Hostname: page-component-cd9895bd7-fscjk Total loading time: 0 Render date: 2024-12-26T12:42:25.023Z Has data issue: false hasContentIssue false
  • English
  • Français

MtDNA diversity of the Indonesian giant barrel sponge Xestospongia testudinaria (Porifera: Haplosclerida) – implications from partial cytochrome oxidase 1 sequences

Published online by Cambridge University Press:  09 September 2015

Edwin Setiawan ,
Nicole J. de Voogd ,
Thomas Swierts ,
John N.A. Hooper ,
Gert Wörheide  and
Dirk Erpenbeck
Edwin Setiawan
Affiliation:
Department of Earth and Environmental Sciences, Palaeontology & Geobiology, Ludwig-Maximilians-Universität München, Munich, Germany Zoology lab, Biology Department, Mathematic and Natural Science Faculty, Sepuluh November Institute of Technology, Surabaya, Indonesia Naturalis Biodiversity Center, Leiden, the Netherlands
Nicole J. de Voogd*
Affiliation:
Naturalis Biodiversity Center, Leiden, the Netherlands
Thomas Swierts
Affiliation:
Naturalis Biodiversity Center, Leiden, the Netherlands
John N.A. Hooper
Affiliation:
Biodiversity Program, Queensland Museum, South Brisbane, Australia Eskitis Institute for Drug Discovery, Griffith University, Nathan, Queensland 4111, Australia
Gert Wörheide
Affiliation:
Department of Earth and Environmental Sciences, Palaeontology & Geobiology, Ludwig-Maximilians-Universität München, Munich, Germany GeoBio-CenterLMU Ludwig-Maximilians-Universität München, Munich, Germany SNSB – Bayerische Staatssammlung für Paläontologie und Geologie, Munich, Germany
Dirk Erpenbeck*
Affiliation:
Department of Earth and Environmental Sciences, Palaeontology & Geobiology, Ludwig-Maximilians-Universität München, Munich, Germany GeoBio-CenterLMU Ludwig-Maximilians-Universität München, Munich, Germany
*
Correspondence should be addressed to:N.J. de Voogd and D. Erpenbeck, Naturalis Biodiversity Center, Leiden, the Netherlands; Department of Earth and Environmental Sciences, Palaeontology & Geobiology, and GeoBio-Center, Ludwig-Maximilians-Universität München, Munich, Germany email: [email protected], [email protected]
Correspondence should be addressed to:N.J. de Voogd and D. Erpenbeck, Naturalis Biodiversity Center, Leiden, the Netherlands; Department of Earth and Environmental Sciences, Palaeontology & Geobiology, and GeoBio-Center, Ludwig-Maximilians-Universität München, Munich, Germany email: [email protected], [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

The Indonesian archipelago is a ‘hotspot’ for invertebrate biodiversity (‘Coral Triangle’). In this area of ‘peak’ biodiversity, the origins of this high species diversity have often been debated. Xestospongia testudinaria is one of the sponge species that dominates coral reef sponge communities in this region. The role of the so-called ‘giant barrel sponge’ for the reef ecosystem has been studied repeatedly, as have its various bioactive compounds. However, the genetic variation of this iconic sponge in the region remains unknown. We investigate over 200 barrel sponge samples from Indonesia, and neighbouring as well as more distant localities (Saudi Arabia, Tanzania, Thailand, Taiwan, Java, Sulawesi and the Great Barrier Reef, Australia) using the mitochondrial cytochrome oxidase subunit 1. We compare our results with those from the studies on the congeneric barrel sponges Xestospongia muta from the Caribbean, and Xestospongia bergquistia from the Indo-Pacific, and observe a high degree of overlapping haplotypes between the three barrel sponge species, likely indicating the presence of ancestral polymorphisms. We discuss the implications of these findings to better interpret the phylogeography of barrel sponge taxa in the Indo-Pacific.

