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Marine Biology

, Volume 148, Issue 5, pp 1051–1060 | Cite as

Population genetic structure of the prosobranch Nassarius reticulatus (L.) in a ria seascape (NW Iberian Peninsula) as revealed by RAPD analysis

  • Rodolfo Barreiro
  • Lucia Couceiro
  • María Quintela
  • José Miguel Ruiz
Research Article

Abstract

Randomly amplified polymorphic DNA (RAPD) banding patterns were compared between samples of the netted dogwhelk Nassarius reticulatus from 11 locations along the NW Iberian Peninsula coast. To detect if rias (estuaries formed by drowned river valleys) might promote genetic differentiation, five sampling sites were located within a ria (ria of Muros) and the remaining six were scattered along open-coast areas at increasing distances from the ria mouth. Population differentiation statistics (Φ-values) were estimated using a hierarchical analysis of molecular variance (AMOVA) with samples sorted into two groups: open-coast and ria populations. Despite a high potential to disperse, AMOVA demonstrated a modest, statistically significant genetic heterogeneity among N. reticulatus populations. Most of the genetic structure resided in differences among open-coast populations; ria populations were genetically homogeneous. No obvious geographical pattern was detected for the pairwise genetic distances (non-metric multidimensional scaling; UPGMA tree; Mantel test). Unlike previous studies with other species at a variety of estuarine systems other than rias, there was no evidence that the ria of Muros may enhance the genetic divergence of N. reticulatus populations. This discrepancy is discussed in relation to the biological features of the species (high dispersal potential and a preference for mid-low estuarine habitat) and the strong hydrographic connectivity between ria and neighbouring off-shore waters.

Keywords

Genetic Differentiation Restrict Gene Flow Larval Retention North Atlantic Central Water Nassarius Reticulatus 
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

Funding for this work was provided by the Ministerio de Ciencia y Tecnología grant REN2001-0899 (partially co-funded by FEDER, Fondo Europeo de Desarrollo Regional) and the Xunta de Galicia grant PGIDT01MAM10301PR. We acknowledge a postgraduate fellowship to L.C. from the Ministerio de Educación y Ciencia (AP2002-0928).

