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Staying well connected – Lithistid sponges on seamounts

Published online by Cambridge University Press:  22 June 2015

Merrick Ekins*
Affiliation:
Queensland Museum, PO Box 3300, South Brisbane 4101, Brisbane, Queensland, Australia
Dirk Erpenbeck
Affiliation:
Department of Earth and Environmental Sciences and GeoBio-Center, Ludwig-Maximilians-Universität München, Richard-Wagner-Straße 10, 80333 München, Germany
Gert Wörheide
Affiliation:
SNSB – Bavarian State Collections for Palaeontology and Geology, Richard-Wagner-Straße 10, 80333 München, Germany
John N. A. Hooper
Affiliation:
Queensland Museum, PO Box 3300, South Brisbane 4101, Brisbane, Queensland, Australia Eskitis Institute for Drug Discovery, Griffith University, Brisbane 4111, Queensland, Australia
*
Correspondence should be addressed to:M. Ekins, Queensland Museum, PO Box 3300, South Brisbane 4101, Brisbane, Queensland, Australia email: m.ekins@qm.qld.gov.au

Abstract

Three species of lithistid sponges, Neoaulaxinia zingiberadix, Isabella mirabilis and Neoschrammeniella fulvodesmus were collected from deep seamounts off New Caledonia to address questions about their population structure, gene flow and the relative contribution of sexual and asexual reproductive strategies to their populations. The sponges were tested by sequencing the ITS (internal transcribed spacer) and CO1 regions of their genomes. These rare and presumably ancient sponges have a distribution restricted to seamounts in the south-western Pacific. Deep seamounts represent geographically separated islands. Although the sponges could be expected to have sexual reproduction restricted to near neighbours due to low sexual dispersal opportunities via larvae, this study found surprisingly high levels of gene flow between the seamounts. Amongst the specimens of N. zingiberadix taken from two seamounts there was no population structure; CO1 resulted in identical genotypes. For the population structure within N. fulvodesmus, as revealed by ITS, most of the variation was within each individual from the six seamounts on which it occurred and CO1 revealed no difference between individuals or seamounts. The third species I. mirabilis showed four genotypes based on CO1, which were distributed across all the seamounts. Indirect measures of different species showed a range of reproductive strategies from asexual to sexual, but with much higher connection between seamounts than previously thought. Individual seamounts did not show a separate population structure as one might expect from ‘islands’. The conclusion must be that these sponges have mechanisms to attain greater dispersal than previously thought.

Type
Research Article
Copyright
Copyright © Marine Biological Association of the United Kingdom 2015 

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References

REFERENCES

Atlas of Living Australia (ALA) (2014). Available at: http://bie.ala.org.au/ (accessed 16 April 2014).Google Scholar
Ayre, D.J. and Willis, B.L. (1988) Population structure in the coral Pavona cactus: clonal genotypes show little phenotypic plasticity. Marine Biology 99, 495505.CrossRefGoogle Scholar
Battershill, C.N. and Bergquist, P.R. (1990) The influence of storms on asexual reproduction, recruitment, and survivorship of sponges. In Rützler, K. (eds) New perspectives in sponge biology. Washington, DC: Smithsonian Institution Press, pp. 397403.Google Scholar
Bautista-Guerrero, E., Carballo, J.L. and Maldonado, M. (2010) Reproductive cycle of the coral-excavating sponge Thoosa mismalolli (Clionaidae) from Mexican Pacific coral reefs. Invertebrate Biology 129, 285296.CrossRefGoogle Scholar
Bentlage, B. and Worheide, G. (2007) Low generic structuring among Pericharax heteroraphis (Porifera; Calcarea) population from the Great Barrier Reef (Australia), revealed by analysis of nrDNA and nuclear intron sequences. Coral Reefs 26, 807816.CrossRefGoogle Scholar