Keywords

Poriferabarrel spongesXestospongiaIndo-Pacifictaxonomymitochondrial DNA
Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 96 , Issue 2: Proceedings of the 9th World Sponge Conference held in Fremantle Australia in 2013: New Frontiers in Sponge Science , March 2016 , pp. 323 - 332
Copyright
Copyright © Marine Biological Association of the United Kingdom 2015 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Akaike, H. (1974) A new look at the statistical model identification. IEEE Transactions on Automatic Control 19, 716–723.CrossRefGoogle Scholar
Becking, L.E., Cleary, D.F.R. and de Voogd, N.J. (2013) Sponge species composition, abundance, and cover in marine lakes and coastal mangroves in Berau, Indonesia. Marine Ecology Progress Series 481, 105–120.CrossRefGoogle Scholar
Bell, J.J. (2007) The use of volunteers for conducting sponge biodiversity assessments and monitoring using a morphological approach on Indo-Pacific coral reefs. Aquatic Conservation: Marine and Freshwater Ecosystems 17, 133–145.CrossRefGoogle Scholar
Bell, J.J. (2008) The functional roles of marine sponges. Estuarine, Coastal and Shelf Science 79, 341–353.CrossRefGoogle Scholar
Bell, J.J., Smith, D., Hannan, D., Haris, A., Jompa, J. and Thomas, L. (2014a) Resilience to disturbance despite limited dispersal and self-recruitment in tropical barrel sponges: implications for conservation and management. PLoS ONE 9, e91635.CrossRefGoogle ScholarPubMed
Bell, J.J., Smith, D., Hannan, D., Haris, A. and Thomas, L. (2014b) Isolation and characterisation of twelve polymorphic microsatellite markers for Xestospongia spp. and their use for confirming species identity. Conservation Genetics Resources 6, 105–106.CrossRefGoogle Scholar
Bellwood, D.R. and Meyer, C.P. (2009) Searching for heat in a marine biodiversity hotspot. Journal of Biogeography 36, 569–576.CrossRefGoogle Scholar
Bentlage, B. and Wörheide, G. (2007) Low genetic structuring among Pericharax heteroraphis (Porifera: Calcarea) populations from the Great Barrier Reef (Australia), revealed by analysis of rDNA and nuclear intron sequences. Coral Reefs 26, 807–816.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, 392–397.CrossRefGoogle Scholar
Boury-Esnault, N. (2006) Systematics and evolution of Demospongiae. Canadian Journal of Zoology 84, 205–224.CrossRefGoogle Scholar
Briggs, J.C. (1999) Coincident biogeographic patterns: Indo-West Pacific ocean. Evolution 53, 326–335.CrossRefGoogle ScholarPubMed
Calcul, L., Longeon, A., Mourabit, A.A., Guyot, M. and Bourguet-Kondracki, M.L. (2003) Novel alkaloids of the aaptamine class from an Indonesian marine sponge of the genus Xestospongia. Tetrahedron 59, 6539–6544.CrossRefGoogle Scholar
Cao, S., Foster, C., Brisson, M., Lazo, J.S. and Kingston, D.G.I. (2005) Halenaquinone and xestoquinone derivatives, inhibitors of Cdc25B phosphatase from a Xestospongia sp. Bioorganic & Medicinal Chemistry 13, 999–1003.CrossRefGoogle ScholarPubMed
Carballo, J., Naranjo, S. and García-Gómez, J. (1996) Use of marine sponges as stress indicators in marine ecosystems at Algeciras bay (southern Iberian Peninsula). Marine Ecology Progress Series 135, 109–122.CrossRefGoogle Scholar
Cárdenas, P., Pérez, T. and Boury-Esnault, N. (2012) Sponge systematics facing new challenges. Advances in Marine Biology 61, 79–209.Google Scholar
Charlesworth, D. (2010) Don't forget the ancestral polymorphisms. Heredity (Edinburgh) 105, 509–510.CrossRefGoogle ScholarPubMed
Cleary, D.F.R. and de Voogd, N.J. (2007) Environmental associations of sponges in the Spermonde Archipelago, Indonesia. Journal of the Marine Biological Association of the United Kingdom 87, 1669–1676.CrossRefGoogle Scholar
Clement, M., Posada, D. and Crandall, K.A. (2000) TCS: a computer program to estimate gene genealogies. Molecular Ecology 9, 1657–1659.CrossRefGoogle ScholarPubMed
Darriba, D., Taboada, G.L., Doallo, R. and Posada, D. (2012) jModelTest 2: more models, new heuristics and parallel computing. Nature Methods 9, 772.CrossRefGoogle ScholarPubMed
