Marine Biology

, Volume 154, Issue 2, pp 277–286 | Cite as

Regional patterns of microsatellite variation in Mytilus galloprovincialis from the Iberian Peninsula

  • Angel P. Diz
  • Pablo PresaEmail author
Research Article


The Almería-Oran Oceanographic Front (AOOF) has been proposed as an effective marine barrier to gene flow between the NE Atlantic Ocean and the Mediterranean Sea for several species. Previous studies using allozymes and mitochondrial DNA have reported a scenario of secondary intergradation between populations of Mytilus galloprovincialis from those basins, with the allelic frequencies of some loci showing abrupt clinal patterns across the AOOF. In this study, we aimed at testing the congruence between six neutral polymorphic microsatellites versus previous data on allozymes and mtDNA-RFLPs, at depicting the population structure of this species in the Iberian Peninsula. Microsatellite genotyping was scored on 17 samples of mussels collected in the Iberian coast, including some areas not sampled before. Microsatellites exhibited larger intrabasin diversity (FSC = 1.72%, \( \overline{H} _{{\text{E}}} \pm {\text{SD}} = 0.772 \pm 0.154 \)), similar interbasin differentiation (FCT = 2.81%) and fewer allelic clines than allozymes or mtDNA haplotypes. These results fully support the scenario of secondary intergradation with some ongoing gene flow between basins, as proposed in previous analyses. Moreover, this congruence between markers and analyses separated by a 12-year period (1988–2000) confirm the temporal stability of this marine barrier at shaping the Iberian phylogeographic break in M. galloprovincialis. In addition, the genetic continuity between the NE Atlantic (Portugal) and the Alboran Sea seems to be warranted across the Gulf of Cadiz and the Gibraltar strait after the present microsatellite data.


Iberian Peninsula Mediterranean Population Exclusion Zone Heterozygote Deficit Iberian Population 
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.



Authors are grateful to M. Pérez and A. Seoane for their experimental help, to D.O.F. Skibinski, E. Da Silva, and four anonymous referees, for their valuable comments on a previous draft. This study has been supported by grant BIO2001/3659 from Ministerio Español de Ciencia y Tecnología, with funds from FEDER (70%) and PGE (30%). A.P. Diz was supported by a grant from Xunta de Galicia, devoted to the improvement of molecular methods for the genetic management of M. galloprovincialis. All the experiments made comply with the current Spanish laws.

Supplementary material

227_2008_921_MOESM1_ESM.doc (430 kb)
Allele frequencies for six Mytilus galloprovincialis microsatellites assayed in 17 mussel populations of the Iberian Peninsula (DOC 427 kb)
227_2008_921_MOESM2_ESM.doc (208 kb)
Diversity parameters for six microsatellite loci analyzed in M. galloprovincialis from the Iberian Peninsula (DOC 205 kb)
227_2008_921_MOESM3_ESM.doc (68 kb)
Pairwise FST values between Iberian populations of Mytilus galloprovincialis. Sample codes are indicated in table 1. ***P < 0.001, **P < 0.01, *P < 0.05, corrected with Bonferroni secuencial test (DOC 64 kb)


