Marine Biology

, Volume 156, Issue 9, pp 1857–1868

Colonization of the northwest Atlantic by the blue mussel, Mytilus trossulus postdates the last glacial maximum

Original Paper


Blue mussels in the genus Mytilus first arrived in the Atlantic Ocean from the Pacific during the Pliocene, following the opening of the Bering Strait. Repeated periods of glaciation throughout the Pleistocene led to re-isolation of the two ocean basins and the allopatric divergence of Mytilus edulis in the Atlantic and M. trossulus in the Pacific. Mytilus trossulus has subsequently colonized the northwest Atlantic (NW Atlantic) so that the two species are presently sympatric and hybridize throughout much of the Canadian Maritimes and the Gulf of Maine. To estimate when M. trossulus arrived in the NW Atlantic, we have examined sequence variation within a portion of the female mtDNA lineage large untranslated region (F-LUR) for 156 mussels sampled from three Pacific and eleven Atlantic populations of M. trossulus. Although we found no evidence of reciprocal monophyly for Pacific and NW Atlantic M. trossulus, limited gene flow between ocean basins has led to the divergence of unique sequence clades within each ocean basin. In contrast, relative genetic homogeneity indicates high levels of gene flow within each basin. Coalescence-based analysis of the F-LUR sequences suggests that M. trossulus recolonized the NW Atlantic from the northeast Pacific subsequent to a demographic expansion in the Pacific that occurred ~96,000 years before present (ybp). Estimates of timing of divergence for Pacific and NW Atlantic populations and the time since expansion among NW Atlantic sequence clades indicate that M. trossulus arrived in the NW Atlantic more recently, between 20,000 and 46,000 ybp. Given that these estimates overlap with the dates of peak ice in the NW Atlantic during the last glacial maximum (LGM, ~18,000–21,000 ybp), we suggest that colonization of the NW Atlantic by M. trossulus occurred during, but more likely just subsequent to, the LGM and was followed by rapid temporal and spatial expansion in the region.


