Marine Biology

, Volume 146, Issue 1, pp 79–92 | Cite as

Mitochondrial DNA lineages in the European populations of mussels (Mytilus spp.)

  • B. Śmietanka
  • M. Zbawicka
  • M. Wołowicz
  • R. Wenne
Research Article


Marine mussels (Mytilus spp.) belong to a group of benthic species crucial to coastal ecosystems in Europe and are important for the cultivation industry. In the present study, the nuclear adhesive protein marker (Me15/16) was used for identification of Mytilus species in coastal areas, on a large geographic scale in Europe. Pure M. edulis populations were found in the White Sea and Iceland. M. edulis, M. trossulus and their hybrids were found in the Baltic Sea and the North Sea (Oosterschelde, The Netherlands). M. galloprovincialis, M. edulis and their hybrids occurred in Ireland. M. galloprovincialis populations were observed in the Sea of Azov (Black Sea), the Mediterranean and Portugal. The mitochondrial (mt) DNA coding-region ND2-COIII was studied by PCR (polymerase chain reaction) and RFLP (restriction fragment length polymorphism) assay methods. The mtDNA control region was studied by PCR. Substantial differentiation in the frequency of female haplotypes among the studied populations in Europe was observed. Despite isolation between the Mytilus taxa on a macro-geographic scale, considerable mitochondrial gene flow occurred between populations, with introgression in hybrid zones on a more local geographic scale in Europe. MtDNA of the Atlantic Iberian (Portugal) population of M. galloprovincialis was more similar to mtDNA in populations of M. galloprovincialis and M. edulis from the Atlantic coasts of the Ireland and M. edulis from the North Sea, than to M. galloprovincialis from the Mediterranean. Lower polymorphism of mtDNA in populations of the Baltic and Azov Sea mussels in comparison with other European populations was observed and can be explained by the recent history of both seas after the Pleistocene glaciation. In the M. galloprovincialis population from the Azov Sea, the presence of the male-inherited (M) genome was demonstrated for the first time by sequencing the control region and was observed at high frequency. Possible influence of mussel culture on geographic distribution of the Mytilus taxa in Europe is discussed.



The authors are indebted to Dr. R. Väinölä, Prof. T. Sywula and Dr. W. Kuliński for their help in obtaining the samples of mussels used in this study. The research was partially funded through grant KBN 6P04C 004 11 and SPB no. 31/E-45/5.PR UE. R.W. was supported by EC INCO fellowship ICA1-CT-2002–70021 “COGENE”.