de Goeij, J.M., van Oevelen, D., Vermeij, M.J.A., Osinga, R., Middelburg, J.J., de Goeij, A.F.P.M. and Admiraal, W. (2013) Surviving in a marine desert: the sponge loop retains resources within coral reefs. Science 342, 108–110.CrossRefGoogle Scholar
de Queiroz, K. (2007) Species concepts and species delimitation. Systematic Biology 56, 879–886.CrossRefGoogle ScholarPubMed
de Voogd, N.J. and Cleary, D.F.R. (2007) Relating species traits to environmental variables in Indonesian coral reef sponge assemblages. Marine and Freshwater Research 58, 240–249.CrossRefGoogle Scholar
de Voogd, N.J. and Cleary, D.F.R. (2008) An analysis of sponge diversity and distribution at three taxonomic levels in the Thousand islands/Jakarta bay reef complex, West-Java, Indonesia. Marine Ecology 29, 205–215.CrossRefGoogle Scholar
Edgar, R.C. (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research 32, 1792–1797.CrossRefGoogle ScholarPubMed
Erpenbeck, D., Breeuwer, J.A.J., Parra-Velandia, F.J. and van Soest, R.W.M. (2006a) Speculation with spiculation? – Three independent gene fragments and biochemical characters versus morphology in demosponge higher classification. Molecular Phylogenetics and Evolution 38, 293–305.CrossRefGoogle ScholarPubMed
Erpenbeck, D., Breeuwer, J.A.J., van der Velde, H.C. and Soest, R.W.M. (2002) Unravelling host and symbiont phylogenies of halichondrid sponges (Demospongiae, Porifera) using a mitochondrial marker. Marine Biology 141, 377–386.Google Scholar
Erpenbeck, D., Hooper, J.N.A. and Woerheide, G. (2006b) CO1 phylogenies in diploblasts and the ‘Barcoding of Life’ – are we sequencing a suboptimal partition? Molecular Ecology Notes 61, 550–553.CrossRefGoogle Scholar
Erpenbeck, D., Knowlton, A.L., Talbot, S.L., Highsmith, R.C. and van Soest, R.W.M. (2003) A molecular comparison of Alaskan and North East Atlantic Halichondria panicea (Pallas 1766) (Porifera: Demospongiae) populations. Bollettino Museo Istituti Universita Genova 68, 319–325.Google Scholar
Erpenbeck, D. and van Soest, R.W.M. (2007) Status and perspective of sponge chemosystematics. Marine Biotechnology 9, 2–19.CrossRefGoogle ScholarPubMed
Excoffier, L., Laval, G. and Schneider, S. (2005) Arlequin ver. 3.0: an integrated software package for population genetics data analysis. Evolution Bioinformatics Online 1, 47–50.Google Scholar
Fromont, J. (1988) Aspects of the reproductive biology of Xestospongia testudinaria (Great Barrier Reef). In Choat, J.H. (ed.) The 6th Coral Reef Symposium 8–12 August, Volume 2. Australia, pp. 685–691.Google Scholar
Fromont, J. (1991) Descriptions of species of the Petrosida (Porifera: Demospongiae) occurring in the tropical waters of the Great Barrier Reef. Beagle: Records of the Museums and Art Galleries of the Northern Territory 8, 73–95.Google Scholar
Fromont, J. and Bergquist, P.R. (1994) Reproductive biology of three sponge species of the genus Xestospongia (Porifera: Demospongiae: Petrosida) from the Great Barrier Reef. Coral Reefs 13, 119–126.CrossRefGoogle Scholar
Fromont, J., Kerr, S., Kerr, R., Riddle, M. and Murphy, P. (1994) Chemotaxonomic relationships within, and comparisons between, the orders Haplosclerida and Petrosida (Porifera: Demospongiae) using sterol complements. Biochemical Systematics and Ecology 22, 735–753.CrossRefGoogle Scholar
Hoeksema, B. (2007) Delineation of the Indo-Malayan centre of maximum marine biodiversity: the coral triangle. In Renema, W. (ed.) Biogeography, time, and place: distributions, barriers, and islands. Volume 29. Dordrecht: Springer, pp. 117–178.CrossRefGoogle Scholar
Hooper, J.N.A. and van Soest, R.W.M. (2002) Systema Porifera: a guide to the classification of sponges. New York, NY: Kluwer Academic/Plenum Publishers.CrossRefGoogle Scholar
Hooper, J.N.A. and Wiedenmayer, F. (1994) Porifera. In Wells, A. (ed.) Zoological catalogue of Australia. Melbourne: CSIRO, pp. 1–621.Google Scholar