  1. Addison JA, Hart MW (2005) Colonization, dispersal, and hybridization influence phylogeography of north Atlantic sea urchins (Strongylocentrotus droebachiensis). Evol Int J Org Evol 59:532–543Google Scholar
  2. Ayala F (1997) Vagaries of the molecular clock. Proc Natl Acad Sci USA 94:7776–7783. doi:10.1073/pnas.94.15.7776 PubMedCrossRefGoogle Scholar
  3. Bandelt H-J, Forster P, Röhl A (1999) Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol 16:37–48PubMedGoogle Scholar
  4. Bates JA, Innes DJ (1995) Genetic variation among populations of Mytilus spp. in eastern Newfoundland. Mar Biol (Berl) 124:417–424. doi:10.1007/BF00363915 CrossRefGoogle Scholar
  5. Beaumont AR, Hawkins MP, Doig FL, Davies IM, Snow M (2008) Three species of Mytilus and their hybrids identified in a Scottish Loch: natives, relicts and invaders? J Exp Mar Biol Ecol 367:100–110. doi:10.1016/j.jembe.2008.08.021 CrossRefGoogle Scholar
  6. Bigg GR, Cunningham CW, Ottersen G, Pogson GH, Wadley MR, Williamson P (2008) Ice-age survival of Atlantic cod: agreement between palaeoecology models and genetics. Proc R Soc Lond B Biol Sci 275:163–172. doi:10.1098/rspb.2007.1153 CrossRefGoogle 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 20:388–392. doi:10.1093/molbev/msg058 PubMedCrossRefGoogle Scholar
  8. Cao L, Kenchington E, Zouros E, Rodakis GC (2004) Evidence tha the large noncoding sequence is the main control region of maternally and paternally transmitted mitochondrial genomes of the marine mussel (Mytilus spp.). Genetics 167:835–850. doi:10.1534/genetics.103.026187 PubMedCrossRefGoogle Scholar
  9. Comesaña AS, Toro JE, Innes DJ, Thompson RJ (1999) A molecular approach to the ecology of a mussel (Mytilus edulis-M. trossulus) hybrid zone on the east coast of Newfoundland, Canada. Mar Biol (Berl) 133:213–221. doi:10.1007/s002270050460 CrossRefGoogle Scholar
  10. Cronin TM (1988) Evolution of marine climates of the U.S. Atlantic coast during the past four million years. Philos Trans R Soc Lond Ser B 318:661–678. doi:10.1098/rstb.1988.0029 CrossRefGoogle Scholar
  11. Cunningham CW (2007) How to use genetic data to distinguish between natural and human-mediated introduction of Littorina littorea to North America. Biol Inv 10:1–6. doi:10.1007/s10530-007-9099-8 CrossRefGoogle Scholar
  12. Darby DA, Polyak L, Bauch HA (2006) Past glacial and interglacial conditions in the Arctic Ocean and marginal seas—a review. Prog Oceanogr 71:129–144. doi:10.1016/j.pocean.2006.09.009 CrossRefGoogle Scholar
  13. Dawson AG (1992) Ice age earth: late quaternary geology and climate. Routledge, New YorkGoogle Scholar
  14. Dodson JJ, Tremblay S, Colombani F, Carscadden JE, Lecomte F (2007) Trans-Arctic dispersals and the evolution of a circumpolar marine fish species complex, the capelin (Mallotus villosus). Mol Ecol 16:5030–5043. doi:10.1111/j.1365-294X.2007.03559.x PubMedCrossRefGoogle Scholar
  15. Dyke AS, Andrews JT, Clark PU, England JH, Miller GH, Shaw J, Veillette JJ (2002) The Laurentide and Innuitian ice sheets during the last glacial maximum. Quat Sci Rev 21:9–31. doi:10.1016/S0277-3791(01)00095-6 CrossRefGoogle Scholar
  16. Excoffier L, Smouse P, Quattro J (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: applications to human mitochondrial DNA restriction data. Genetics 131:479–491PubMedGoogle Scholar
  17. Fu Y-X (1997) Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147:915–925PubMedGoogle Scholar
  18. Geller JB, Carlton JT, Powers DA (1994) PCR-based detection of mtDNA haplotypes of native and invading mussels on the northeastern Pacific coast: latitudinal pattern of invasion. Mar Biol (Berl) 119:243–249. doi:10.1007/BF00349563 CrossRefGoogle Scholar
  19. Heath DD, Rawson PD, Hilbish TJ (1995) PCR-based nuclear markers identify alien blue mussel (Mytilus spp.) genotypes on the west coast of Canada. Can J Fish Aquat Sci 52:2621–2627. doi:10.1139/f95-851 CrossRefGoogle Scholar