  1. Algan O, Cagatay N, Tchepalyga A, Ongan D, Eastoe C, Gokasan E (2001) Stratigraphy of the sediment in fill in Bosphorus Strait: water exchange between the Black and Mediterranean Seas during the last glacial Holocene. Geo-Mar Lett 20:209–218Google Scholar
  2. Asmussen MA, Basten CJ (1996) Constraints and normalised measures for cytonuclear disequilibria. Heredity 76:207–214PubMedGoogle Scholar
  3. Bell SR (1996) Mitochondrial DNA length variation in the mussel Mytilus. PhD thesis, School of Biological Sciences, University of Wales, Swansea, UKGoogle Scholar
  4. Bierne N, David P, Langlade A, Bonhomme F (2003a) Can habitat specialisation maintain a mosaic hybrid zone in marine bivalves? Mol Ecol Prog Ser 245:157–170Google Scholar
  5. Bierne N, Borsa P, Daguin C, Jollivet D, Viard F, Bonhomme F, David P (2003b) Introgression patterns in the mosaic hybrid zone between Mytilus edulis and M. galloprovincialis. Mol Ecol 12:447–461CrossRefPubMedGoogle Scholar
  6. Borsa P, Daguin C, Caetano SR, Bonhomme F (1999) Nuclear-DNA evidence that northeastern Atlantic Mytilus trossulus mussels carry M. edulis genes. J Molluscan Stud 65:504–507CrossRefGoogle Scholar
  7. Burzyński A, Zbawicka M, Skibinski DOF, Wenne R (2003) Evidence for recombination of mtDNA in the marine mussel Mytilus trossulus from the Baltic. Mol Biol Evol 20:388–392CrossRefPubMedGoogle Scholar
  8. Cao L, Kenchington E, Zouros E, Rodakis GC (2004) Evidence that the large non-coding sequence is the main control region of maternally and paternally transmitted mitochondrial genomes of the marine mussel (Mytilus spp.). Genetics 166:883–894PubMedGoogle Scholar
  9. Carlsson R (2002) Shell gravel deposits on the Aland Islands, southwestern Finland, with special reference to the molluscan assemblages. Boreas (Oslo) 31:203–211Google Scholar
  10. Comesana AS, Toro JE, Innes DJ, Thompson RJ (1999) A molecular approach to the ecology of a mussel (Mytilus edulisM. trossulus) hybrid zone on the east coast of Newfoundland, Canada. Mar Biol 133:213–221CrossRefGoogle Scholar
  11. Coustau C, Renaud F, Delay B (1991) Genetic characterisation of the hybridisation between Mytilus edulis and M. galloprovincialis on the Atlantic coast of France. Mar Biol 111:87–93Google Scholar
  12. Daguin C, Bonhomme F, Borsa P (2001) The zone of sympatry and hybridisation of Mytilus edulis and M. galloprovincialis, as described by intron length polymorphism at locus mac-1. Heredity 86:342–354CrossRefPubMedGoogle Scholar
  13. Dijkema R (1997) Molluscan fisheries and culture in The Netherlands. NOAA (Natl Ocean Atmos Adm) Tech Rep NMFS (Natl Mar Fish Serv) 129:115–136Google Scholar
  14. 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 131:479–491PubMedGoogle Scholar
  15. Felsenstein J (1993) PHYLIP (Phylogeny Inference Package, version 3.5c). Department of Genetics, SK-50, University of Washington, SeattleGoogle Scholar
  16. Fitch WM, Margoliash E (1967) Construction of phylogenetic trees. Science 155:279–284PubMedGoogle Scholar
  17. Gardner JPA, Skibinski DOF, Bajdik CD (1993) Shell growth and viability differences between the marine mussels Mytilus edulis (L.), Mytilus galloprovincialis (Lmk.), and their hybrids from two sympatric populations in S.E. England. Biol Bull (Woods Hole) 185:405–416Google Scholar
  18. Gilek M, Littorin B, Saetre P (2001) Spatial patterns of abundance and growth of Mytilus edulis on boulders in the northern Baltic Sea proper. Hydrobiologia 452:59–68CrossRefGoogle Scholar
  19. Gilg MR, Hilbish TJ (2003) Spatio-temporal patterns in the genetic structure of recently settled blue mussels (Mytilus spp.) across a hybrid zone. Mar Biol 143:679–690CrossRefGoogle Scholar
  20. Gosling EM (1991) Genetics of Mytilus. In: Gosling EM (ed) The mussel Mytilus: ecology, physiology, genetics and culture. Elsevier, Amsterdam, pp 309–382Google Scholar
  21. Gosling EM (1994) Speciation and species concepts in the marine environment. In: Beaumont AR (ed) Genetics and evolution of aquatic organisms. Chapman and Hall, London, pp 1–14Google Scholar