Blanquer, A. and Uriz, M.J. (2007) Cryptic speciation in marine sponges evidenced by mitochondrial and nuclear genes. A phylogenetic approach. Molecular Phylogenetics and Evolution 45, 392397.CrossRefGoogle Scholar
Blanquer, A. and Uriz, M.J. (2011) “Living together apart”: the hidden genetic diversity of sponge populations. Molecular Biology and Evolution 28, 24352438.CrossRefGoogle ScholarPubMed
Blanquer, A., Uriz, M.J. and Caujape-Castells, J. (2009) Small-scale spatial genetic structure in Scopalina lophyropoda, and encrusting sponge with philopatric larval dispersal and frequent fission and fusion events. Marine Ecology Progress Series 380, 95102.CrossRefGoogle Scholar
Blanquer, A., Uriz, M.J. and Pascal, M. (2005) Polymorphic microsatellite loci isolated from the marine sponge Scopalina lophyropoda (Demospongiae: Halichondrida). Molecular Ecology Notes 5, 466468.CrossRefGoogle Scholar
Bohonak, A.J. (1999) Dispersal, gene flow and population structure. Quarterly Review of Biology 74, 2145.CrossRefGoogle ScholarPubMed
Boisselier-Dubayle, M.C. (1999) Genetic relationships between marine and marginal-marine populations of Cerithium species from the Mediterranean Sea. Marine Biology 135, 671682.CrossRefGoogle Scholar
Bond, C. and Harris, A.K. (1988) Locomotion of sponges and its physical mechanism. Journal of Experimental Zoology 246, 271284.CrossRefGoogle ScholarPubMed
Borchiellini, C., Alivon, E. and Vacelet, J. (2004) The systematic position of Alectona (Porifera, Demospongiae): a tetractinellid sponge. Bollettino dei Musei e degli Istituti Biologici della Università di Genova 68, 209217.Google Scholar
Buss, L.W. (1982) Somatic cell parasitism and the evolution of somatic tissue compatibility. Proceedings of the National Academy of Sciences USA 79, 53375341.CrossRefGoogle ScholarPubMed
Calderon, I., Ortega, N., Duran, S., Becerro, M.A., Pascal, M. and Turon, X. (2007) Finding the relevant scale: clonality and genetic structure in a marine invertebrate (Carme crambe, Porifera). Molecular Ecology 16, 17991810.CrossRefGoogle Scholar
Clark, M.R., Schlacher, T.A., Rowden, A.A., Stocks, K.I. and Consalvey, M. (2012) Science priorities for seamounts: research links to conservation and management. PLoS ONE, e29232. doi:10.1371/journal.pone.0029232.Google ScholarPubMed
Collin, R. (2001) The effects of mode of development on phylogeography and population structure of North Atlantic Crepidula (Gastropoda: Calyptraeidae). Molecular Ecology 10, 22492262.CrossRefGoogle ScholarPubMed
Dailianis, T., Tsigenopoulos, C.S., Dounas, C. and Voultsiadou, E. (2011) Genetic diversity of the imperilled bath sponge Spongia officinalis Linnaeus, 1759 across the Mediterranean Sea: patterns of population differentiation and implications for taxonomy and conservation. Molecular Ecology 20, 37573772.CrossRefGoogle ScholarPubMed
Duran, S., Giribet, G. and Turon, X. (2004a) Phylogeographical history of the sponge Crambe crambe (Porifera, Poecilosclerida): range expansion and recent invasion of the Macaronesian islands from the Mediterranean Sea. Molecular Ecology 13, 109122.CrossRefGoogle ScholarPubMed
Duran, S., Pascal, M., Estoup, A. and Turon, X. (2004c) Strong population structure in the marine sponge Crambe crambe (poecilosclerida) as revealed by microsatellite markers. Molecular Ecology 13, 511522.CrossRefGoogle ScholarPubMed
Duran, S., Pascal, M., Estoup, A. and Turon, X. (2002) Polymorphic microsatellite loci in the sponge Crambe crambe (Porifera: Poecilosclerida) and their variation in two distant populations. Molecular Ecology Notes 2, 478480.CrossRefGoogle Scholar