Huang, D., Meier, R., Todd, P. and Chou, L. (2008) Slow mitochondrial COI sequence evolution at the base of the metazoan tree and its implications for DNA barcoding. Journal of Molecular Evolution 66, 167–174.CrossRefGoogle ScholarPubMed
Jones, G.P., Srinivasan, M. and Almany, G.R. (2007) Population connectivity and conservation of marine biodiversity. Oceanography 20, 100–111.CrossRefGoogle Scholar
Kayal, E. and Lavrov, D.V. (2008) The mitochondrial genome of Hydra oligactis (Cnidaria, Hydrozoa) sheds new light on animal mtDNA evolution and cnidarian phylogeny. Gene 410, 177–186.CrossRefGoogle ScholarPubMed
Kelly-Borges, M., Bergquist, P.R. and Bergquist, P.L. (1991) Phylogenetic relationships within the order Hadromerida (Porifera, Demospongiae, Tetractinomorpha) as indicated by ribosomal RNA sequence comparisons. Biochemical Systematics and Ecology 19, 117–125.CrossRefGoogle Scholar
Knowlton, N. and Weigt, L. (1998) New dates and new rates for divergence across the Isthmus of Panama. Proceedings of the Royal Society of London, Biological Sciences 265, 2257–2263.CrossRefGoogle Scholar
Knowlton, N., Weigt, L., Solorzano, L., Mills, D. and Bermingham, E. (1993) Divergence in proteins, mitochondrial DNA, and reproductive compatibility across the Isthmus of Panama. Science 260, 1629–1632.CrossRefGoogle ScholarPubMed
Librado, P. and Rozas, J. (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25, 1451–1452.CrossRefGoogle ScholarPubMed
Lopez-Legentil, S. and Pawlik, J.R. (2009) Genetic structure of the Caribbean giant barrel sponge Xestospongia muta using the I3-M11 partition of COI. Coral Reefs 28, 157–165.CrossRefGoogle Scholar
Maldonado, M. (2006) The ecology of the sponge larva. Canadian Journal of Zoology 84, 175–194.CrossRefGoogle Scholar
Montalvo, N.F. and Hill, R.T. (2011) Sponge-sssociated bacterial symbionts are strictly maintained to two closely-related but geographically distant sponge hosts. Applied and Environmental Microbiology 77, 7207–7216.CrossRefGoogle ScholarPubMed
Newman, D.J. and Cragg, G.M. (2012) Natural products as sources of new drugs over the 30 years from 1981 to 2010. Journal of Natural Products 75, 311–335.CrossRefGoogle ScholarPubMed
Palumbi, S.R., Grabowsky, G., Duda, T.F. Jr, Geyer, L. and Tachino, N. (1997) Speciation and population genetic structure in tropical Pacific sea urchins. Evolution 51, 1506–1517.CrossRefGoogle ScholarPubMed
Powell, A. (2013) The Impacts of Predation and Habitat Degradation on Coral Reef Sponge Assemblages in SE Sulawesi, Indonesia. PhD thesis. School of Biological Sciences, Victoria University of Wellington, Wellington, New Zealand.Google Scholar
Rannala, B. and Yang, Z. (2003) Bayes estimation of species divergence times and ancestral population sizes using DNA sequences from multiple loci. Genetics 164, 1645–1656.CrossRefGoogle ScholarPubMed
Reveillaud, J., van Soest, R.W.M., Derycke, S., Picton, B., Rigaux, A. and Vanreusel, A. (2011) Phylogenetic relationships among NE Atlantic Plocamionida Topsent (1927) (Porifera, Poecilosclerida): under-estimated diversity in reef ecosystems. PLoS ONE 6, e16533.CrossRefGoogle ScholarPubMed
Rice, W.R. (1989) Analyzing tables of statistical tests. Evolution 43, 223–225.CrossRefGoogle ScholarPubMed
Ritson-Williams, R., Becerro, M.A. and Paul, V.J. (2005) Spawning of the giant barrel sponge Xestospongia muta in Belize. Coral Reefs 24, 160.CrossRefGoogle Scholar
Ronquist, F., Teslenko, M., van der Mark, P., Ayres, D.L., Darling, A., Höhna, S., Larget, B., Liu, L., Suchard, M.A. and Huelsenbeck, J.P. (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology 61, 539–542.CrossRefGoogle ScholarPubMed
Rot, C., Goldfarb, I., Ilan, M. and Huchon, D. (2006) Putative cross-kingdom horizontal gene transfer in sponge (Porifera) mitochondria. BMC Evolutionary Biology 6, 71.CrossRefGoogle ScholarPubMed
Ruiz, G.M., Torchin, M.E. and Grant, K. (2007) Using the Panama canal to test predictions about tropical marine invasions. In Lang, M.A., MacIntyre, I.G. and Rützler, K. (ed.) Smithsonian Contributions to the Marine Sciences. Volume 38. Washington, DC: Smithsonian Institution Scholarly Press, pp. 529.Google Scholar
