Molecular evidence of cryptic speciation in the "cosmopolitan" excavating sponge Cliona celata (Porifera, Clionaidae)

Molecular Phylogenetics and Evolution

Volumn 56, Issue 1, 2010, Pages 13-20

  Xavier, J R ^a,b,c   Rachello Dolmen, P G ^a,b   Parra Velandia, F ^d   Schonberg C H L ^e   Breeuwer, J A J ^a   van Soest, R W M ^b  

^a UNIVERSITY OF AMSTERDAM   (Netherlands)

^b UNIVERSITY OF AMSTERDAM   (Netherlands)

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

^d UNIVERSIDAD NACIONAL DE COLOMBIA   (Colombia)

^e Institut für Bio und Umweltwissenschaften   (Germany)

Author keywords

Cryptic species; Mediterranean; Northeast Atlantic; Nuclear and mitochondrial markers; Phylogeny

Indexed keywords

MITOCHONDRIAL DNA;

ANIMAL; ARTICLE; ATLANTIC OCEAN; CELL NUCLEUS; CLASSIFICATION; DNA SEQUENCE; GENETIC VARIABILITY; GENETICS; GEOGRAPHY; MEDITERRANEAN SEA; MOLECULAR EVOLUTION; PHYLOGENY; SPECIES DIFFERENTIATION; SPONGE (PORIFERA);

ANIMALS; ATLANTIC OCEAN; CELL NUCLEUS; DNA, MITOCHONDRIAL; EVOLUTION, MOLECULAR; GENETIC SPECIATION; GENETIC VARIATION; GEOGRAPHY; MEDITERRANEAN SEA; PHYLOGENY; PORIFERA; SEQUENCE ANALYSIS, DNA;

CLIONA CELATA; CLIONAIDAE; HADROMERIDA; PORIFERA;

EID: 77953135660     PISSN: 10557903     EISSN: 10959513     Source Type: Journal    
DOI: 10.1016/j.ympev.2010.03.030     Document Type: Article

References (81)