  20. Hewitt GM (1996) Some genetic consequences of ice ages and their role in divergence and speciation. Bot J Linn Soc 58:247–276Google Scholar
  21. Hewitt GM (2000) The genetic legacy of the quaternary ice ages. Nature 405:907–913. doi:10.1038/35016000 PubMedCrossRefGoogle Scholar
  22. Hey J, Nielsen R (2004) Multilocus methods for estimating population sizes, migration rates and divergence time, with applications to the divergence of Drosophila pseudobscura and D. persimilis. Genetics 167:747–760. doi:10.1534/genetics.103.024182 PubMedCrossRefGoogle Scholar
  23. Ho SYW, Phillips MJ, Cooper A, Drummond AJ (2005) Time dependency of molecular rate estimates and systematic overestimation of recent divergence times. Mol Biol Evol 22:1561–1568. doi:10.1093/molbev/msi145 PubMedCrossRefGoogle Scholar
  24. Hoffman RJ, Boore JL, Brown WM (1992) A novel mitochondrial genome organization for the blue mussel, Mytilus edulis. Genetics 131:397–412Google Scholar
  25. Ingolfsson A (1992) The origin of the rocky shore fauna of Iceland and the Canadian Maritimes. J Biogeography 19:705–712. doi:10.2307/2845711 CrossRefGoogle Scholar
  26. Kaufman DS, Ager TA, Anderson NJ, Anderson PM, Andrews JT, Bartlein PJ, Brubaker LB, Coats LL, Cwynar LC, Duvall ML, Dyke AS, Edwards ME, Eisner WR, Gajewski K, Geirsdottir A, Hu FS, Jennings AE, Kaplan MR, Kerwin MW, Lozhkin AV, MacDonald GM, Miller GH, Mock CJ, Oswald WW, Otto-Bliesner BL, Porinchu DF, Ruhland K, Smol JP, Steig EJ, Wolfe BB (2004) Holocene thermal maximum in the western Arctic. Quat Sci Rev 23:529–560. doi:10.1016/j.quascirev.2003.09.007 CrossRefGoogle Scholar
  27. Luttikhuizen PC, Drent J, Baker AJ (2003) Disjunct distribution of highly diverged mitochondrial lineage clade and population subdivision in a marine bivalve with pelagic larval dispersal. Mol Ecol 12:2215–2229. doi:10.1046/j.1365-294X.2003.01872.x PubMedCrossRefGoogle Scholar
  28. Marincovich L, Gladenkov AY (1998) Evidence for an early opening of the Bering Strait. Nature 397:149–151. doi:10.1038/16446 CrossRefGoogle Scholar
  29. McDonald JH, Seed R, Koehn RK (1991) Allozymes and morphometric characters of three species of Mytilus in the Northern and Southern Hemispheres. Mar Biol (Berl) 111:323–333. doi:10.1007/BF01319403 CrossRefGoogle Scholar
  30. Nikula R, Strelkov P, Väinölä R (2007) Diversity and trans-Arctic invasion history of mitochondrial lineages in the North Atlantic Macoma balthica complex (Bivalvia: Tellinidae). Evol Int J Org Evol 61:928–941. doi:10.1111/j.1558-5646.2007.00066.x Google Scholar
  31. O’Foighil D, Jozefowicz CJ (1999) Amphi-Atlantic phylogeography of direct developing lineages of Lasaea, a genus of brooding bivalves. Mar Biol (Berl) 135:115–122. doi:10.1007/s002270050608 CrossRefGoogle Scholar
  32. Palumbi SR, Kessing BD (1991) Population biology of the trans-Arctic exchange: mtDNA sequence similarity between Pacific and Atlantic sea urchins. Evol Int J Org Evol 45:1790–1805. doi:10.2307/2409832 Google Scholar
  33. Palumbi SR, Wilson AC (1990) Mitochondrial DNA diversity in the sea urchins Strongylocentrotus purpuratus and S. droebachiensis. Evol Int J Org Evol 44:403–415. doi:10.2307/2409417 Google Scholar
  34. Posada D, Crandall KA (1998) Modeltest: testing the model of DNA substitution. Bioinformatics 14:817–818. doi:10.1093/bioinformatics/14.9.817 PubMedCrossRefGoogle Scholar
  35. Quesada H, Wenne R, Skibinski DOF (1995) Differential introgression of mitochondrial DNA across species boundaries within the marine mussel genus Mytilus. Proc R Soc Lond B Biol Sci 262:51–56. doi:10.1098/rspb.1995.0175 CrossRefGoogle Scholar
  36. Ramos-Onsins SE, Rozas J (2002) Statistical properties of new neutrality tests against population growth. Mol Biol Evol 19:2092–2100PubMedGoogle Scholar
  37. Rawson PD (2005) Nonhomologous recombination between the large unassigned region of the male and female mitochondrial genomes in the mussel Mytilus trossulus. J Mol Evol 61:717–732. doi:10.1007/s00239-004-0035-6 PubMedCrossRefGoogle Scholar