  22. Goulletquer P, Le Moine O (2002) Shellfish farming and Coastal Zone Management (CZM) development in the Marennes-Oléron Bay and Charentais Sounds (Charente Maritime, France): a review of recent developments. Aquac Int 10:507–525CrossRefGoogle Scholar
  23. Grant WS, Waples RS (2000) Spatial and temporal scales of genetic variability in marine and anadromous species: implications for fisheries oceanography. In: Harrison PJ, Parsons TR (eds) Fisheries oceanography: an integrative approach to fisheries ecology and management. Blackwell Science, Oxford, pp 63–93Google Scholar
  24. Hauser L, Turan C, Carvalho GR (2001) Haplotype frequency distribution and discriminatory power of two mtDNA fragments in a marine pelagic teleost (Atlantic herring, Clupea harengus). Heredity 87:621–630CrossRefPubMedGoogle Scholar
  25. Hickman RW (1992) Mussel cultivation. In: Gosling EM (ed) The mussel Mytilus: ecology, physiology, genetics and culture. Dev Aquac Fish Sci 25:465–510Google Scholar
  26. Hilbish TJ, Mullinax A, Dolven SI, Meyer A, Koehn RK, Rawson PD (2000) Origin of the antitropical distribution pattern in marine mussels (Mytilus spp.): routes and timing of transequatorial migration. Mar Biol 136:69–77CrossRefGoogle Scholar
  27. Hilbish TJ, Carson EW, Plante JR, Weaver LA, Gilg MR (2002) Distribution of Mytilus edulis, M. galloprovincialis, and their hybrids in open-coast populations of mussels in southwestern England. Mar Biol 140:137–142CrossRefGoogle Scholar
  28. Hilbish TJ, Timmons J, Agrawal V, Schneider KR, Gilg MR (2003) Estuarine habitats protect hybrid mussels from selection. J Exp Mar Biol Ecol 292:177–186CrossRefGoogle Scholar
  29. Hoeh WR, Stewart DT, Saavedra C, Sutherland BW, Zouros E (1997) Phylogenetic evidence for role-reversals of gender-associated mitochondrial DNA in Mytilus (Bivalvia: Mytilidae). Mol Biol Evol 14:959–967PubMedGoogle Scholar
  30. Hoffmann RJ, Boore JL, Brown WM (1992) A novel mitochondrial genome organisation for the blue mussel, Mytilus edulis. Genetics 131:397–412PubMedGoogle Scholar
  31. Hummel H, Colucci F, Bogaards RH, Strelkov P (2001) Genetic traits in the bivalve Mytilus from Europe, with an emphasis on Arctic populations. Polar Biol 24:44–52CrossRefGoogle Scholar
  32. Inoue K, Waite JH, Matsuoka M, Odo S, Harayama S (1995) Interspecific variations in adhesive protein gene sequences of Mytilus edulis, M. galloprovincialis and M. trossulus. Biol Bull (Woods Hole) 189:370–375Google Scholar
  33. Inoue K, Odo S, Noda T, Nakao S, Takeyama S, Yamaha E, Yamazaki F, Harayama S (1997) A possible hybrid zone in the Mytilus edulis complex in Japan revealed by PCR markers. Mar Biol 128:91–95CrossRefGoogle Scholar
  34. Kamermans P, Smaal AC (2002) Mussel culture and cockle fisheries in the Netherlands: finding a balance between economy and ecology. J Shellfish Res 21:509–517Google Scholar
  35. Khalaman VV (2001) Succession of fouling communities on an artificial substrate of a mussel culture in the White Sea. Russ J Mar Biol 27:345–352CrossRefGoogle Scholar
  36. Koehn RK (1991) The genetics and taxonomy of species in the genus Mytilus. Aquaculture 94:125–145CrossRefGoogle Scholar
  37. Ladoukakis E, Zouros E (2001) Direct evidence for homologues recombination in mussel (Mytilus galloprovincialis) mitochondrial DNA. Mol Ecol 18:1168–1175Google Scholar
  38. Ladoukakis E, Saavedra C, Magoulas A, Zouros E (2002) Mitochondrial DNA variation in a species with two mitochondrial genomes: the case of Mytilus galloprovincialis from the Atlantic, the Mediterranean and the Black Sea. Mol Ecol 11:755–769CrossRefPubMedGoogle Scholar
  39. Luttikhuisen PC, Koolhaas A, Bol A, Piersma T (2002) Mytilus galloprovincialis-type foot-protein-1 alleles occur at low frequency among mussels in the Dutch Wadden Sea. J Sea Res 48:241–245CrossRefGoogle Scholar
