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Marine Biology

, Volume 144, Issue 1, pp 31–35 | Cite as

Low levels of genetic variation in mtDNA sequences over the western Mediterranean and Atlantic range of the sponge Crambe crambe (Poecilosclerida)

  • S. Duran
  • M. Pascual
  • X. Turon
Research Article

Abstract

Crambe crambe is a common encrusting sponge found in the Mediterranean and Atlantic littoral. An analysis of a partial sequence (535 bp) of the mitochondrial DNA (mtDNA) gene cytochrome oxidase subunit I (COI) was conducted in an attempt to determine population structure in this species. This is the first study of population genetics using this kind of marker in the phylum. Samples (N=86) were taken in eight populations separated by distances from 20 to 3,000 km, spanning from the western Mediterranean to the Atlantic. Low variability of this gene was found, as only two haplotypes were identified, along with low nucleotide diversity (π=0.0006). However, the different frequencies found among populations revealed genetic structure and low gene flow between close populations, as expected from the dispersal biology of the species. The low variability found in sponges is in agreement with reports on cnidarians and points to a high conservation of mtDNA in diploblastic phyla.

Keywords

Sponge Ballast Water Messinian Sponge Species High Genetic Similarity 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgements

We are grateful to M. Zabala, C. Palacin, S. López, P. Wirtz and E. Cebrian for providing us with Crambe crambe specimens from Corsica, Cabo de Gata, Banyuls-sur-Mer, Madeira and Gran Canaria, respectively. J. Rozas made useful comments on the manuscript. This research was supported by a predoctoral fellowship from the Government of Catalonia to S.D. Research was funded by projects BOS2000-0295 and REN2001-2312 of the Spanish Ministry of Science and Technology. We declare that all the experiments done comply with current Spanish laws.