  1. 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
  2. Avise JC (1994) Molecular markers, natural history and evolution. Chapman and Hall, New YorkCrossRefGoogle Scholar
  3. Ayvazian SG, Johnson DJ, McGlashan DJ (1994) High levels of subdivision of marine and estuarine populations of the estuarine catfish Cnidoglanis macrocephalus (Plotosidae) in southeastern Australia. Mar Biol 118:25–31CrossRefGoogle Scholar
  4. Balloux F, Brünner H, Lugon-Moulin N, Hausser J, Goudet J (2000) Microsatellites can be misleading: an empirical and simulation study. Evolution 54:1414–1422CrossRefGoogle Scholar
  5. Bargelloni L, Alarcon JA, Alvarez MC, Penzo E, Magoulas A, Reis C, Patarnello T (2003) Discord in the family Sparidae (Teleostei): divergent phylogeographical patterns across the Atlantic-Mediterranean divide. J Evol Biol 16:1149–1158CrossRefGoogle Scholar
  6. Barton NH (1986) The effects of linkage and density-dependent regulation on gene flow. Heredity 57:415–426CrossRefGoogle Scholar
  7. Barton NH, Hewitt GM (1985) Analysis of hybrid zones. Annu Rev Ecol Syst 16:113–148CrossRefGoogle Scholar
  8. Beaumont MA (2005) Adaptation and speciation: what can FST tell us? Trends Ecol Evol 20:435–440CrossRefGoogle Scholar
  9. Castro J, Bouza C, Presa P, Pino-Querido A, Riaza A., Ferreiro I, Sánchez L, Martínez P (2004) Potential sources or error in parentage assessment of turbot (Scophthalmus maximus) using microsatellite loci. Aquaculture 242:119–135CrossRefGoogle Scholar
  10. Cimmaruta R, Bondanelli P, Nascetti G (2005) Genetic structure and environmental heterogeneity in the European hake (Merluccius merluccius). Mol Ecol 14:2577–2591CrossRefGoogle Scholar
  11. Côrte-Real HB, Hawkins SJ, Thorpe JP (1996) Population differentiation and the taxonomic status of the exploited limpet Patella candia in the Macaronesian Islands (Azores, Madeira, Canaries). Mar Biol 125:141–152CrossRefGoogle Scholar
  12. Crow JD, Aoki K (1984) Group selection for a polygenic trait: estimating the degree of population subdivision. Proc Natl Acad Sci USA 81:6073–6077CrossRefGoogle Scholar
  13. Cruz F, Pérez M, Presa P (2005) Distribution and abundance of microsatellites in the genome of Bivalvia. Gene 346:241–247CrossRefGoogle Scholar
  14. Dando PR, Southward AJ (1981) Existence of “Atlantic” and “Mediterranean” forms of Chthamalus montagui (Crustacea, Cirripedia) in the Western Mediterranean. Mar Biol Lett 2:239–248Google Scholar
  15. 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 131:479–491PubMedPubMedCentralGoogle Scholar
  16. Gockel J, Kennington WJ, Hoffmann AA, Goldstein DB, Partridge L (2001) Non-clinality of molecular variation implicates selection in maintaining a morphological cline of Drosophila melanogaster. Genetics 158:319–323PubMedPubMedCentralGoogle Scholar
  17. Goudet J (1995) Fstat (vers. 3.9.5.): a computer program to calculate F-statistics. J Hered 86:485–486CrossRefGoogle Scholar
  18. Hedgecock D (1986) Is gene flow from pelagic larval dispersal important in the adaptation and evolution of marine invertebrates? Bull Mar Sci 39:550–565Google Scholar
  19. Hedgecock D, Li G, Hubert S, Bucklin K, Ribes V (2004) Widespread null alleles and poor cross-species amplification of microsatellite DNA loci cloned from the Pacific oyster, Crassostrea gigas. J Shellfish Res 23:379–385Google Scholar
  20. Johnson MS, Black R (1995) Neighbourhood size and the importance of barriers to gene flow in an intertidal snail. Heredity 2:142–154CrossRefGoogle Scholar
  21. Kenchington EL, Patwary MU, Zouros E, Bird CJ (2006) Genetic differentiation in relation to marine landscape in a broadcast-spawning bivalve mollusc (Placopecten magellanicus). Mol Ecol 15:1781–1796CrossRefGoogle Scholar
  22. Koehn RK (1991) The genetics and taxonomy of species in the genus Mytilus. Aquaculture 94:125–145CrossRefGoogle Scholar