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, 2475–2487.CrossRefGoogle ScholarPubMed
Silvestro, D. and Michalak, I. (2012) RaxmlGUI: a graphical front-end for RAxML. Organisms Diversity and Evolution 12, 335–337.CrossRefGoogle Scholar
Solé-Cava, A.M. and Boury-Esnault, N. (1999) Patterns of intra and interspecific genetic divergence in marine sponges. Memoirs of the Queensland Museum 44, 591–602.Google Scholar
Solé-Cava, A.M. and Wörheide, G. (2007) The perils and merits (or the Good, the Bad and the Ugly) of DNA barcoding of sponges – a controversial discussion. In Custódio, M.R., Lôbo-Hajdu, G., Hajdu, E. and Muricy, G. (ed.) Porifera research: biodiversity, innovation and sustainability. Série Livros 28. Rio de Janeiro: Museu Nacional, pp. 603–612.Google Scholar
Stamatakis, A., Hoover, P. and Rougemont, J. (2008) A rapid bootstrap algorithm for the RAxML web servers. Systematic Biology 57, 758–771.CrossRefGoogle ScholarPubMed
Sutherland, K., Porter, J. and Torres, C. (2004) Disease and immunity in Caribbean and Indo-Pacific zooxanthellate corals. Marine Ecology Progress Series 266, 273–302.CrossRefGoogle Scholar
Swierts, T., Peijnenburg, K.T.C.A., de Leeuw, C., Cleary, D.F.R., Hörnlein, C., Setiawan, E., Wörheide, G., Erpenbeck, D. and de Voogd, N.J. (2013) Lock, stock and two different barrels: comparing the genetic composition of morphotypes of the Indo-Pacific sponge Xestospongia testudinaria. PLoS ONE 8, e74396.CrossRefGoogle ScholarPubMed
Tajima, F. (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123, 585–595.CrossRefGoogle ScholarPubMed
Takahata, N. and Satta, Y. (1997) Evolution of the primate lineage leading to modern humans: phylogenetic and demographic inferences from DNA sequences. Proceedings of the National Academy of Sciences USA 94, 4811–4815.CrossRefGoogle ScholarPubMed
Uriz, M.J. and Turon, X. (2012) Sponge ecology in the molecular era. Advances in Marine Biology 61, 345–410.Google Scholar
van Soest, R.W.M. (1989) The Indonesian sponge fauna: a status report. Netherlands Journal of Sea Research 23, 223–230.CrossRefGoogle Scholar
van Soest, R.W.M., Boury-Esnault, N., Vacelet, J., Dohrmann, M., Erpenbeck, D., de Voogd, N.J., Santodomingo, N., Vanhoorne, B., Kelly, M. and Hooper, J.N.A. (2012) Global diversity of sponges (Porifera). PLoS ONE 7, e35105.CrossRefGoogle ScholarPubMed
Vargas, S., Schuster, A., Sacher, K., Büttner, G., Schätzle, S., Läuchli, B., Hall, K., Hooper, J.N.A., Erpenbeck, D. and Wörheide, G. (2012) Barcoding sponges: an overview based on comprehensive sampling. PLoS ONE 7, e39345.CrossRefGoogle ScholarPubMed
Veron, J.E.N. (1995) Corals in space and time: biogeography & evolution of the Scleractinia. Sydney: University of New South Wales Press, pp. 1–321.Google Scholar
Wapstra, M. and van Soest, R.W.M. (1987) Sexual reproduction, larval morphology and behaviour in Demosponges from the Southwest of the Netherlands. In Vacelet, J. and Boury-Esnault, N. (eds) Taxonomy of Porifera. Berlin: Springer-Verlag, pp. 281–307.CrossRefGoogle Scholar
Wörheide, G., Epp, L. 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, 24.CrossRefGoogle ScholarPubMed
Wörheide, G., Sole-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, 377–385.CrossRefGoogle ScholarPubMed
Wu, C.-I. (1991) Inferences of species phylogeny in relation to segregation of ancient polymorphisms. Genetics 127, 429–435.CrossRefGoogle ScholarPubMed
Xavier, J.R., Rachello-Dolmen, P.G., Parra-Velandia, F.J., Schönberg, C.H.L., Breeuwer, J.A. 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, 13–20.CrossRefGoogle ScholarPubMed
Zhou, R., Zeng, K., Wu, W., Chen, X., Yang, Z., Shi, S. and Wu, C.-I. (2007) Population genetics of speciation in nonmodel organisms: I. Ancestral polymorphism in mangroves. Molecular Biology and Evolution 24, 2746–2754.CrossRefGoogle ScholarPubMed
Supplementary material: File

Setiawan supplementary material

Setiawan supplementary material 1

Download Setiawan supplementary material(File)
File 409.6 KB