Duran, S., Pascual, M. and Turon, X. (2004b) Low levels of genetic variation in mtDNA sequences over the western Mediterranean and Atlantic range of the sponge Crambe crambe (Poecilosclerida) Crambe crambe (Poecilosclerida). Marine Biology 144, 3135.CrossRefGoogle Scholar
Duran, S. and Rützler, K. (2006) Ecological speciation in a Caribbean marine sponge. Molecular Phylogenetics and Evolution 40, 292297.CrossRefGoogle Scholar
Edgar, R.C. (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research 32, 17921797.CrossRefGoogle ScholarPubMed
Ereskovsky, A.V. (2010) The comparative embryology of sponges. Saint-Petersburg: Springer.CrossRefGoogle Scholar
Ereskovsky, A.V. and Tokina, D.B. (2007) Asexual reproduction in homoscleromorph sponges (Porifera; Homoscleromorpha). Marine Biology 151, 425434.CrossRefGoogle Scholar
Erpenbeck, D., Hooper, J.N.A. and Wörheide, G. (2006) CO1 phylogenies in diploblasts and the ‘Barcoding of Life’ – are we sequencing a suboptimal partition? Molecular Ecology Notes 6, 550553.CrossRefGoogle Scholar
Excoffier, L., Laval, G. and Schneider, S. (2005) Arlequin ver. 3.0: an integrated software package for population genetics data analysis. Evolutionary Bioinformatics Online 1, 4750.Google Scholar
Foster, N.L., Iliana, B.B. and Mumby, P.J. (2007) Sexual vs. asexual recombination in an ecosystem engineer: the massive coral Montastrea annularis. Journal of Animal Ecology 76, 384391.CrossRefGoogle Scholar
Fromont, J. and Bergquist, P.R. (1994) Reproductive biology of three sponge species of the genus Xestospongia (Porifera: Demospongiae: Petrosiida) from the Great Barrier Reef. Coral Reefs 13, 119126.CrossRefGoogle Scholar
Galtier, N., Gouy, M. and Gautier, C. (1996) SEAVIEW and PHYLO_WIN: two graphic tools for sequence alignment and molecular phylogeny. Computer Applications in the Biosciences 12, 543548.Google ScholarPubMed
Hall, K.A., Ekins, M.G. and Hooper, J.N.A. (2014) Two new desma-less species of Theonella Gray, 1868, (Demospongiae: Astrophorida: Theonellidae) from the Great Barrier Reef, Australia, and a re-evaluation of one species assigned previously to Dercitus Gray, 1867. Zootaxa 3814, 451477.CrossRefGoogle Scholar
Hall, T.A. (1999) Bioedit: a user friendly biological sequence alignment editor and analyis program for Windows 95/98/NT. Nuclei Acids Symposium Series 41, 9598.Google Scholar
Hooper, J.N.A. and Van Soest, R.W.M. (2002) Systema Porifera. A guide to the classification of sponges. New York: Kluwer Academic/Plenum Publishers.CrossRefGoogle Scholar
Hoshino, S., Saito, D.S. and Fujita, T. (2008) Contrasting genetic structure of two Pacific Hymeniacidon species. Hydrobiologia 603, 313326.CrossRefGoogle Scholar
Hughes, T.P., Ayre, D.J. and Connell, J.H. (1992) Evolutionary ecology of corals. Trends in Ecology and Evolution 40, 357365.Google Scholar
Jablonski, D. (1986) Larval ecology and macroevolution in marine invertebrates. Bulletin of Marine Science 39, 565587.Google Scholar
Jackson, J.B.C. (1986) Modes of dispersal of clonal benthic invertebrates: consequences for species’ distributions and genetic structure of local populations. Bulletin of Marine Science 39, 588606.Google Scholar
Kaye, H.R. (1990) Reproduction in West Indian commercial sponges: oogenesis, larval development, and behaviour. In Rützler, K. (eds) New perspectives in sponge biology. Washington, DC: Smithsonian Institution Press, pp. 161435.Google Scholar
Kelly, M. (2007) The marine fauna of New Zealand: Porifera: lithistis Demospongiae (Rock Sponges). NIWA Biodiversity Memoir 121, 1100.Google Scholar
Klautau, M., Russo, C.A.M., Lazoski, C., Boury-Esnault, N., Thorpe, J.P. and Solé-Cava, A.M. (1999) Does cosmopolitanism result from overconservative systematics? A case study using the marine sponge Chondrilla nucula. Evolution 53, 14141422.CrossRefGoogle ScholarPubMed
Kyle, C.J. and Boulding, E.G. (2000) Comparative population genetic structure of marine gastropods (Littorina spp.) with and without pelagic larval dispersal. Marine Biology 137, 835845.CrossRefGoogle Scholar