  23. Koehn RK, Newell RIE, Immermann F (1980) Maintenance of an aminopeptidase allele frequency cline by natural selection. Proc Natl Acad Sci USA 77:5385–5389CrossRefGoogle Scholar
  24. Koehn RKJ, Hall G, Innes DJ, Zera AJ (1984) Genetic differentiation of Mytilus edulis in eastern North America. Mar Biol 79:117–126CrossRefGoogle Scholar
  25. Lemaire C, Versini JJ, Bonhomme F (2005) Maintenance of genetic differentiation across a transition zone in the sea: discordance between nuclear and cytoplasmic markers. J Evol Biol 18:70–80CrossRefGoogle Scholar
  26. Marshall TC, Slate J, Kruuk LEB, Pemberton JM (1998) Statistical confidence for likelihood-based paternity inference in natural populations. Mol Ecol 7:639–655CrossRefGoogle Scholar
  27. McMillan WO, Palumbi SR (1995) Concordant evolutionary patterns among Indo-West Pacific Butterflyfishes. Proc R Soc Lond B Biol Sci 260:229–236CrossRefGoogle Scholar
  28. Nagylaki T (1976) Clines with variable migration. Genetics 83:867–886PubMedPubMedCentralGoogle Scholar
  29. Nielsen EE, Hansen MM, Meldrup D (2006) Evidence of microsatellite hitch-hiking selection in Atlantic cod (Gadus morhua L.): implications for inferring population structure in nonmodel organisms. Mol Ecol 15:3219–29CrossRefGoogle Scholar
  30. Palumbi SR (1992) Marine speciation on a small planet. Trends Ecol Evol 7:114–118CrossRefGoogle Scholar
  31. Palumbi SR, Grabowsky G, Duda T, Geyer L, Tachino N (1997) Speciation and population genetic structure in tropical Pacific sea urchins. Evolution 51:1506–1517CrossRefGoogle Scholar
  32. Pannacciulli FG, Bishop JDD, Hawkins SJ (1997) Genetic structure of populations of two species of Chthamalus (Crustacea: Cirripedia) in the North-East Atlantic and Mediterranean. Mar Biol 128:73–82CrossRefGoogle Scholar
  33. Pérez-Losada M, Guerra A, Carvalho GR, Sanjuan A, Shaw PW (2002) Extensive population subdivision of the cuttlefish Sepia officinalis (Mollusca: Cephalopoda) around the Iberian Peninsula indicated by microsatellite DNA variation. Heredity 89:417–424CrossRefGoogle Scholar
  34. Pla C, Vila A, García-Marín JL (1991) Différentiation de stocks de merlu (Merluccius merluccius) par l’analyse génétique: comparaison de plusieurs populations Méditerranéennes et Atlantiques du littoral Espagnol. FAO, Rapport sur les Pêches, Conseil Général des Pêches pour la Méditerranée. Rapport de la Sixième Consultation Technique 447:87–93Google Scholar
  35. Powers DA, Ropson I, Brown DC, Van Beneden R, Cashon R, González-Villaseñor LI, DiMichelle JA (1986) Genetic variation in Fundulus heteroclitus: geographic distribution. Am Zool 26:131–144CrossRefGoogle Scholar
  36. Presa P, Pérez M, Diz AP (2002) Polymorphic microsatellite markers for blue mussels (Mytilus spp.). Conserv Genet 3:441–443CrossRefGoogle Scholar
  37. Pujolar JM, Roldán MI, Pla C (2003) Genetic analysis of tuna populations Thunnus thynnus thynnus and T. alalunga. Mar Biol 143:613–621CrossRefGoogle Scholar
  38. Quesada H, Zapata C, Alvarez G (1995a) A multilocus allozyme discontinuity in the mussel Mytilus galloprovincialis: the interaction of ecological and life-history factors. Mar Ecol Prog Ser 116:99–115CrossRefGoogle Scholar
  39. Quesada H, Beynon CM, Skibinski DOF (1995b) A mitochondrial DNA discontinuity in the mussel Mytilus galloprovincialis Lmk: pleistocene vicariance biogeography and secondary intergradation. Mol Biol Evol 12:521–524PubMedGoogle Scholar
  40. Quesada H, Gallagher C, Skibinski DAG, Skibinski DOF (1998a) Patterns of polymorphism and gene flow of gender-associated mitochondrial DNA lineages in European mussel populations. Mol Ecol 7:1041–1051CrossRefGoogle Scholar
