of genetic variation in mtDNA sequences over the western Mediterranean and Atlantic range of the sponge Crambe crambe (Poecilosclerida). Mar. Biol. 144 (2004) 31-35
20. Duran S., and Rutzler K. Ecological speciation in a Caribbean marine sponge. Mol. Phylogenet. Evol. 40 (2006) 292-297
21. Erpenbeck D., Breeuwer J.A.J., van der Velde H.C., and Van Soest R.W.M. Unravelling host and symbiont phylogenies of halichondrid sponges (Demospongiae, Porifera) using a mitochondrial marker. Mar. Biol. 141 (2002) 377-386
22. Erpenbeck D., Breeuwer J.A.J., Parra-Velandia F.J., and Van Soest R.W.M. Speculation with spiculation? Three independent gene fragments and biochemical characters versus morphology in demosponge higher classification. Mol. Phylogenet. Evol. 38 (2006) 293-305
23. Erpenbeck D., and Van Soest R.W.M. Status and perspective of sponge chemosystematics. Mar. Biotechnol. 9 (2007) 2-19
24. Erwin P.M., and Thacker R.W. Phylogenetic analyses of marine sponges within the order Verongida: a comparison of morphological and molecular data. Invertebr. Biol. 126 (2007) 220-234
25. Folmer O., Black M., Hoeh W., Lutz R., and Vrijenhoek R. DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol. Mar. Biol. Biotechnol. 3 (1994) 294-299
26. France S.C., and Hoover L.L. DNA sequences of the mitochondrial COI gene have low levels of divergence among deep-sea octocorals (Cnidaria: Anthozoa). Hydrobiologia 471 (2002) 149-155
27. Freiwald A., Fosså J.H., Grehan A., Koslow T., and Roberts J.M. Cold-water coral reefs. UNEP-WCMC, Cambridge, UK. Biodivers. Ser. 22 (2004) 1-84
28. Hughes T.P., Baird A.H., Bellwood D.R., Card M., Connolly S.R., Folke C., Grosberg R., Hoegh-Guldberg O., Jackson J.B.C., Kleypas J., Lough J.M., Marshall P., Nystrom M., Palumbi S.R., Pandolfi J.M., Rosen B., and Roughgarden J. Climate change, human impacts, and the resilience of coral reefs. Science 301 (2003) 929-933
29. Hooper J.N.A., and Van Soest R.W.M. Systema Porifera, A Guide to the Classification of Sponges (2002), Kluwer Academic/Plenum Publishers, New York
30. Jarman S.N., Ward R.D., and Elliott N.G. Oligonucleotide primers for PCR amplification of coelomate introns. Mar. Biotechnol. 4 (2002) 347-355
31. Jensen A., and Frederiksen R. The Fauna associated with the bank-forming deepwater coral Lophelia pertusa (Scleractinaria) on the Faroe shelf. Sarsia 77 (1992) 53-69
32. Jones W.C. Spicule dimensions as taxonomic criteria in the identification of Haplosclerid sponges from the Shores of Anglesey. Zool. J. Linn. Soc. 80 (1984) 239-259
33. Katoh K., Misawa K., Kuma K., and Miyata T. MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res. 30 (2002) 3059-3066
34. Klautau M., Solé-Cava A.M., and Borojevic R. Biochemical systematics of sibling sympatric species of Clathrina (Porifera: Calcarea). Biochem. Syst. Ecol. 22 (1994) 367-375
35. Klautau M., Russo C.A.M., Lazoski C., Boury-Esnault N., Thorpe J.P., and Solé-Cava A.M. Does cosmopolitanism result from overconservative systematics? A case study using the marine sponge Chondrilla nucula. Evolution 53 (1999) 1414-1422
36. Knowlton N. Molecular genetic analyses of species boundaries in the sea. Hydrobiologia 420 (2000) 73-90