Le Goff-Vitry, M.C., Pybus, O.G. and Rogers, A.D. (2004) Genetic structure of the deep-sea coral Lophelia pertusa in the northeast Atlantic revealed by microsatellites and internal transcribed spacer sequences. Molecular Ecology 13, 537549.CrossRefGoogle ScholarPubMed
Leong, W. and Pawlik, J.R. (2010) Fragments of propagules? Reproductive tradeoffs among Callyspongia spp. from Florida coral reefs. Oikos 119, 14171422.CrossRefGoogle Scholar
Lévi, C. (1991) Lithistid sponges from the Norfolk Rise. Recent and Mesozoic genera. In Reitner, J. and Keupp, H. (eds) Fossil and recent sponges. Berlin: Springer-Verlag, pp. 7282.CrossRefGoogle Scholar
Lévi, C. and Lévi, P. (1983) Éponges Tétractinellides et Lithistides bathyales de Nouvelle-Calédonie. Bulletin du Muséum National d'Histoire Naturelle, Paris (4) 5, 101168.CrossRefGoogle Scholar
Longo, C., Pontassuglia, C., Corriero, G. and Gaino, E. (2012) Life-cycle traits of Paraleucilla magna, a calcerous sponge invasive in a coastal Mediterranean basin. PLoS ONE 7, 112.CrossRefGoogle Scholar
Lopez, J.V., Peterson, C.L., Willoughby, R., Wright, A.E., Enright, E., Zoladz, S., Reed, J.K. and Pomponi, S.A. (2002) Characterization of genetic markers for in vitro cell line identification of the marine sponge Axinella corrugata. Journal of Heredity 93, 2736.CrossRefGoogle ScholarPubMed
Maldonado, M. (1998) Do chimeric sponges have improved chances of survival? Marine Ecology Progress Series 164, 301306.CrossRefGoogle Scholar
Maldonado, M. (2004) Choanoflagellates, choanocytes, and animal multicellularity. Invertebrate Biology 123, 231242.CrossRefGoogle Scholar
Maldonado, M. and Bergquist, P.R. (2002) Phylum porifera. In Young, C. (eds) Atlas of marine invertebrate larvae. San Diego, CA: Academic Press, pp. 2149.Google Scholar
Maldonado, M. and Riesgo, A. (2008) Reproduction in the Phylum Porifera: a synoptic overview. Treballs de la SCB 59, 2949.Google Scholar
Maldonado, M. and Uriz, M.J. (1999a) Sexual propagation by sponge fragments. Nature 398, 476.CrossRefGoogle Scholar
Maldonado, M. and Uriz, M.J. (1999b) An experimental approach to the ecological significance of microhabitat-scale movement in an encrusting sponge. Marine Ecology Progress Series 185, 239255.CrossRefGoogle Scholar
Meyer, C.P., Geller, J.B. and Paulay, G. (2005) Fine scale endemism on coral reefs: archipelagic differentiation in turbinid gastropods. Evolution 59, 113125.Google ScholarPubMed
Miller, K.J. and Ayre, D.J. (2004) The role of sexual and asexual reproduction in structuring high latitude populations of the reef coral Pocillopora damicornis. Heredity 92, 557568.CrossRefGoogle ScholarPubMed
Morrison, C.L., Ross, S.W., Nizinski, M.S., Brooke, S., Jarnegren, J., Waller, R.G., Johnson, R.L. and King, T.L. (2011) Genetic discontinuity among regional populations of Lophelia pertusa in the North Atlantic Ocean. Conservation Genetics 12, 713729.CrossRefGoogle Scholar
Neigel, J.E. and Avise, J.C. (1983) Histocompatibility bioassays of population structure in marine sponges. Clonal structure in Verongia longissima and Iotrochota birotulata. Journal of Heredity 74, 134140.CrossRefGoogle Scholar
Nichols, S.A. and Barnes, P.A.G. (2005) A molecular phylogeny and historical biogeography of the marine sponge genus Placospongia (Phylum Porifera) indicate low dispersal capabilities and widespread crypsis. Journal of Experimental Marine Biology and Ecology 323, 115.CrossRefGoogle Scholar
Perez-Portela, R. and Turon, X. (2008) Cryptic divergence and strong population structure in the colonial invertebrate Pycnoclavella communis (Ascidiacea) inferred from molecular data. Zoology 111, 163178.CrossRefGoogle ScholarPubMed