  41. Quesada H, Warren M, Skibinski DOF (1998b) Nonneutral evolution and differential mutation rate of gender-associated mitochondrial DNA lineages in the marine mussel Mytilus. Genetics 149:1511–1526PubMedPubMedCentralGoogle Scholar
  42. Raymond M, Rousset F (1995) GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. J Hered 86:248–249CrossRefGoogle Scholar
  43. Rice WR (1989) Analyzing tables of statistical tests. Evolution 43:223–225CrossRefGoogle Scholar
  44. Ríos C, Sanz S, Saavedra C, Peña JB (2002) Allozyme variation in populations of scallops, Pecten jacobaeus (L.) and P. maximus (L.) (Bivalvia: Pectinidae), across the Almería-Oran front. J Exp Mar Biol Ecol 267:223–244CrossRefGoogle Scholar
  45. Rocha-Olivares A, Vetter RD (1999) Effects of oceanographic circulation on the gene flow, genetic structure, and phylogeography of the rosethorn rockfish (Sebastes helvomaculatus). Can J Fish Aquat Sci 56:803–813CrossRefGoogle Scholar
  46. Sardà F, Calafat A, Flexas MM, Tselepides A, Canals M, Espino M, Tursi A (2004) An introduction to Mediterranean deep-sea biology. Sci Mar 68:7–38CrossRefGoogle Scholar
  47. Schneider S, Kueffer JM, Roessli D, Excoffier L (1997) Arlequin vs. 1.1. A software for population genetic data analysis. Genetics and Biometry Laboratory, University of Geneva, Switzerland. Available at
  48. Shulman MJ, Bermingham E (1995) Early life histories, ocean currents, and the population genetics of Caribbean Reef fishes. Evolution 5:897–910CrossRefGoogle Scholar
  49. Skibinski DOF, Beardmore JA, Cross TF (1983) Aspects of the population genetics of Mytilus (Mytilidae; Mollusca) in the British Isles. Biol J Linn Soc Lond 19:137–183CrossRefGoogle Scholar
  50. Sokolov EP (2000) An improved method for DNA isolation from mucopolysaccharide-rich Molluscan tissues. J Molluscan Stud 66:573–575CrossRefGoogle Scholar
  51. Stickle WB, Diehl WJ (1987) Effects of salinity on echinoderms. In: Jangoux M, Lawrence JM (eds) Echinoderm studies 2. AA Balkema, Rotterdam, pp 235–285Google Scholar
  52. Tintoré J, La Violette PE, Blade I, Cruzado G (1988) A study of an intense density front in the eastern Alboran sea: the Almería-Oran front. J Phys Oceanogr 18:1384–1397CrossRefGoogle Scholar
  53. Vadopalas B, Leclair LL, Bentzen P (2004) Microsatellite and allozyme analyses reveal few genetic differences among spatially distinct aggregations of geoduck clams (Panopea abrupta, Conrad 1849). J Shellfish Res 23:693–706Google Scholar
  54. van Oosterhout C, Hutchinson WF, Wills DPM, Shipley P (2004) Micro-checker: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4:535–538CrossRefGoogle Scholar
  55. Vasemägi A (2006) The adaptive hypothesis of clinal variation revisited: single-locus clines as a result of spatially restricted gene flow. Genetics 173:2411–2414CrossRefGoogle Scholar
  56. Viñas J, Alvarado JR, Bremer, Pla C (2004) Inter-oceanic genetic differentiation among albacore (Thunnus alalunga) populations. Mar Biol 145:225–232CrossRefGoogle Scholar
  57. Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:1358–1370Google Scholar
  58. Williams ST, Benzie JAH (1998) Evidence of a biogeographic break between populations of a high dispersal starfish, congruent regions within the Indo-West Pacific defined by color morphs, mtDNA and allozyme data. Evolution 52:87–99PubMedGoogle Scholar
  59. Zane L, Ostellari L, Maccatrozzo L, Bargelloni L, Cuzin-Roudy J, Buchholz F, Patarnello T (2000) Genetic differentiation in a pelagic crustacean (Meganyctiphanes norvegica, Euphausiacea) from the North East Atlantic and the Mediterranean Sea. Mar Biol 136:191–199CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2008

Authors and Affiliations

  1. 1.Faculty of Marine Sciences—ECIMAT, Department of Biochemistry, Genetics and ImmunologyUniversity of VigoVigoSpain
  2. 2.Department of GeneticsUniversity of Swansea, School of MedicineSwanseaUK

Personalised recommendations