References

  1. Alvarez-Salgado XA, Gago J, Miguez BM, Gilcoto M, Perez FF (2000) Surface waters of the NW Iberian margin: upwelling on the shelf versus outwelling of upwelled waters from the Rias Baixas. Estuar Coast Shelf Sci 51:821–837CrossRefGoogle Scholar
  2. Alvarez-Salgado XA, Figueiras FG, Perez FF, Groom S, Nogueira E, Borges AV, Chou L, Castro CG, Moncoiffe G, Rios AF (2003) The Portugal coastal counter current off NW Spain: new insights on its biogeochemical variability. Prog Oceanogr 56:281–321CrossRefGoogle Scholar
  3. Avise JC (1992) Molecular population structure and the biogeographic history of a regional fauna: a case history with lessons for conservation biology. Oikos 63:62–76CrossRefGoogle Scholar
  4. Barnett PRO, Hardy BLA, Watson J (1980) Substratum selection and egg-capsule deposition in Nassarius reticulatus (L.). J Exp Mar Biol Ecol 45:95–103CrossRefGoogle Scholar
  5. Barreiro R, González R, Quintela M, Ruiz JM (2001) Imposex, organotin bioaccumulation and sterililty of female Nassarius reticulatus in polluted areas of NW Spain. Mar Ecol Prog Ser 218:203–212CrossRefGoogle Scholar
  6. Barroso CM, Moreira MH (1998) Reproductive cycle of Nassarius reticulatus in the Ria de Aveiro, Portugal: implications for imposex studies. J Mar Biol Assoc UK 78:1233–1246CrossRefGoogle Scholar
  7. Bilton DT, Paula J, Bishop JDD (2002) Dispersal, genetic differentiation and speciation in estuarine organisms. Estuar Coast Shelf Sci 55:937–952CrossRefGoogle Scholar
  8. Bohonak AJ (1999) Dispersal, gene flow, and population structure. Q Rev Biol 74:21–45CrossRefGoogle Scholar
  9. Bohonak AJ (2002) IBD (Isolation by distance): a program for analysis of isolation by distance. J Hered 93:153–154CrossRefGoogle Scholar
  10. 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
  11. Botsford LW, Micheli F, Hastings A (2003) Principles for the design of marine reserves. Ecol Appl 13:S25–S31CrossRefGoogle Scholar
  12. Bryan GW, Burt GR, Gibbs PE, Pascoe PL (1993) Nassarius reticulatus (Nassariidae: Gastropoda) as an indicator of tributyltin pollution before and after TBT restrictions. J Mar Biol Assoc UK 73:913–929CrossRefGoogle Scholar
  13. De Wolf H, Blust R, Backeljau T (2004) The use of RAPD in ecotoxicology. Mut Res/Rev Mut Res 566:249–262CrossRefGoogle Scholar
  14. Edmands S, Moberg PE, Burton RS (1996) Allozyme and mitochondrial DNA evidence of population subdivision in the purple sea urchin Strongylocentrotus purpuratus. Mar Biol 126:443–450CrossRefGoogle Scholar
  15. Evans G, Prego R (2003) Rias, estuaries and incised valleys: is a ria an estuary? Mar Geol 196:171–175CrossRefGoogle Scholar
  16. Excoffier L, Smouse PE, Quattro JM (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 21:479–491Google Scholar
  17. Felsenstein J (2004) PHYLIP (Phylogeny Inference Package) v. 3.6. Distributed by the author at http://evolution.gs.washington.edu/phylip.html, Department of Genome Sciences, University of Washington, SeattleGoogle Scholar
  18. Flowers JM, Burton RS, Schroeter SC (2002) The recruitment sweepstakes has many winners: genetic evidence from the sea urchin Strongylocentrotus purpuratus. Evolution 56:1445–1453CrossRefGoogle Scholar
  19. Fretter V, Shale D (1973) Seasonal-changes in population density and vertical distribution of prosobranch veligers in offshore plankton at Plymouth. J Mar Biol Assoc UK 53:471–492CrossRefGoogle Scholar
  20. Fretter V, Graham A (1994) British prosobranch molluscs: their functional anatomy and ecology, 2nd edn. Ray Society, LondonGoogle Scholar
  21. Grosberg R, Cunningham CW (2001) Genetic structure in the sea: from populations to communities. In: Bertness MD, Gaines S, Hay ME (eds) Marine community ecology. Sinauer Associates, Sunderland, pp 61–84Google Scholar
  22. Grosberg RK, Levitan DR, Cameron BB (1996) Characterization of genetic structure and genealogies using RAPD-PCR markers: a random primer for the novice and nervous. In: Ferraris JD, Palumbi SR (eds) Molecular zoology: advances, strategies and protocols. Wiley-Liss, New York, pp 67–100Google Scholar
  23. Hadrys H, Balick M, Schierwater B (1992) Applications of random amplified polymorphic DNA (RAPD) in molecular ecology. Mol Ecol 1:55–63CrossRefGoogle Scholar
  24. Haig SM, Rhymer JM, Heckel DG (1994) Population differentiation in randomly amplified polymorphic DNA of red-cockaded woodpeckers Picoides borealis. Mol Ecol 3:581–595CrossRefGoogle Scholar
  25. Hedgecock D (1994) Does variance in reproductive success limit effective population size of marine organisms? In: Beaumont AR (ed) Genetics and evolution of aquatic organisms. Chapman & Hall, London, pp 122–134Google Scholar
  26. Heipel DA, Bishop JDD, Brand AR, Thorpe JP (1998) Population genetic differentiation of the great scallop Pecten maximus in western Britain investigated by randomly amplified polymorphic DNA. Mar Ecol Prog Ser 162:163–171CrossRefGoogle Scholar
  27. Hellberg ME, Burton RS, Neigel JE, Palumbi SR (2002) Genetic assessment of connectivity among marine populations. Bull Mar Sci 70:273–290Google Scholar
  28. Huang BX, Peakall R, Hanna PJ (2000) Analysis of genetic structure of blacklip abalone (Haliotis rubra) populations using RAPD, minisatellite and microsatellite markers. Mar Biol 136:207–216CrossRefGoogle Scholar
  29. Huff DR, Peakall R, Smouse PE (1993) RAPD variation within and among natural populations of outcrossing buffalograss [Buchloe dactyloides (Nutt.) Engelm.]. Theor Appl Genet 86:927–934CrossRefGoogle Scholar
  30. Johnson MS, Black R (1982) Chaotic genetic patchiness in an inter-tidal limpet, Siphonaria sp. Mar Biol 70:157–164CrossRefGoogle Scholar
