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New polymorphic mitochondrial markers for sponge phylogeography

Published online by Cambridge University Press:  01 February 2011

Cintia P.J. Rua ,
Carla Zilberberg  and
Antonio M. Solé-Cava
Cintia P.J. Rua
Affiliation:
Departamento de Genética, Universidade Federal do Rio de Janeiro, Brazil
Carla Zilberberg
Affiliation:
Departamento de Genética, Universidade Federal do Rio de Janeiro, Brazil Departamento de Zoologia, Universidade Federal do Rio de Janeiro, Brazil
Antonio M. Solé-Cava*
Affiliation:
Departamento de Genética, Universidade Federal do Rio de Janeiro, Brazil
*
Correspondence should be addressed to: A.M. Solé-Cava, Laboratório de Biodiversidade Molecular, A2-098, Instituto de Biologia, Universidade Federal do Rio de Janeiro, Ilha do Fundão, 21941-590–Rio de Janeiro, RJ, Brazil email: [email protected]
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Abstract

Phylogeography and population genetic studies in the Porifera have been limited by the lack of available polymorphic DNA markers. In this paper, we tested four new mitochondrial markers in nine demosponge species from a wide taxonomic range: partial sequences of the ATP synthase 6 (ATP6) and the cytochrome oxidase 2 (CO2) genes and two spacers: one located between ATP6 and CO2 and the other between the NADH dehydrogenase subunit 5 (ND5) and the small subunit ribosomal RNA (rns) genes. The new markers presented levels of nucleotide diversity up to 2.4 times higher (π = 0.015 for CO2) than those observed for the most commonly used mitochondrial marker in sponges, the cytochrome oxidase 1 gene (π = 0.006), making them suitable for alpha-level systematics, phylogeography and population genetics studies. 

Keywords

DNA markersPoriferapopulation genetics
Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 91 , Issue 5 , August 2011 , pp. 1015 - 1022
Copyright
Copyright © Marine Biological Association of the United Kingdom 2011