  40. Martel AL, Auffrey LM, Robles CD, Honda BM (2000) Identification of settling and early postlarval stages of mussles (Mytilus spp.) from the Pacific coast of North America, using prodissoconch morphology and genomic DNA. Mar Biol 137:811–818CrossRefGoogle Scholar
  41. McDonald JH, Seed R, Koehn RK (1991) Allozyme and morphometric characters of three species of Mytilus in the northern and southern hemispheres. Mar Biol 111:323–335Google Scholar
  42. McElroy D, Moran P, Bermingham E, Kornfield I (1991) REAP (The Restriction Enzyme Analysis Package, version 4.0). Department of Zoology, Migratory Fish Research Institute and Center for Marine Studies, University of Maine, OronoGoogle Scholar
  43. Miller JC (1991) Restsite. A phylogenetic program that sorts raw restriction data. J Hered 82:262–263PubMedGoogle Scholar
  44. Nei M, Tajima F (1981) DNA polymorphism detectable by restriction endonucleases. Genetics 97:145–163PubMedGoogle Scholar
  45. Quesada H, Beynon CM, Skibinski DOF (1995a) A mitochondrial DNA discontinuity in the mussel Mytilus galloprovincialis Lmk: Pleistocene vicariance biogeography and secondary intergradation. Mol Biol Evol 12:521–524PubMedGoogle Scholar
  46. Quesada H, Wenne R, Skibinski DOF (1995b) Differential introgression of mitochondrial DNA across species boundaries within the marine mussel genus Mytilus. Proc R Soc Lond 262:57–64Google Scholar
  47. Quesada H, Zapata C, Alvarez G (1995c) A multilocus allozyme discontinuity in the mussel Mytilus galloprovincialis: the interaction of ecological and life-history factors. Mar Ecol Prog Ser 116:99–115Google Scholar
  48. Quesada H, Skibinski DAG, Skibinski DOF (1996) Sex-biased heteroplasmy and mitochondrial DNA inheritance in the mussel Mytilus galloprovincialis Lmk. Curr Genet 29:423–426CrossRefPubMedGoogle Scholar
  49. Quesada H, Gallagher C, Skibinski DAG, Skibinski DOF (1998) Patterns of polymorphism and gene flow of gender-associated mitochondrial DNA lineages in European mussel populations. Mol Ecol 7:1041–1051CrossRefGoogle Scholar
  50. Quesada H, Wenne R, Skibinski DOF (1999) Interspecies transfer of female mitochondrial DNA is coupled with role-reversal and departure from neutrality in the mussel Mytilus trossulus. Mol Biol Evol 16:655–665PubMedGoogle Scholar
  51. Rawson PD, Hilbish TJ (1998) Asymmetric introgression of mitochondrial DNA among European population of blue mussels (Mytilus spp.). Evolution 52:100–108Google Scholar
  52. Rawson PD, Agrawal V, Hilbish TJ (1999) Hybridisation between the blue mussels Mytilus galloprovincialis and M. trossulus along the Pacific coast of North America: evidence for limited introgression. Mar Biol 134:201–211CrossRefGoogle Scholar
  53. Riginos C, Sukhedeo K, Cunningham CW (2002) Evidence for selection at multiple allozyme loci across a mussel hybrid zone. Mol Biol Evol 19:347–351PubMedGoogle Scholar
  54. Roff DA, Bentzen P (1989) The statistical analysis of mitochondrial DNA polymorphism: χ2 and the problem of small samples. Mol Biol Evol 6:539–545PubMedGoogle Scholar
  55. Saavedra C, Stewart DT, Stanwood RR, Zouros E (1996) Species-specific segregation of gender-associated mitochondrial DNA types in an area where two mussel species (Mytilus edulis and Mytilus trossulus) hybridize. Genetics 143:1359–1367PubMedGoogle Scholar
  56. Saavedra C, Reyero MI, Zouros E (1997) Male-dependent doubly uniparental inheritance of mitochondrial DNA and female-dependent sex ratio in the mussel Mytilus galloprovincialis. Genetics 145:1073–1082PubMedGoogle Scholar
  57. Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual, 2nd edn. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y., USAGoogle Scholar
  58. Saranchova OL, Flyachinskaya LP (2001) The influence of salinity on early ontogeny of the mussel Mytilus edulis and the starfish Asterias rubens from the White Sea. Russ J Mar Biol 27:87–93CrossRefGoogle Scholar
  59. 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, SwitzerlandGoogle Scholar
  60. Skibinski DOF, Beardmore JA (1979) Genetic study of intergradation between Mytilus edulis and Mytilus galloprovincialis. Experientia 35:1442–1445PubMedGoogle Scholar