  31. Johnson MS, Black R (1991) Genetic subdivision of the intertidal snail Bembicium vittatum (Gastropoda: Littorinidae) varies with habitat in the Houtman Abrolhos Islands, Western Australia. Heredity 67:205–213CrossRefGoogle Scholar
  32. Johnson MS, Wernham J (1999) Temporal variation of recruits as a basis of ephemeral genetic heterogeneity in the western rock lobster Panulirus cygnus. Mar Biol 135:133–139CrossRefGoogle Scholar
  33. Jones GP, Milicich MJ, Emslie MJ, Lunow C (1999) Self-recruitment in a coral reef fish population. Nature 402:802–804CrossRefGoogle Scholar
  34. Lambeck RHD (1984) Dynamics, migration and growth of Nassarius reticulatus (Mollusca: Prosobranchia) colonizing saline lake Grevelingen (SW Netherlands). Neth J Sea Res 18:395–417CrossRefGoogle Scholar
  35. Lambert WJ, Todd CD, Thorpe JP (2003) Genetic population structure of two intertidal nudibranch molluscs with contrasting larval types: temporal variation and transplant experiments. Mar Biol 142:461–471CrossRefGoogle Scholar
  36. Lebour MV (1931) The larval stages of Nassarius reticulatus and Nassarius incrassatus. J Mar Biol Assoc UK 17:797–818CrossRefGoogle Scholar
  37. Lewontin RC (1972) The apportionment of human diversity. Evol Biol 6:381–394Google Scholar
  38. Li G, Hedgecock D (1998) Genetic heterogeneity, detected by PCR-SSCP, among samples of larval Pacific oysters (Crassostrea gigas) supports the hypothesis of large variance in reproductive success. Can J Fish Aquat Sci 55:1025–1033CrossRefGoogle Scholar
  39. Lynch M, Milligan BG (1994) Analysis of population genetic structure with RAPD markers. Mol Ecol 3:91–99CrossRefGoogle Scholar
  40. Mantel N (1967) The detection of disease of clustering and a generalized regression approach. Cancer Res 27:209–220Google Scholar
  41. Miller MP (1997) Tools for population genetic analyses (TFPGA) 1.3: a Windows program for the analysis of allozyme and molecular population genetic data. (Computer software distributed by author)Google Scholar
  42. Moberg PE, Burton RS (2000) Genetic heterogeneity among adult and recruit red sea urchins, Strongylocentrotus franciscanus. Mar Biol 136:773–784CrossRefGoogle Scholar
  43. Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New YorkGoogle Scholar
  44. Palumbi SR (1994) Genetic divergence, reproductive isolation, and marine speciation. Annu Rev Ecol Syst 25:547–572CrossRefGoogle Scholar
  45. Palumbi SR (2003) Population genetics, demographic connectivity, and the design of marine reserves. Ecol Appl 13:S146–S158CrossRefGoogle Scholar
  46. Palumbi SR, Gaines SD, Leslie H, Warner RR (2003) New wave: high-tech tools to help marine reserve research. Front Ecol Evol 1:73–79CrossRefGoogle Scholar
  47. Parsons KE (1996) The genetic effects of larval dispersal depend on spatial scale and habitat characteristics. Mar Biol 126:403–414CrossRefGoogle Scholar
  48. Perrin C, Wing SR, Roy MS (2004) Effects of hydrographic barriers on population genetic structure of the sea star Coscinasterias muricata (Echinodermata, Asteroidea) in the New Zealand fiords. Mol Ecol 13:2183–2195CrossRefGoogle Scholar
  49. Raymond M, Rousset F (1995) An exact test for population differentiation. Evolution 449:1280–1283CrossRefGoogle Scholar
  50. 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, Geneva, SwitzerlandGoogle Scholar
  51. Shanks AL, Grantham BA, Carr MH (2003) Propagule dispersal distance and the size and spacing of marine reserves. Ecol Appl 13:S159–S169CrossRefGoogle Scholar
  52. Skroch P, Nienhuis J (1995) Impact of scoring error and reproducibility of RAPD data on RAPD based estimates of genetic distance. Theor Appl Genet 91:1086–1091PubMedGoogle Scholar
  53. Sokal RR, Rohlf FJ (1995) Biometry: the principles and practice of statistics in biological research, 3rd edn. W.H. Freeman and Co., New YorkGoogle Scholar
  54. Stroben E, Oehlmann J, Fioroni P (1992) The morphological expression of imposex in Hinia reticulata (Gastropoda: Buccinidae): a potential indicator of tributyltin pollution. Mar Biol 113:625–636CrossRefGoogle Scholar
  55. Swearer SE, Caselle JE, Lea DW, Warner RR (1999) Larval retention and recruitment in an island population of a coral-reef fish. Nature 402:799–802CrossRefGoogle Scholar
  56. Tallmark B (1980) Population dynamics of Nassarius reticulatus (Gastropoda: Prosobranchia) in Gullmar Fjord, Sweden. Mar Ecol Prog Ser 3:51–62CrossRefGoogle Scholar
  57. Taylor MS, Hellberg ME (2003) Genetic evidence for local retention of pelagic larvae in a Caribbean reef fish. Science 299:107–109CrossRefGoogle Scholar
  58. Uthicke S, Benzie JAH (2001) Restricted gene flow between Holothuria scabra (Echinodermata : Holothuroidea) populations along the north-east coast of Australia and the Solomon Islands. Mar Ecol Prog Ser 216:109–117CrossRefGoogle Scholar
  59. Waples RS (1998) Separating the wheat from the chaff: Patterns of genetic differentiation in high gene flow species. J Hered 89:438–450CrossRefGoogle Scholar
  60. Watts RJ, Johnson MS (2004) Estuaries, lagoons and enclosed embayments: habitats that enhance population subdivision of inshore fishes. Mar Freshw Res 55:641–651CrossRefGoogle Scholar
  61. Watts RJ, Johnson MS, Black R (1990) Effects of recruitment on genetics patchiness in the urchin Echinometra mathaei in Western Australia. Mar Biol 105:145–151CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2005

Authors and Affiliations

  • Rodolfo Barreiro
    • 1
  • Lucia Couceiro
    • 1
  • María Quintela
    • 1
  • José Miguel Ruiz
    • 1
  1. 1.Área de Ecología, Facultad de CienciasUniversidade da CoruñaA CoruñaSpain

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