Pisera, A. and Lévi, C. (2002) ‘Lithistid’ Demospongiae. In Hooper, J.N.A. and Van Soest, R.W.M. (eds) Systema Porifera: a guide to the classification of sponges. New York: Kluwer Academic/Plenum Publishers.Google Scholar
Puill-Stephan, E., Willis, B.L., van Herwerden, L. and van Oppen, J.H. (2009) Chimerism in wild adult populations of the broadcast spawning coral Acropora millepora on the Great Barrier Reef. PLoS ONE 4, e7751.CrossRefGoogle ScholarPubMed
Reiswig, H.M. (1973) Population dynamics of three Jamaican Demospongiae. Bulletin of Marine Science 23, 191226.Google Scholar
Richer de Forges, B., Koslow, J.A. and Poore, G.C.B. (2000) Diversity and endemism of the benthic seamount fauna in the southwest Pacific. Nature 405, 944947.CrossRefGoogle Scholar
Ridgway, K.R. and Dunn, J.R. (2003) Mesoscale structure of the mean East Australian Current System and its relationship with topography. Progress in Oceanography 56, 189222.CrossRefGoogle Scholar
Samadi, S., Bottan, L., Macpherson, E. and Richer de Forges, B. and Boisselier, M.C. (2006) Seamount endemism questioned by the geographic distribution and population genetic structure of marine invertebrates. Marine Biology 149, 14631475.CrossRefGoogle Scholar
Samadi, S., Schlacher, T. and Richer de Forges, B. (2007) Seamount benthos. In Pitcher, T.J., Horato, T., Hart, P.J.B., Clark, M.R., Hagger, N. and Santos, R.S. (eds) Seamounts: ecology, fisheries and conservation. Carlton: Blackwell Publishing.Google Scholar
Sambrook, J., Fritsch, E.F. and Maniatis, T. (1989) Molecular cloning: a laboratory manual, 2nd edn.Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.Google Scholar
Sarà, A., Cerrano, C. and Sara, M. (2002) Viviparious development in the Antarctic sponge Stylocordyla borealis Loven, 1868. Polar Biology 25, 425431.CrossRefGoogle Scholar
Schlacher-Hoenlinger, M.A., Pisera, A. and Hooper, J.N.A. (2005) Deep-sea “lithistid” assemblages from the Norfolk Ridge (New Caledonia), with description of seven new species and a new genus (Porifera, Demospongiae). Zoosystema 27, 649698.Google Scholar
Schmitt, S., Hentschel, U., Zea, S., Dandekar, T. and Wolf, M. (2005) ITS-2 and 18S gene phylogeny of Aplysiniidae (Verongida, Demospongiae). Journal of Molecular Evolution 60, 237336.CrossRefGoogle ScholarPubMed
Schuster, A., Erpenbeck, D., Pisera, A., Hooper, J.N.A., Bryce, M., Fromont, J. and Wörheide, G. (2015) Deceptive desmas: molecular phylogenetics suggests a new classification and uncovers convergent evolution of lithistid demosponges. PLoS ONE 10, e116038.CrossRefGoogle ScholarPubMed
Shearer, T.L., Van Oppen, M.J.H., Romano, S.L. and Wörheide, G. (2002) Slow mitochondrial DNA sequence evolution in the Anthozoa (Cnidaria). Molecular Ecology 11, 24752487.CrossRefGoogle ScholarPubMed
Silva, E.P. and Russo, C.A.M. (2000) Techniques and statistical data analysis in molecular population genetics. Hydrobiologia 420, 119135.CrossRefGoogle Scholar
Sommerfeldt, A.D., Bishop, J.D.D. and Wood, C.A. (2003) Chimerism following fusion in a clonal ascidian (Urochordata). Biological Journal of the Linnean Society 79, 182192.CrossRefGoogle Scholar
Stamatakis, A. (2006) RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22, 26882690.CrossRefGoogle ScholarPubMed
Teixido, N., Gili, J.P., Uriz, M.J., Gutt, J. and Arntz, W.E. (2006) Observations of asexual reproductive strategies in Antarctic hexactinellid sponges from ROV video records. Deep Sea Research II 53, 972984.CrossRefGoogle Scholar
Todd, C.D., Lambert, W.J. and Thorpe, J.P. (1998) The genetic structure of intertidal populations of two species of nudibranch mollusks with planktotrophic and pelagic lecithotrophic larval stages: are pelagic larvae ‘for’ dispersal? Journal of Experimental Marine Biology and Ecology 228, 128.CrossRefGoogle Scholar
Uriz, M.J. and Turon, X. (2012) Sponge ecology in the molecular era. Advances in Marine Biology 61, 345410.CrossRefGoogle ScholarPubMed