  61. Skibinski DOF, Ahmad M, Beardmore JA (1978) Genetic evidence for naturally occurring hybrids between Mytilus edulis and Mytilus galloprovincialis. Evolution 32:354–364Google Scholar
  62. Skibinski DOF, Beardmore JA, Cross TF (1983) Aspects of the population genetics of Mytilus (Mytilidae: Mollusca) in the British Isles. Biol J Linn Soc 19:137–183Google Scholar
  63. Skibinski DOF, Gallagher C, Beynon CM (1994) Sex-limited mitochondrial-DNA transmission in the marine mussel Mytilus edulis. Genetics 138:801–809PubMedGoogle Scholar
  64. Skurikhina LA, Kartavtsev YuF, Chichvarkhin AYu, Pan’kova MV (2001) Study of two species of mussels, Mytilus trossulus and Mytilus galloprovincialis (Bivalvia, Mytilidae), and their hybrids in Peter the Great Bay of the Sea of Japan with the use of PCR marker. Russ J Genet 37:1448–1451CrossRefGoogle Scholar
  65. Smaal AC (2002) European mussel cultivation along the Atlantic coast: production status, problems and perspectives. Hydrobiologia 484:89–98CrossRefGoogle Scholar
  66. Stepien CA (1999) Phylogeographical structure of the Dover sole Microstomus pacificus: the larval retention hypothesis and genetic divergence along the deep continental slope of the northeastern Pacific Ocean. Mol Ecol 8:923–939CrossRefPubMedGoogle Scholar
  67. Suchanek TH, Geller JB, Kreiser BR, Mitton JB (1997) Zoogeographic distributions of the sibling species Mytilus galloprovincialis and M. trossulus (Bivalvia: Mytilidae) and their hybrids in the North Pacific. Biol Bull (Woods Hole) 193:187–194Google Scholar
  68. Thorarinsdóttir GG, Gunnarsson K (2003) Reproductive cycles of Mytilus edulis L. on the west and east coasts of Iceland. Polar Res 22:217–223Google Scholar
  69. Toro JE (1998) PCR-based nuclear and mtDNA markers and shell morphology as an approach to study the taxonomic status of the Chilean blue mussel, Mytilus chilensis (Bivalvia). Aquat Living Resour 11:347–353CrossRefGoogle Scholar
  70. Toro JE, Thompson RJ, Innes DJ (2002) Reproductive isolation and reproductive output in two sympatric mussel species (Mytilus edulis and M. trossulus) and their hybrids from Newfoundland. Mar Biol 141:897–909CrossRefGoogle Scholar
  71. Väinölä R, Hvilsom MM (1991) Genetic divergence and a hybrid zone between Baltic and North Sea Mytilus populations (Mytilidae: Mollusca). Biol J Linn Soc 43:127–148Google Scholar
  72. Wenne R, Skibinski DOF (1995) Mitochondrial DNA heteroplasmy in European populations of the mussels Mytilus trossulus. Mar Biol 122:619–624Google Scholar
  73. Westerbom M, Kilpi M, Mustonen O (2002) Blue mussels, Mytilus edulis, at the edge of the range: population structure, growth and biomass along a salinity gradient in the north-eastern Baltic Sea. Mar Biol 140:991–999CrossRefGoogle Scholar
  74. Yeh FC, Rong-cai Y, Boyle T (1999) Popgene version 1.31. Freeware for population genetic analysis, available from
  75. Zbawicka M, Skibinski DOF, Wenne R (2003) Doubly uniparental transmission of mitochondrial DNA length variants in the mussel Mytilus trossulus. Mar Biol 142:455–460Google Scholar
  76. Zouros E (2000) The exceptional mitochondrial DNA system of the mussel family Mytilidae. Genes Genet Syst 75:313–318CrossRefPubMedGoogle Scholar
  77. Zouros E, Ball AO, Saavedra C, Freeman KR (1994) An unusual type of mitochondrial-DNA inheritance in the blue mussel Mytilus. Proc Natl Acad Sci USA 91:7463–7467PubMedGoogle Scholar

Copyright information

© Springer-Verlag 2004

Authors and Affiliations

  • B. Śmietanka
    • 1
  • M. Zbawicka
    • 1
  • M. Wołowicz
    • 2
  • R. Wenne
    • 1
    • 3
  1. 1.Department of Genetics and Marine BiotechnologyInstitute of Oceanology PASGdyniaPoland
  2. 2.Laboratory of Estuarine Ecology, Institute of OceanographyUniversity of GdańskGdyniaPoland
  3. 3.Molecular Ecology and Fisheries Genetics Laboratory, Department of Biological SciencesUniversity of HullHullUK

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