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References

REFERENCES

Addis, J.S. and Peterson, K.J. (2005) Phylogenetic relationships of freshwater sponges (Porifera, Spongillina) inferred from analyses of 18S rDNA, COI mtDNA, and ITS2 rDNA sequences. Zoologica Scripta 34, 549–557.CrossRefGoogle Scholar
Alvarez, B., Krishnan, M. and Gibb, K. (2007) Analysis of intragenomic variation of the rDNA internal transcribed spacers (ITS) in Halichondrida (Porifera: Demospongiae). Journal of the Marine Biological Association of the United Kingdom 87, 1599–1605.CrossRefGoogle Scholar
Avise, J.C. (1986) Mitochondrial DNA and the evolutionary genetics of higher animals. Philosophical Transactions of the Royal Society of London Series B—Biological Sciences 312, 325–342.Google ScholarPubMed
Baker, P., Austin, J.D., Bowen, B.W. and Baker, S.M. (2008) Range-wide population structure and history of the northern quahog (Mercenaria mercenaria) inferred from mitochondrial DNA sequence data. ICES Journal of Marine Science 65, 155–163.CrossRefGoogle Scholar
Bavestrello, G., Benatti, U., Calcinai, B., Cattaneo-Vietti, R., Cerrano, C., Favre, A., Giovine, M., Lanza, S., Pronzato, R. and Sarà, M. (1998) Body polarity and mineral selectivity in the demosponge Chondrosia reniformis. Biological Bulletin. Marine Biological Laboratory, Woods Hole 195, 120–125.CrossRefGoogle Scholar
Beheregaray, L.B. (2008) Twenty years of phylogeography: the state of the field and the challenges for the Southern Hemisphere. Molecular Ecology 17, 3754–3774.CrossRefGoogle ScholarPubMed
Benson, G. (1999) Tandem repeats finder: a program to analyze DNA sequences. Nucleic Acids Research 27, 573–580.CrossRefGoogle Scholar
Blanquer, A., Uriz, M.J. and Caujape-Castells, J. (2009) Small-scale spatial genetic structure in Scopalina lophyropoda, an encrusting sponge with philopatric larval dispersal and frequent fission and fusion events. Marine Ecology Progress Series 380, 95–102.CrossRefGoogle Scholar
Boury-Esnault, N. (2006) Systematics and evolution of Demospongiae. Canadian Journal of Zoology—Revue Canadienne de Zoologie 84, 205–224.CrossRefGoogle Scholar
Boury-Esnault, N., Hajdu, E., Klautau, M., Custódio, M. and Borojevic, R. (1994) The value of cytological criteria in distinguishing sponges at the species level: the example of the genus Polymastia. Canadian Journal of Zoology—Revue Canadienne de Zoologie 72, 795–804.CrossRefGoogle Scholar
Boury-Esnault, N. and Solé-Cava, A.M. (2004) Recent contribution of genetics to the study of sponge systematics and biology. Bolletino dei Musei e degli Istituti Biologici dell Università di Genova 68, 3–18.Google Scholar
Davis, A.R., Ayre, D.J., Billingham, M.R., Styan, C.A. and White, G.A. (1996) The encrusting sponge Halisarca laxus: population genetics and association with the ascidian Pyura spinifera. Marine Biology 126, 27–33.CrossRefGoogle Scholar
DeBiasse, M.B., Richards, V.P. and Shivji, M.S. (2010) Genetic assessment of connectivity in the common reef sponge, Callyspongia vaginalis (Demospongiae: Haplosclerida) reveals high population structure along the Florida reef tract. Coral Reefs 29, 47–55.CrossRefGoogle Scholar
Duran, S., Pascual, M. and Turon, X. (2004a) Low levels of genetic variation in mtDNA sequences over the western Mediterranean and Atlantic range of the sponge Crambe crambe (Poecilosclerida). Marine Biology 144, 31–35.CrossRefGoogle Scholar
Duran, S., Pascual, M., Estoup, A. and Turon, X. (2004b) Strong population structure in the marine sponge Crambe crambe (Poecilosclerida) as revealed by microsatellite markers. Molecular Ecology 13, 511–522.CrossRefGoogle ScholarPubMed
Erpenbeck, D., Breeuwer, J.A.J., van der Velde, H.C. and van 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 Wörheide, G. (2006) CO1 phylogenies in diploblasts and the ‘Barcoding of Life’—are we sequencing a suboptimal partition? Molecular Ecology Notes 6, 550–553.CrossRefGoogle Scholar
Erpenbeck, D., Duran, S., Rutzler, K., Paul, V., Hooper, J.N.A. and Wörheide, G. (2007) Towards a DNA taxonomy of Caribbean demosponges: a gene tree reconstructed from partial mitochondrial CO1 gene sequences supports previous rDNA phylogenies and provides a new perspective on the systematics of Demospongiae. Journal of the Marine Biological Association of the United Kingdom 87, 1563–1570.CrossRefGoogle Scholar
Erpenbeck, D., Voigt, O., Wörheide, G. and Lavrov, D.V. (2009) The mitochondrial genomes of sponges provide evidence for multiple invasions by Repetitive Hairpin-forming Elements (RHE). BMC Genomics 10, 591.CrossRefGoogle ScholarPubMed