1. Avise J.C., Nelson W.S., and Sugita H. A speciational history of "living fossils": molecular evolutionary patterns in horseshoe crabs. Evolution 48 6 (1999) 1986-2001
2. Barbieri M., Bavestrello G., and Sarà M. Morphological and ecological differences in two electrophoretically detected species of Cliona (Porifera, Demospongiae). Biol. J. Linn. Soc. 54 (1995) 193-200
3. Barucca M., Azzini F., Bavestrello G., Biscotti M.A., Calcinai B., Canapa A., Cerrano C., and Olmo E. The systematic position of some boring sponges (Demospongiae, Hadromerida) studied by molecular analysis. Mar. Biol. 151 (2007) 529-535
4. Bavestrello G., and Sarà M. Morphological and genetic differences in ecologically distinct populations of Petrosia (Porifera, Demospongiae). Biol. J. Linn. Soc. 47 (1992) 49-60
5. Bavestrello G., Calcinai B., Cerrano C., Pansini M., and Sarà M. The taxonomic status of some Mediterranean clionids (Porifera: Demospongiae) according to morphological and genetic characters. Bull. Inst. R. Sci. Nat. Belg. 66 (1996) 185-195
6. 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
7. Bell J.J. The functional roles of marine sponges. Estuarine Coastal Shelf Sci. 79 (2008) 341-353
8. Benzie J.A.H., Sandusky C., and Wilkinson C.R. Genetic structure of dictyoceratid sponge populations on the western Coral Sea reefs. Mar. Biol. 119 (1994) 335-345
9. Bickford D., Lohman D.J., Sodhi N.V., Ng P.K.L., Meier R., Winker K., Ingram K.K., and Das I. Cryptic species as a window on diversity and conservation. TREE 22 3 (2006) 148-155
10. Blanquer A., and Uriz M. Cryptic speciation in marine sponges evidenced by mitochondrial and nuclear genes: a phylogenetic approach. Mol. Phylogenet. Evol. 45 (2007) 392-397
11. Blanquer A., and Uriz M.J. "A posteriori" searching for phenotypic characters to describe new cryptic species of sponges revealed by molecular markers (Scopalina: Dictyonellidae). Invert. Syst. 22 (2008) 489-502
12. Borchiellini C., Chombard C., Manuel M., Alivon E., Vacelet J., and Boury-Esnault N. Molecular phylogeny of Demospongiae: implications for classification and scenarios of character evolution. Mol. Phylogenet. Evol. 32 (2004) 823-837
13. 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
14. 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
15. Calcinai B., Cerrano C., and Sarà M. Boring sponges (Porifera, Demospongiae) from the Indian Ocean. Ital. J. Zool. 67 (2000) 203-219
16. Calcinai B., Azzini F., Bavestrello G., Cerrano C., Pansini M., and Thung D.C. Boring sponges from Ha Long Bay, Tonkin Gulf, Vietnam. Zool. Stud. 45 2 (2006) 201-212
17. Carballo J.L., Sanchez-Moyano J.E., and Garcia-Gomez J.C. Taxonomic and ecological remarks on boring sponges (Clionidae) from the Straits of Gibraltar (southern Spain): tentative bioindicators?. Zool. J. Linn. Soc. 112 (1994) 407-424
18. Castellanos L., Duque C., Rodríguez J., and Jiménez C. Synthesis of acetylhomoagmatine. Mar. Drugs 4 (2006) 286-289
19. Clavier J. Infestation of Haliotis tuberculata shells by Cliona celata and Polydora species. In: Shepherd S.A., Tegner M.J., and Guzman del Proo S.A. (Eds). Abalone of the World, Biology, Fisheries and Culture-Supplementary Papers. Proceedings of the First International Symposium on Abalone (1989), Fishing New Books, Oxford 16-20
20. 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
21. Duran S., and Rützler K. Ecological speciation in a Caribbean marine sponge. Mol. Phylogenet. Evol. 40 (2006) 292-297
22. Erpenbeck D., Hooper J., and Wörheide G. COI phylogenies in diploblasts and the 'Barcoding of Life'-are we sequencing a suboptimal partition?. Mol. Ecol. Notes 6 (2006) 550-553
23. 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
24. Fromont J., Craig R., Rawlinson L., and Alder J. Excavating sponges that are destructive to farmed pearl oysters in Western and Northern Australia. Aquacult. Res. 36 (2005) 150-162
25. Goreau T.F., and Hartman W.D. Boring sponges as controlling factors in the formation and maintenance of coral reefs. In: Soggnaes R.F. (Ed). Mechanisms of Hard Tissue Destruction vol. 75 (1963), Publication of American Association of the Advancement Science 25-54
26. Grant R.E. Notice of a New Zoophyte (Cliona celata Gr.) from the Firth of Forth. Edinburgh New Philos. J. 1 (1826) 78-81
27. Hall T.A. Bioedit: a user-friendly biological sequence alignment, editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp. Ser. 41 (1999) 95-98
28. Hartman W.D. Ecological niche differentiation in the boring sponges (Clionidae). Evol. 11 3 (1957) 294-297
29. Hartman W.D. Natural history of the marine sponges of southern New England. Peabody Mus. Nat. Hist.: Yale Univ. Bull. 12 (1958) 1-155