Vargas, S., Erpenbeck, D., Schuster, A., Sacher, K., Büttner, G., Schätzle, S. and Wörheide, G. (2010) A high-throughput, low-cost Porifera DNA barcoding pipeline. In VIII. World Sponge Conference. Girona, Spain.Google Scholar
Whalan, S., De Nys, C., Smith-Keune, R., Evans, B.R., Battershill, C.N. and Jerry, D.R. (2008) Low genetic variability within and among populations of the brooding sponge Rhopaloeides odorabile on the central Great Barrier Reef. Aquatic Biology 3, 111119.CrossRefGoogle Scholar
Wörheide, G. (2006) Low variation in partial cytochrome oxidase subunit i (CO1) across mitochondrial sequences in the coralline demosponge Astrosclera willeyana across the Indo-Pacific. Marine Biology 148, 907912.CrossRefGoogle Scholar
Wörheide, G., Degnan, B.M., Hooper, J.N.A. and Reitner, J. (2002b) Biogeography and taxonomy of the Indo-Pacific reef cave dwelling coralline demosponge Astrosclera ‘willeyana': new data from nuclear internal transcribed spacer sequences. In Moosa, K.M., et al. (eds) Proceedings of the 9th International Coral Reef Symposium, Bali, Indonesia 23–27 October 2000. State Ministry for the Environment, Indonesia, Indonesian Institute of Sciences & The International Society for Reef Studies, pp. 339345.Google Scholar
Wörheide, G., Epp, L.S. and Macis, L. (2008) Deep genetic divergences among Indo-Pacific populations of the coral reef sponge Leucetta chagosensis (Leucettidae): founder effects, vicariance, or both? BMC Evolutionary Biology 8, 118.CrossRefGoogle ScholarPubMed
Wörheide, G. and Erpenbeck, D. (2007) DNA taxonomy of sponges – progress and perspectives. Journal of the Marine Biological Association of the United Kingdom 87, 16291633.CrossRefGoogle Scholar
Wörheide, G., Hooper, J. and Degnan, B.M. (2002a) Phylogeography of western Pacific Leucettachagosensis’ (Porifera: Calcarea) from ribosomal DNA sequences: implications for population history and conservation of the Great Barrier Reef World Heritage Area (Australia). Molecular Ecology 11, 17531768.CrossRefGoogle ScholarPubMed
Wörheide, G., Nichols, S.A. and Goldberg, J. (2004) Intragenomic variation of the rDNA internal transcribed spacers in sponges (Phylum Porifera): implications for phylogenetic studies. Molecular Phylogenetics and Evolution 33, 816830.CrossRefGoogle ScholarPubMed
Wörheide, G., Solé-Cava, A.M. and Hooper, J.N.A. (2005) Biodiversity, molecular ecology and phylogeography of marine sponges: patterns, implications and outlooks. Integrative and Comparative Biology 45, 377385.CrossRefGoogle ScholarPubMed
Wulff, J.L. (1990) Patterns and processes of size change in Caribbean demosponges of branching morphology. In Rützler, K. (eds) New perspectives in sponge biology. Washington, DC: Smithsonian Institution Press, pp. 425435.Google Scholar
Wulff, J.L. (1991) Asexual fragmentation, genotype success and population dynamics of erect branching sponges. Journal of Experimental Marine Biology and Ecology 149, 227247.CrossRefGoogle Scholar
Xavier, J.R., Rachello-Dolmen, P.G., Parra-Velandia, F., Schönbeg, C.H.L., Brewer, J.A.J. and Van Soest, R.W.M. (2010) Molecular evidence of cryptic speciation in the “cosmopolitan” excavating sponge Cliona celata (Porifera, Clionaidae). Molecular Phylogenetics and Evolution 56, 1320.CrossRefGoogle ScholarPubMed
Zilberberg, C., Maldonado, M. and Solé-Cava, A.M. (2006b) Assessment of the relative contribution of asexual propagation in a population of the coral-excavating sponge Cliona delitrix from the Bahamas. Coral Reefs 25, 297301.CrossRefGoogle Scholar
Zilberberg, C., Solé-Cava, A.M. and Klautau, M. (2006a) The extent of asexual reproduction in sponges of the genus Chondrilla (Demospongiae: Chondrosida) from the Caribbean and the Brazilian coasts. Journal of Experimental Marine Biology and Ecology 336, 211220.CrossRefGoogle Scholar