37. Lazoski C., Solé-Cava A., Boury-Esnault N., Klautau M., and Russo C. Cryptic speciation in a high gene flow scenario in the oviparous marine sponge Chondrosia reniformis. Mar. Biol. 139 (2001) 421-429
38. Le Goff-Vitry M.C., Rogers A.D., and Baglow D. A deep-sea slant on the molecular phylogeny of the Scleractinia. Mol. Phylogenet. Evol. 30 (2004) 167-177
39. Le Goff-Vitry M.C., and Rogers A.D. Molecular ecology of Lophelia pertusa in the NE Atlantic. In: Freiwald A., and Roberts J.M. (Eds). Cold-Water Corals and Ecosystems (2005), Springer, Heidelberg. 653-662
40. Lindner A., Cairns S.D., and Cunningham C.W. From offshore to onshore: multiple origins of shallow-water corals from deep-sea ancestors. PLoS One 3 (2008) 1-6
41. Longo C., Mastrototaro F., and Corriero G. Sponge fauna associated with a Mediterranean deep-sea coral bank. J. Mar. Biol. Assoc. UK 85 (2005) 1341-1352
42. Maldonado M., Carmona M.G., Uriz M.J., and Cruzado A. Decline in Mesozoic reef-building sponges explained by silicon limitation. Nature 401 (1999) 785-788
43. Maldonado M. The ecology of the sponge larva. Can. J. Zool. 84 (2006) 175-194
44. Maldonado M. Embryonic development of verongid demosponges supports the independent acquisition of sponging skeletons as an alternative to the siliceous skeleton of sponges. Biol. J. Linn. Soc. 97 (2009) 427-447
45. McCormack G.P., and Kelly M. New indications of the phylogenetic affinity of Spongosorites suberitoides (Porifera, Demospongiae) as revealed by 28S ribosomal DNA. J. Nat. Hist. 36 (2002) 1009-1021
46. Meyer C.P., Geller J.B., and Paulay G. Fine scale endemism on coral reefs: archipelagic differentiation in turbinid gastropods. Evolution 59 (2005) 113-125
47. Moritz C. Defining "evolutionary significant units" for conservation. Trends Ecol. Evol. 9 (1994) 373-375
48. Morris S.A., and Andersen R.J. Nitrogenous metabolites from the deep water sponge Hexadella sp. Can. J. Chem. 67 (1989) 677
49. Mortensen P.B., Hovland M., Brattegard T., and Farestveit R. Deep-water bioherms of the scleractinian coral Lophelia pertusa (L.) at 64-Degrees-N on the Norwegian shelf-structure and associated megafauna. Sarsia 80 (1995) 145-158
50. Nylander, J., 2002. MrModeltest. Available from: .
51. Palumbi S.R. Tactics of acclimation - morphological changes of sponges in an unpredictable environment. Science 225 (1984) 1478-1480
52. Palumbi S.R. How body plans limit acclimation - responses of a demosponge to wave force. Ecology 67 (1986) 208-214
53. Palumbi S.R. Marine reserves and ocean neighborhoods: the spatial scale of marine populations and their management. Annu. Rev. Environ. Res. 29 (2004) 31-68
54. Pandolfi J.M., Bradbury R.H., Sala E., Hughes T.P., Bjorndal K.A., Cooke R.G., McArdle D., McClenachan L., Newman M.J.H., Paredes G., Warner R.R., and Jackson J.B.C. Global trajectories of the long-term decline of coral reef ecosystems. Science 301 (2003) 955-958
55. Posada D., and Crandall K.A. Modeltest: testing the model of DNA substitution. Bioinformatics 14 (1998) 817-818
56. Reveillaud J., Freiwald A., Van Rooij D., Le Guilloux E., Altuna A., Foubert A., Vanreusel A., Roy K.O.L., and Henriet J.P. The distribution of scleractinian corals in the Bay of Biscay, NE Atlantic. Facies 54 (2008) 317-331