30. Hoeksema B.W. Excavation patterns and spiculae dimensions of the boring sponge Cliona celata from the SW Netherlands. Senckenbergiana Marit. 15 (1983) 55-85
31. Hooper J.N.A., and Lévi C. Biogeography of the Indo-West Pacific sponges: Microcionidae, Raspailiidae, Axinellidae. In: van Soest R.W.M., Van Kempen T., and Braekman J.C. (Eds). Sponges in Time and Space (1994), Balkema, Rotterdam 191-212
32. Huelsenbeck J.P., and Ronquist F. MrBayes: Bayesian inference of phylogenetic trees. Bioinformatics 17 (2001) 754-755
33. Keyzers R.A., Daoust J., Davies-Coleman M.T., van Soest R.W.M., Balgi A., Donohue E., Roberge M., and Andersen R.J. Autophagy-modulating aminosteroids isolated from the sponge Cliona celata. Org. Lett. 10 14 (2008) 2959-2962
34. Klautau M., Solé-Cava A.M., and Borojevic R. Biochemical systematics of sibling sympatric species of Clathrina (Porifera: Calcarea). Biochem. Syst. Ecol. 22 4 (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 5 (1999) 1414-1422
36. Knowlton N. Sibling species in the sea. Ann. Rev. Ecol. Syst. 24 (1993) 189-216
37. Knowlton N. Molecular genetic analyses of species boundaries in the sea. Hydrobiologia 420 (2000) 73-90
38. Kumar S., Tamura K., and Nei M. MEGA3: integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief. Bioinform. 5 (2004) 150-163
39. Lazoski C., Solé-Cava A.M., Boury-Esnault N., Klautau M., and Russo C.A. Cryptic speciation in a high gene flow scenario in the oviparous marine sponge Chondrosia reniformis. Mar. Biol. 139 (2001) 421-429
40. López-Legentil S., and Pawlik J.R. Genetic structure of the Caribbean giant barrel sponges Xestospongia muta using the I3-M11 partition of COI. Coral Reefs 28 (2008) 157-165
41. Loukaci A., Muricy G., Brouard J.P., Guyot M., Vacelet J., and Boury-Esnault N. Chemical divergence between two sibling species of Oscarella (Porifera) from the Mediterranean Sea. Biochem. Syst. Ecol. 32 (2004) 893-899
42. Maldonado M. The ecology of sponge larvae. Can. J. Zool. 84 (2006) 175-194
43. Mariani S., Uriz M., and Turon X. The dynamics of sponge larvae assemblages from northwestern Mediterranean nearshore bottoms. J. Plankton Res. 27 3 (2005) 249-262
44. Mariani S., Uriz M., Turon X., and Alcoverro T. Dispersal strategies in sponge larvae: integrating the life history of larvae and the hydrologic component. Oecologia 149 (2006) 174-184
45. Marques D., Almeida M., Xavier J.R., and Humanes M. Biomarkers in marine sponges: acetylcholinesterase in the sponge Cliona celata. In: Custódio M.R., Lôbo-Hajdu G., Hajdu E., and Muricy G. (Eds). Porifera Research: Biodiversity, Innovation and Sustainability. Série Livros, vol. 28 (2007), Museu Nacional, Rio de Janeiro 427-432
46. Marques D., Esteves A.I., Almeida M., Xavier J.R., and Humanes M. Superoxide dismutase in the marine sponge Cliona celata. Mar. Biol. 153 (2008) 807-813
47. Miller K., Alvarez B., Battershill C., Northcote P., and Parthasarathy H. Genetic, morphological and chemical divergence in the sponge genus Latrunculia (Porifera: Demospongiae) from New Zealand. Mar. Biol. 139 (2001) 235-250
48. Munro M.H.G., Blunt J.W., Dumdei E.J., Hickford S.J.H., Lill R.E., Li S., Battershill C.N., and Duckworth A.R. The discovery and development of marine compounds with pharmaceutical potential. J. Biotechnol. 70 (1999) 15-25
49. Muricy G., Solé-Cava A.M., Thorpe J.P., and Boury-Esnault N. Genetic evidence for extensive cryptic speciation in the subtidal sponge Plakina trilopha (Porifera: Demospongiae: Homoscleromorpha). Mar. Ecol. Prog. Ser. 138 (1996) 181-187
50. Nichols S.A., and Barnes P.A.G. A molecular phylogeny and historical biogeography of the marine sponge genus Placospongia (Phylum Porifera) indicate low dispersal capabilities and widespread crypsis. J. Exp. Mar. Biol. Ecol. 323 (2005) 1-15
51. Nicol W.L., and Reisman H.M. Ecology of the boring sponge (Cliona celata) at Gardiner's Island, New York. Chesapeake Sci. 17 (1976) 1-7
52. Posada D., and Crandall K.A. Modeltest: testing the model of DNA substitution. Bioinformatics 15 (1998) 817-818
53. Rosell D., and Uriz M.J. Phylogenetic relationships within the excavating Hadromerida (Porifera), with a systematic revision. Cladistics 13 (1997) 349-366
54. Rosell D., and Uriz M.J. Excavating and endolithic sponge species (Porifera) from the Mediterranean: species descriptions and identification key. Org. Div. Evol. 2 (2002) 55-86
55. Rosell D., Uriz M.J., and Martin D. Infestation by excavating sponges on the oyster (Ostrea edulis) populations of the Blanes littoral zone (northwestern Mediterranean Sea). J. Mar. Biol. Assoc. UK 79 (1999) 409-413
56. Rozas J., Sanchez-Delbarrio J., Messeguer X., and Rozas R. DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19 (2003) 2496-2497
57. Rützler K. Family Clionaidae D'Orbigny, 1851. 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 173-185