Folmer, O., Black, M., Hoeh, W., Lutz, R. and Vrijenhoek, R. (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology 3, 294–299.Google ScholarPubMed
Groeneveld, J.C., Gopal, K., George, R.W. and Matthee, C.A. (2007) Molecular phylogeny of the spiny lobster genus Palinurus (Decapoda: Palinuridae) with hypotheses on speciation in the NE Atlantic/Mediterranean and SW Indian Ocean. Molecular Phylogenetics and Evolution 45, 102–110.CrossRefGoogle ScholarPubMed
Hare, M.P. (2001) Prospects for nuclear gene phylogeography. Trends in Ecology and Evolution 16, 700–706.CrossRefGoogle Scholar
Heim, I., Nickel, M. and Brümmer, F. (2007) Phylogeny of the genus Tethya (Tethyidae: Hadromerida: Porifera): molecular and morphological aspects. Journal of the Marine Biological Association of the United Kingdom 87, 1615–1627.CrossRefGoogle Scholar
Hooper, J.N.A., Capon, R.J., Keenan, C.P. and Parry, D.L. (1991) Morphometric and biochemical differences between sympatric populations of the Clathria ‘spicata’ species complex (Demospongiae: Poecilosclerida: Microcionidae) from Northern Australia. In Reitner, J. and Keupp, H. (eds) Fossil and recent sponges. New York: Springer Verlag, pp. 271–288.CrossRefGoogle Scholar
Hoshino, S., Saito, D.S. and Fujita, T. (2008) Contrasting genetic structure of two Pacific Hymeniacidon species. Hydrobiologia 603, 313–326.CrossRefGoogle Scholar
Imron, , Jeffrey, B., Hale, P., Degnan, B.M. and Degnan, S.M. (2007) Pleistocene isolation and recent gene flow in Haliotis asinina, an Indo-Pacific vetigastropod with limited dispersal capacity. Molecular Ecology 16, 289–304.CrossRefGoogle ScholarPubMed
Itskovich, V.B., Belikov, S.I., Efremova, S.M., Masuda, Y., Krasko, A., Schröder, H.C. and Müller, W.E.G. (2006) Monophyletic origin of freshwater sponges in ancient lakes based on partial structures of COXI gene. Hydrobiologia 568, 155–159.CrossRefGoogle Scholar
Klautau, M., Solé-Cava, A.M. and Borojevic, R. (1994) Biochemical systematics of sibling sympatric species of Clathrina (Porifera, Calcarea). Biochemical Systematics and Ecology 22, 367–375.CrossRefGoogle 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, 1414–1422.CrossRefGoogle ScholarPubMed
Larkin, M.A., Blackshields, G., Brown, N.P., Chenna, R., McGettigan, P.A., McWilliam, H., Valentin, F., Wallace, I.M., Wilm, A., Lopez, R., Thompson, J.D., Gibson, T.J. and Higgins, D.G. (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23, 2947–2948.CrossRefGoogle ScholarPubMed
Lavrov, D.V. and Lang, B.F. (2005) Transfer RNA gene recruitment in mitochondrial DNA. Trends in Genetics 21, 129–133.CrossRefGoogle ScholarPubMed
Lavrov, D.V., Forget, L., Kelly, M. and Lang, B.F. (2005) Mitochondrial genomes of two demosponges provide insights into an early stage of animal evolution. Molecular Biology and Evolution 22, 1231–1239.CrossRefGoogle ScholarPubMed
Lavrov, D.V., Wang, X.J. and Kelly, M. (2008) Reconstructing ordinal relationships in the Demospongiae using mitochondrial genomic data. Molecular Phylogenetics and Evolution 49, 111–124.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
Lôbo-Hajdu, G., Guimarães, A.C.R., Mendes, A.M.S., Lamarão, F.R.M., Vieiralves, T., Mansure, J.J. and Albano, R.M. (2004) Intragenic, intra- and interspecific variation in the rDNA ITS of Porifera revealed by PCR-single-strand conformation polymorphism (PCR-SSCP). Bolletino dei Musei e degli Istituti Biologici dell ‘Università di Genova 68, 413–423.Google Scholar
López-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
Lukic-Bilela, L., Brandt, D., Pojskic, N., Wiens, M., Gamulin, V. and Müller, W.E.G. (2008) Mitochondrial genome of Suberites domuncula: palindromes and inverted repeats are abundant in non-coding regions. Gene 412, 1–11.CrossRefGoogle ScholarPubMed
Muths, D., Jollivet, D., Gentil, F. and Davoult, D. (2009) Large-scale genetic patchiness among NE Atlantic populations of the brittle star Ophiothrix fragilis. Aquatic Biology 5, 117–132.CrossRefGoogle Scholar
Nichols, S.A. (2005) An evaluation of support for order-level monophyly and interrelationships within the class Demospongiae using partial data from the large subunit rDNA and cytochrome oxidase subunit I. Molecular Phylogenetics and Evolution 34, 81–96.CrossRefGoogle ScholarPubMed
Noyer, C., Agell, G., Pascual, M. and Becerro, M.A. (2009) Isolation and characterization of microsatellite loci from the endangered Mediterranean sponge Spongia agaricina (Demospongiae: Dictyoceratida). Conservation Genetics 10, 1895–1898.CrossRefGoogle Scholar