  38. Rawson PD, Hilbish TJ (1998) Asymmetric introgression of mitochondrial DNA among European populations of blue mussels (Mytilus spp.). Evol Int J Org Evol 52:100–108. doi:10.2307/2410924 Google Scholar
  39. Rawson PD, Joyner KL, Meetze K, Hilbish TJ (1996) Evidence for intragenic recombination within a novel genetic marker that distinguishes mussels in the Mytilus edulis species complex. Heredity 77:599–607. doi:10.1038/hdy.1996.187 PubMedCrossRefGoogle Scholar
  40. Rawson PD, Hayhurst S, VanScoyoc B (2001) Species composition of blue mussel populations in the northeastern Gulf of Maine. J Shellfish Res 20:31–38Google Scholar
  41. Riginos C, Cunningham CW (2005) Local adaptation and species segregation in two mussel (Mytilus edulis × Mytilus trossulus) hybrid zones. Mol Ecol 14:381–400. doi:10.1111/j.1365-294X.2004.02379.x PubMedCrossRefGoogle Scholar
  42. Riginos C, Henzler CM (2008) Patterns of mtDNA diversity in North Atlantic populations of the mussel Mytilus edulis. Mar Biol (Berl) 155:399–412. doi:10.1007/s00227-008-1038-4 CrossRefGoogle Scholar
  43. Riginos C, Hickerson MJ, Henzler CM, Cunningham CW (2004) Differential patterns of male and female mtDNA exchange across the Atlantic Ocean in the blue mussel, Mytilus edulis. Evol Int J Org Evol 58:2438–2451Google Scholar
  44. Riser JAM (2001) Quaternary geology and the environment. Praxis Publishing, ChichesterGoogle Scholar
  45. Rogers AR, Harpending H (1992) Population growth makes waves in the distribution of pairwise genetic differences. Mol Biol Evol 9:552–569PubMedGoogle Scholar
  46. Schneider S, Roessli D, Excoffier L (2000) Arlequin ver. 2.0. software for population genetic data analysis. Genetics and Biometry Laboratory, University of Geneva, SwitzerlandGoogle Scholar
  47. Suchanek TH, Geller JB, Kresier 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 193:187–194. doi:10.2307/1542764 CrossRefGoogle Scholar
  48. Swofford DL (2001) PAUP*: Phylogenetic analysis using parsimony (* and Other Methods), Ver. 4. Sinauer Associates. Massachusetts, SunderlandGoogle Scholar
  49. Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585–595PubMedGoogle Scholar
  50. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The ClustalX-Windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882. doi:10.1093/nar/25.24.4876 PubMedCrossRefGoogle Scholar
  51. Väinölä R (2003) Repeated trans-Arctic invasions in littoral bivalves: molecular zoogeography of the Macoma balthica complex. Mar Biol (Berl) 143:935–946. doi:10.1007/s00227-003-1137-1 CrossRefGoogle Scholar
  52. Väinölä R, Varvio SL (1989) Biosystematics of Macoma balthica in northwestern Europe. In: Ryland JS, Tyler PA (eds) Reproduction, genetics and distribution of marine organisms. 23rd Eur Mar Bio Symp Olsen & Olsen. Fredensborg, Denmark, pp 309–316Google Scholar
  53. Vermeij GJ (1991) Anatomy of an invasion: the trans-Arctic interchange. Paleobiology 17:281–307Google Scholar
  54. Vermeij GJ (2005) From Europe to America: pliocene to recent trans-Atlantic expansion of cold-water North Atlantic molluscs. Proc R Soc Lond B Biol Sci 272:2545–2550. doi:10.1098/rspb.2005.3177 CrossRefGoogle Scholar
  55. Wares JP, Cunningham CW (2001) Phylogeography and historical ecology of the North Atlantic intertidal. Evol Int J Org Evol 55:2455–2469Google Scholar
  56. Won Y-J, Hey J (2005) Divergence population genetics of chimpanzees. Mol Biol Evol 22:297–307. doi:10.1093/molbev/msi017 PubMedCrossRefGoogle Scholar
  57. Zbawicka M, Wenne R, Skibinski DOF (2003) Mitochondrial DNA variation in populations of the mussel Mytilus trossulus from the Southern Baltic. Hydrobiologia 499:1–12. doi:10.1023/A:1026356603105 CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2009

Authors and Affiliations

  1. 1.School of Marine SciencesUniversity of MaineOronoUSA
  2. 2.Department of BiologyRollins CollegeWinter ParkUSA

Personalised recommendations