References

  1. Avise JC (2000) Phylogeography: the history and formation of species. Harvard University Press, CambridgeGoogle Scholar
  2. Avise JC, Arnold J, Ball RM, Bermingham E, Lamb T, Neigel JE, Reeb CA, Saunders NC (1987) Intraspecific phylogeography: the mitochondrial DNA bridge between population genetics and systematics. Annu Rev Ecol Syst 18:489–522CrossRefGoogle Scholar
  3. Becerro MA (1994) Chemically mediated bioactivity of the encrusting sponge Crambe crambe and its ecological implications. Department of Animal Biology, Barcelona, SpainGoogle Scholar
  4. Becerro MA, Uriz MJ, Turon X (1997) Chemically-mediated interactions in benthic organisms: the chemical ecology of Crambe crambe (Porifera, Poecilosclerida). Hydrobiologia 356:77–89CrossRefGoogle Scholar
  5. Benzie JAH, Sandusky C, Wilkinson CR (1994) Genetic structure of dictyoceratid sponge populations on the western Coral Sea reefs. Mar Biol 119:335–345Google Scholar
  6. Borchiellini C, Chombard C, Lafay B, Boury-Esnault N (2000) Molecular systematics of sponges (Porifera). Hydrobiologia 420:15–27Google Scholar
  7. Borojevic R (1970) Différentiation cellulaire dans l'embriogénèse et la morphogénèse chez les spongiaires. In: Fry WG (ed) The biology of the Porifera. Academic, London, pp 467–490Google Scholar
  8. Bossart JL, Prowell DP (1998) Genetic estimates of population structure and gene flow: limitations, lessons and new directions. Trends Ecol Evol 13:202–206CrossRefGoogle Scholar
  9. Boury-Esnault N (1971) Spongiaires de la zone rocheuse littorale de Banyuls-sur-Mer. I. Ecologie et répartition. Vie Milieu 22:159–192Google Scholar
  10. Boury-Esnault N, Solé-Cava AM, Thorpe JP (1992) Genetic and cytological divergence between colour morphs of the Mediterranean sponge Oscarella lobularis Schmidt (Porifera, Demospongiae, Oscarellidae). J Nat Hist 26:271–284Google Scholar
  11. Boury-Esnault N, Klautau M, Bézac C, Wulff J, Solé-Cava AM (1999) Comparative study of putative conspecific sponge populations from both sides of the Isthmus of Panama. J Mar Biol Assoc UK 79:39–50CrossRefGoogle Scholar
  12. Burton M (1936) IX. Sponges. The fishery ground: near Alexandria. Ministry of Commerce and Industry, Alexandria, EgyptGoogle Scholar
  13. Carlton JT, Geller JB (1993) Ecological roulette: the global transport of nonindigenous marine organisms. Science 261:78–82Google Scholar
  14. Duran S, Pascual M, Estoup A, Turon X (2002) Polymorphic microsatellite loci in the sponge Crambe crambe (Porifera: Poecilosclerida) and their variation in two distant populations. Mol Ecol Notes 2:478–480CrossRefGoogle Scholar
  15. Erpenbeck D, Breeuwer JAJ, van der Velde HC, van Soest RWM (2002) Unravelling host and symbiont phylogenies of halichondrid sponges (Demospongiae, Porifera) using a mitochondrial marker. Mar Biol 141:377–386CrossRefGoogle Scholar
  16. Folmer O, Black M, Hoeh W, Lutz R, Vrijenhoek R (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol Mar Biol Biotechnol 3:294–299PubMedGoogle Scholar
  17. France SC, Hoover LL (2002) DNA sequences of the mitochondrial COI gene have low levels of divergence among deep-sea octocorals (Cnidaria: Anthozoa). Hydrobiologia 471:149–155CrossRefGoogle Scholar
  18. Galera J, Turon X, Uriz MJ, Becerro MA (2000) Microstructure variation in sponges sharing growth form: the encrusting demosponges Dysidea avara and Crambe crambe. Acta Zool 81:93–107CrossRefGoogle Scholar
  19. Gopurenko D, Hughes JM, Keenan CP (1999) Mitochondrial DNA evidence for rapid colonisation of the Indo–West Pacific by the mudcrab Scylla serrata. Mar Biol 134:227–233CrossRefGoogle Scholar
  20. King TL, Eackles MS, Gjetvaj B, Hoeh WR (1999) Intraspecific phylogeography of Lasmigona subviridis (Bivalvia: Unionidae): conservation implications of range discontinuity. Mol Ecol 8:65–78Google Scholar
  21. Klautau M, Solé-Cava AM, Borojevic R (1994) Biochemical systematics of sibling sympatric species of Clathrina (Porifera: Calcarea). Biochem Syst Ecol 22:367–375Google Scholar
  22. Klautau M, Russo CAM, Lazoski C, Boury-Esnault N, Thorpe JP, Solé-Cava AM (1999) Does cosmopolitanism result from overconservative systematics? A case study using the marine sponge Chondrilla nucula. Evolution 53:1414–1422Google Scholar
  23. Lazoski C, Solé-Cava AM, Boury-Esnault N, Klautau M, Russo CAM (2001) Cryptic speciation in a high gene flow scenario in the oviparous marine sponge Chondrosia reniformis. Mar Biol 139:421–429CrossRefGoogle Scholar
  24. Lopez JV, Peterson CL, Willoughby R, Wright AE, Enright E, Zoladz S, Pomponi SA (2002) Characterization of genetic markers for in vitro cell line identification of the marine sponge, Axinella corrugata. J Hered 93:27–36CrossRefPubMedGoogle Scholar
  25. Maldonado A (1985) Evolution of the Mediterranean basins and a detailed reconstruction of the Cenozoic paleoceanography. In: Margalef R (ed) Western Mediterranean. Pergamon, Oxford, pp 17–60Google Scholar
  26. Maldonado M, Uriz MJ (1999) Sexual propagation by sponge fragments. Nature 398:476Google Scholar