58. Rützler K., Duran S., and Piantoni C. Adaptation of reef and mangrove sponges to stress: evidence for ecological speciation exemplified by Chondrilla caribensis new species (Demospongiae, Chondrosida). Mar. Ecol. 28 (2007) 95-111
59. Sarà M., Corriero G., and Bavestrello G. Tethya (Porifera, Demospogiae) species coexisting in a Maldivian coral reef lagoon: taxonomical, genetic and ecological data. Mar. Ecol. 14 4 (1993) 341-355
60. Schönberg C.H.L. Bioeroding sponges common to the Central Australian Great Barrier Reef: description of three new species, two new records, and addition to two previously described species. Senckenbergiana Marit. 30 (2000) 161-221
61. Schönberg C.H.L. A history of sponge erosion: from past myths and hypotheses to recent approaches. In: Wisshak M., and Tapanila L. (Eds). Current Developments in Bioerosion (2008), Springer, Berlin 165-202
62. Schönberg C.H.L., Grass S., and Heiermann A.T. Cliona minuscula sp. nov. (Hadromerida: Clionaidae) and other bioeroding sponges that only contain tylostyles. Zootaxa 1312 (2006) 1-24
63. Solé-Cava A.M., Boury-Esnault N., Vacelet J., and Thorpe J.P. Biochemical genetic divergence in sponges of the genera Corticium and Oscarella (Demospongiae: Homoscleromorpha) in the Mediterranean Sea. Mar. Biol. 113 (1992) 299-304
64. Solé-Cava A.M., Klautau M., Boury-Esnault N., Borojevic R., and Thorpe J.P. Genetic evidence for cryptic speciation in allopatric populations of two cosmopolitan species of the calcareous sponge genus Clathrina. Mar. Biol. 111 (1991) 381-386
65. Solé-Cava A.M., and Thorpe J.P. Genetic differentiation between morphotypes of the marine sponge Suberites ficus (Demospongiae: Hadromerida). Mar. Biol. 93 (1986) 247-253
66. Solé-Cava A.M., Thorpe J.P., and Manconi R. A new Mediterranean species of Axinella detected by biochemical genetic methods. In: Keupp H., and Reitner J. (Eds). Fossil and Recent Sponges (1991), Springer, Berlin 313-321
67. Swofford D.L. PAUP*: Phylogenetic Analysis Using Parsimony (and Other Methods). 4.0 Beta for UNIX or OpenVMS (2002), Sinauer Associates, Sunderland, Massachusetts
68. Topsent E. Contribution à l'étude des Clionides. Arch. Zool. Exp. Gen. 5 2 (1888) 1-165
69. Topsent E. Etude monographique des spongiaires de France: III. Monaxonida (Hadromerina). Arch. Zool. Exp. Gen. 8 3 (1900) 1-331
70. Uriz M.J., Turon X., and Mariani S. Ultrastructure and dispersal potential of sponge larvae: tufted versus evenly ciliated parenchymellae. Mar. Ecol. 29 (2008) 280-297
71. van Soest R.W.M., Picton B., and Morrow C. Sponges of the Northeast Atlantic. World Biodiversity Database CD-ROM Series (2000), ETI Expert Center for Taxonomic Identification, University of Amsterdam, The Netherlands
72. van Soest, R.W.M., Boury-Esnault, N., Hooper, J.N.A., Rützler, K., de Voogd, N.J., Alvarez, B., Hajdu, E., Pisera, A.B., Vacelet, J., Manconi, R., Schönberg, C., Janussen, D., Tabachnick, K.R., Klautau, M., Picton, B., 2008. World Porifera database. (consulted 12.11.08).
73. Volz P. Die Bohrschwämme (Clioniden) der Adria. Thalassia 3 (1939) 1-64
74. Vacelet J., and Vasseur P. Eponges des récifs coralliens de Tuléar (Madagascar). Tethys 1 (1971) 51-126
75. Wesche S.J., Adlard R.D., and Hooper J.N.A. The first incidence of clionid sponges (Porifera) from the Sidney rock oyster Saccostrea commercialis (Iredale and Roughley, 1933). Aquaculture 157 (1997) 173-180
76. Wörheide G. Low variation in partial cytochrome oxidase subunit I (COI) mitochondrial sequences in the coralline demosponge Astrosclera willeyana across the Indo-Pacific. Mar. Biol. 148 (2006) 907-912
77. Wörheide, G., Degnan, B.M., Hooper, J.N.A., Reitner, J., 2000. Phylogeography and taxonomy of the Indo-Pacific reef cave dwelling coralline demosponge Astrosclera 'willeyana': new data from nuclear internal transcribed spacer sequences. In: Moosa, K., et al. (Eds.), Proceedings of the Ninth International Coral Reef Symposium, vol. 1, pp. 339-346.
78. 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 10.1186/1471-2148-8-24
79. Wörheide G., and Erpenbeck D. DNA taxonomy of sponges-progress and perspectives. J. Mar. Biol. Assoc. UK 87 (2007) 1629-1633
80. Wörheide G., Erpenbeck D., and Menke C. The Sponge Barcoding Project: aiding in the identification and description of poriferan taxa. In: Custódio M.R., Lôbo-Hajdu G., Hajdu E., and Muricy G. (Eds). Porifera Research: Biodiversity, Innovation and Sustainability. Série Livros, vol. 28 (2007), Rio de Janeiro, Museu Nacional 123-128
81. Wulff J. Sponge systematics by starfish: predators distinguish sympatric species of Caribbean fire sponges, Tedania ignis and Tedania klausi n. sp. (Demospongiae, Poecilosclerida). Biol. Bull. 211 (2006) 83-94