Owen, C.L., Messing, C.G., Rouse, G.W. and Shivji, M.S. (2009) Using a combined approach to explain the morphological and ecological diversity in Phanogenia gracilis Hartlaub, 1893 (Echinodermata: Crinoidea) sensu lato: two species or intraspecific variation? Marine Biology 156, 1517–1529.CrossRefGoogle Scholar
Palero, F., Abello, P., Macpherson, E., Gristina, M. and Pascual, M. (2008) Phylogeography of the European spiny lobster (Palinurus elephas): influence of current oceanographical features and historical processes. Molecular Phylogenetics and Evolution 48, 708–717.CrossRefGoogle ScholarPubMed
Polson, M.P., Hewson, W.E., Eernisse, D.J., Baker, P.K. and Zacherl, D.C. (2009) You say Conchaphila, I say Lurida: molecular evidence for restricting the olympia oyster (Ostrea lurida Carpenter 1864) to temperate western North America. Journal of Shellfish Research 28, 11–21.CrossRefGoogle 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
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 Thorpe, J.P. (1989) Biochemical correlates of genetic variation in marine lower invertebrates. Biochemical Genetics 27, 303–312.CrossRefGoogle ScholarPubMed
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. (eds) Porifera research—biodiversity, innovation and sustainability. Rio de Janeiro: Museu Nacional, pp. 603–612.Google Scholar
Stone, A.R. (1970) Growth and reproduction of Hymeniacidon perleve (Montagu) (Porifera) in Langstone, Hampshire. Journal of Zoology 161, 443–459.CrossRefGoogle Scholar
Tamura, K., Dudley, J., Nei, M. and Kumar, S. (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Molecular Biology and Evolution 24, 1596–1599.CrossRefGoogle ScholarPubMed
Tsurumi, M. and Reiswig, H.M. (1997) Sexual versus asexual reproduction in an oviparous rope-form sponge, Aplysina cauliformis (Porifera; Verongida). Invertebrate Reproduction and Development 32, 1–9.CrossRefGoogle Scholar
van Oppen, M.J.H., Wörheide, G. and Takabayashi, M. (2002) Nuclear markers in evolutionary and population genetic studies of scleractinian corals and sponges. In Moosa, M.K., Soemodihardjo, S., Soegiarto, A., Romimohtarto, K., Nontji, A., Soekarno, and Suharsono, (eds) Proceedings of the Ninth International Coral Reef Symposium, Bali, 23–27 October 2000. Ministry of Environment, Indonesian Institute of Sciences and the International Society for Reef Studies, pp. 131–138.Google Scholar
Wang, X.J. and Lavrov, D.V. (2008) Seventeen new complete mtDNA sequences reveal extensive mitochondrial genome evolution within the Demospongiae. PLoS One 3, e2723.CrossRefGoogle ScholarPubMed
Watkins, R.F. and Beckenbach, A.T. (1999) Partial sequence of a sponge mitochondrial genome reveals sequence similarity to cnidaria in cytochrome oxidase subunit II and the large ribosomal RNA subunit. Journal of Molecular Evolution 48, 542–554.CrossRefGoogle ScholarPubMed
Wiklund, H., Glover, A.G., Johannessen, P.J. and Dahlgren, T.G. (2009) Cryptic speciation at organic-rich marine habitats: a new bacteriovore annelid from whale-fall and fish farms in the North-East Atlantic. Zoological Journal of the Linnean Society 155, 774–785.CrossRefGoogle Scholar
Wörheide, G. (2006) Low variation in partial cytochrome oxidase subunit I (COI) mitochondrial sequences in the coralline demosponge Astrosclera willeyana across the Indo-Pacific. Marine Biology 148, 907–912.CrossRefGoogle Scholar
Wörheide, G., Hooper, J.N.A. and Degnan, B.M. (2002) Phylogeography of western Pacific Leucetta ‘chagosensis’ (Porifera: Calcarea) from ribosomal DNA sequences: implications for population history and conservation of the Great Barrier Reef World Heritage Area (Australia). Molecular Ecology 11, 1753–1768.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, 816–830.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, 377–385.CrossRefGoogle ScholarPubMed
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, 24.CrossRefGoogle ScholarPubMed
Wulff, J.L. (1991) Asexual fragmentation, genotype success, and population dynamics of erect branching sponges. Journal of Experimental Marine Biology and Ecology 149, 227–247.CrossRefGoogle Scholar
Wulff, J.L. (2006) Sponge systematics by starfish: predators distinguish cryptic sympatric species of Caribbean fire sponges, Tedania ignis and Tedania klausi n. sp (Demospongiae, Poecilosclerida). Biological Bulletin. Marine Biological Laboratory, Woods Hole 211, 83–94.CrossRefGoogle Scholar
Xavier, J.R., Rachello-Dolmen, P.G., Parra-Velandia, F., Schönberg, C.H.L., Breeuwer, 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, 13–20.CrossRefGoogle ScholarPubMed