  27. McFadden CS, Tullis I, Hutchison MB, Winner K (2000) Rates of evolution of cnidarian mitochondrial genes. Am Zool 40:11–24Google Scholar
  28. Muricy G, Solé-Cava AM, Thorpe JP, Boury-Esnault N (1996) Genetic evidence for extensive cryptic speciation in the subtidal sponge Plakina trilopha (Porifera, Demospongiae, Homoscleromorpha) from the western Mediterranean. Mar Ecol Prog Ser 138:181–187Google Scholar
  29. Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New YorkGoogle Scholar
  30. Palumbi SR (1995) Using genetics as an indirect estimator of larval dispersal. In: McEdward L (ed) Ecology of marine invertebrate larvae. CRC Press, Boca Raton, Fla., pp 369–387Google Scholar
  31. Palumbi SR, Cipriano F, Hare MP (2001) Predicting nuclear gene coalescence from mitochondrial data: the three-times rule. Evolution 55:859–868PubMedGoogle Scholar
  32. Pulitzer-Finali G (1983) A collection of Mediterranean demosponges (Porifera) with, in appendix, a list of the Demospongiae hitherto recorded from the Mediterranean Sea. Ann Mus Civ Stor Nat Genova 84:445–621Google Scholar
  33. Raymond M, Rousset F (1995a) An exact test for population differentiation. Evolution 49:1280–1283Google Scholar
  34. Raymond M, Rousset F (1995b) GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. J Hered 86:248–249Google Scholar
  35. Rousset F (1997) Genetic differentiation and estimation of gene flow from F-statistics under isolation by distance. Genetics 145:1219–1228Google Scholar
  36. Rozas J, Rozas R (1999) DNAsp version 3.0: an integrated program for molecular population genetics and molecular evolution analyses. Bioinformatics 15:174–175CrossRefPubMedGoogle Scholar
  37. Sarà M, Vacelet J (1973) Ecologie des Démosponges. In: Grassé PP (ed) Spongiaires. Masson, Paris, pp 462–576Google Scholar
  38. Saritas MU (1972) A preliminary study of the siliceous sponge (Porifera) fauna of Engeceli Limani in the Gulf of Izmir (Aegean Sea). Sci Rep Fac Sci Ege Univ 143:17–18Google Scholar
  39. Schmidt O (1862) Die Spongien des adriatischen Meeres. Verlag Wilhelm Engelmann, LeipzigGoogle Scholar
  40. Schneider S, Roessli D, Excoffier L (2000) Arlequin ver. 2.000: a software for population genetics data analysis. Genetics and Biometry Laboratory, University of Geneva, GenevaGoogle Scholar
  41. Schröder HC, Efremova SM, Itskovich VB, Belikov S, Masuda Y, Krasko A, Müller IM, Müller WEG (2003) Molecular phylogeny of the freshwater sponges in Lake Baikal. J Zool Syst Evol Res 41:80–86Google Scholar
  42. Solé-Cava AM, Boury-Esnault N (1999) Patterns of intra- and interspecific genetic divergence in marine sponges. Mem Queensl Mus 44:591–601Google Scholar
  43. Solé-Cava AM, Thorpe JP (1986) Genetic differentiation between morphotypes of the marine sponge Suberites ficus (Demospongiae: Hadromerida). Mar Biol 93:247–253Google Scholar
  44. Tarjuelo I, Posada D, Crandall K, Pascual M, Turon X (2001) Cryptic species of Clavelina (Ascidiacea) in two different habitats: harbours and rocky littoral zones in the northwestern Mediterranean. Mar Biol 139:455–462CrossRefGoogle Scholar
  45. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The Clustal X Windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 24:4876–4882CrossRefGoogle Scholar
  46. Turon X, Tarjuelo I, Uriz MJ (1998) Growth dynamics and mortality of the encrusting sponge Crambe crambe (Poecilosclerida) in contrasting habitats: correlation with population structure and investment in defence. Funct Ecol 12:631–639CrossRefGoogle Scholar
  47. Uriz MJ, Rosell D, Martín D (1992) The sponge population of the Cabrera Archipelago (Balearic Islands): characteristics, distribution and abundance of the most representative species. Mar Ecol 13:101–117Google Scholar
  48. Uriz MJ, Maldonado M, Turon X, Martí R (1998) How do reproductive output, larval behaviour, and recruitment contribute to adult spatial patterns in Mediterranean encrusting sponges? Mar Ecol Prog Ser 167:137–148Google Scholar
  49. Vacelet J (1999) Planktonic armoured propagules of the excavating sponge Alectona (Porifera: Demospongiae) are larvae: evidence from Alectona wallichii and A. mesatlantica sp. nov. Mem Queensl Mus 44:627–642Google Scholar
  50. Watkins RF, Beckenbach AT (1999) Partial sequence of a sponge mitochondrial genome reveals sequence similarity to Cnidaria in cytochrome oxidase subunit II and the large ribosomal RNA subunit. J Mol Evol 48:542–554PubMedGoogle Scholar
  51. Wilke T, Davis GM (2000) Intraspecific mitochondrial sequence diversity in Hydrobia ulvae and Hydrobia ventrosa (Hydrobiidae: Rissooidea: Gastropoda): do their different life histories affect biogeographic patterns and gene flow? Biol J Linn Soc 70:89–105Google Scholar
  52. Wörheide G, Hooper JN, Degnan BM (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). Mol Ecol 11:1753–1768CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag 2003

Authors and Affiliations

  1. 1.Department of Animal Biology (Invertebrates)University of BarcelonaBarcelonaSpain
  2. 2.Department of GeneticsUniversity of BarcelonaBarcelonaSpain

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