57. Roberts J.M., Wheeler A.J., and Freiwald A. Reefs of the deep: the biology and geology of cold-water coral ecosystems. Science 312 (2006) 543-547
58. Rogers A.D. The biology of Lophelia pertusa (Linnaeus 1758) and other deep-water reef-forming corals and impacts from human activities. Int. Rev. Hydrobiol. 84 (1999) 315-406
59. Ronquist F., and Huelsenbeck J.P. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19 (2003) 1572-1574
60. Schönberg C.H.L., and Barthel D. Unreliability of demosponge skeletal characters: the example of Halichondria panicea. In: Watanabe Y., and Fusetani N. (Eds). Sponge Sciences: Multidisciplinary Perspectives (1997), Springer, Tokyo 41-53
61. Schröder-Ritzrau A., Freiwald A., and Mangini A. U/Th dating of deep-water corals from the eastern North Atlantic and the western Mediterranean Sea. In: Freiwald A., and Roberts J.M. (Eds). Cold-Water Corals and Ecosystems (2005), Springer, Heidelberg 157-172
62. Solé-Cava A.M., Boury-Esnault N., Vacelet J., and Thorpe J.P. Biochemical genetic divergence and systematics in sponges of the genera Corticium and Oscarella (Demospongiae: Homoscleromorpha) in the Mediterranean Sea. Mar. Biol. 113 (1992) 299-304
63. Solé-Cava A.M., and Boury-Esnault N. Patterns of intra and interspecific genetic divergence in marine sponges. Mem. Queens Mus. 44 (1999) 591-601
64. Stamatakis A. RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22 (2006) 2688-2690
65. Swofford D.L. PAUP*. Phylogenetic Analysis Using Parsimony (* And Other Methods), ver. 4.0. beta 10 (2002), Sinauer Associates, Sunderland, MA
66. Topsent E. Matériaux pour servir à l'étude de la faune des spongiaires de France. Mem. Soc. Zool. France 9 (1896) 113-133
67. Topsent, E., 1913. Spongiaires provenant des campagnes scientifiques de la 'Princesse Alice' dans les Mers du Nord (1898-1899-1906-1907). Résultats des campagnes scientifiques accomplies par le Prince Albert I Monaco 45, 1-67, pls I-V.
68. Vacelet J. Éponges de la Roche du Large et de l'étage bathyal de Méditérranée (Récoltes de la soucoupe plongeante Cousteau et dragages). Mem. Mus. Natl. Hist. Nat. Ser. A (Paris) 59 (1969) 145-219 pls I-IV
69. Van Soest R.W.M., and Lavaleye M.S.S. Diversity and abundance of sponges in bathyal coral reefs of Rockall Bank, NE Atlantic, from boxcore samples. Mar. Biol. Res. 1 (2005) 338-349
70. Van Soest R.W.M., Cleary D.F.R., de Kluijver M.J., Lavaleye M.S.S., Maier C., and van Duyl F.C. Sponge diversity and community composition in Irish bathyal coral reefs. Contr. Zool. 76 (2007) 121-142
71. Wörheide G., Epp L.S., and Macis L. Deep genetic divergences among Indo-Pacific populations of the coral reef sponge Leucetta chagosensis (Leucettidae): founder effects, vicariance, or both?. BMC Evol. Biol. 8 (2008) 24-42
72. Wu H., Nakamura H., Kobayashi J., Ohizumi Y., and Hirata Y. Lipopurealins, novel bromotyrosine derivatives with long-chain acyl-groups, from the marine sponge Psammaplysilla purea. Experientia 42 (1986) 855-856
73. Wulff J.L. Sponge systematics by Starfish: predators distinguish cryptic sympatric species of Caribbean fire sponges, Tedania ignis and Tedania klausi n. sp (Demospongiae, Poecilosclerida). Biol. Bull. 211 (2006) 83-94