Marine Biology

, Volume 156, Issue 5, pp 913–925 | Cite as

Molecular population genetics of male and female mitochondrial genomes in European mussels Mytilus

Original Paper

Abstract

The doubly uniparental system of mitochondrial inheritance (DUI) is best known in marine mussels Mytilus. Under DUI there are two types of mitochondrial DNA (mtDNA). The female type (F) is transmitted to offspring of both genders and the male type (M) exclusively to sons; consequently two distinct mtDNA lineages exist. The M lineage evolves under more relaxed selection than the F lineage resulting in higher polymorphism within the M lineage. Though this polymorphism is expected to make inferences on fine population structure easier using M instead of F data, no comprehensive comparative data exist to support this claim. We sequenced a 1,205 bp fragment of M and F mtDNA comprising parts of the COIII and ND2 genes, and analysed 204 individuals representing three Mytilus species: M. edulis, M.galloprovincialis and M. trossulus from 13 European sampling sites. A clear distinction between Mediterranean and Atlantic populations was found with both M and F data, but much better geographic differentiation was found within the Atlantic using F rather than M data. In particular, Atlantic M. galloprovincialis can be differentiated from Atlantic M. edulis, and further subdivision of Atlantic M. edulis is possible using the F data but not the M data. Multiple tests of selection were carried out to attempt to explain this paradox. We concluded that the overall pattern of polymorphism is consistent with strong purifying selection; not only is this selection relaxed in the M lineage in comparison with the F lineage, but it is also more frequently interrupted by periodic selective sweeps within the M lineage.

References

  1. Bazin E, Glémin S, Galtier N (2006) Population size does not influence mitochondrial genetic diversity in animals. Science 312:570–572. doi:10.1126/science.1122033 PubMedCrossRefGoogle Scholar
  2. Bierne N, Borsa P, Daguin C, Jollivet D, Viard F, Bonhomme F, David P (2003) Introgression patterns in the mosaic hybrid zone between Mytilus edulis and M. galloprovincialis. Mol Ecol 12:447–461. doi:10.1046/j.1365-294X.2003.01730.x PubMedCrossRefGoogle Scholar
  3. 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 65:504–507. doi:10.1093/mollus/65.4.504 CrossRefGoogle Scholar
  4. Breton S, Burger G, Stewart DT, Blier PU (2006) Comparative analysis of gender-associated complete mitochondrial genomes in marine mussels (Mytilus spp.). Genetics 172:1107–1119. doi:10.1534/genetics.105.047159 PubMedCrossRefGoogle Scholar
  5. Burridge CP, Craw D, Fletcher D, Waters JM (2008) Geological dates and molecular rates: fish DNA sheds light on time dependency. Mol Biol Evol 25:624–633. doi:10.1093/molbev/msm271 PubMedCrossRefGoogle Scholar
  6. Burzyński A, Zbawicka M, Skibinski DOF, Wenne R (2006) Doubly uniparental inheritance is associated with high polymorphism for rearranged and recombinant control region haplotypes in Baltic Mytilus trossulus. Genetics 174:1081–1094. doi:10.1534/genetics.106.063180 PubMedCrossRefGoogle Scholar
  7. 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 (Berl) 111:87–93. doi:10.1007/BF01986350 CrossRefGoogle Scholar
  8. Excoffier L, Laval G, Schneider S (2005) Arlequin (version 3.0): an integrated software package for population genetics data analysis. Evol Bioinform Online 1:47–50Google Scholar
  9. Filipowicz M, Burzyński A, Śmietanka B, Wenne R (2008) Recombination in Mitochondrial DNA of European Mussels Mytilus. J Mol Evol 67:377–388. doi:10.1007/s00239-008-9157-6 PubMedCrossRefGoogle Scholar
  10. 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.W. England. Biol Bull 185:405–416. doi:10.2307/1542481 CrossRefGoogle Scholar
  11. Gillespie JH (2000) Genetic drift in an infinite population. The pseudohitchhiking model. Genetics 155:909–919PubMedGoogle Scholar
  12. Gosling EM (1992) Genetics of Mytilus. In: Gosling EM (ed) The mussels Mytilus: ecology, physiology, genetics and culture. Elsevier, The Netherlands, pp 309–382Google Scholar
  13. 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
  14. Guindon S, Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52:696–704. doi:10.1080/10635150390235520 PubMedCrossRefGoogle Scholar
  15. Heburn G, La Violette PE (1990) Variation in the structure of the anticyclonic gyres found in the Alboran sea. J Geophys Res 95:1599–1613. doi:10.1029/JC095iC02p01599 CrossRefGoogle Scholar
  16. 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 (Berl) 140:137–142. doi:10.1007/s002270100631 CrossRefGoogle Scholar
  17. 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
  18. Hoarau G, Rijnsdorp AD, Van der Veer HW, Stam WT, Olsen JL (2002) Population structure of plaice (Pleuronectes platessa L.) in northern Europe: microsatellites revealed large-scale spatial and temporal homogeneity. Mol Ecol 11:1165–1176. doi:10.1046/j.1365-294X.2002.01515.x PubMedCrossRefGoogle Scholar
  19. 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
  20. Hoffmann RJ, Boore JL, Brown WM (1992) A novel mitochondrial genome organization for the blue mussel, Mytilus edulis. Genetics 131:397–412PubMedGoogle Scholar
  21. Kijewski TK, Zbawicka M, Väinölä R, Wenne R (2006) Introgression and mitochondrial DNA heteroplasmy in the Baltic populations of mussels Mytilus trossulus and M. edulis. Mar Biol (Berl) 149:1373–1385. doi:10.1007/s00227-006-0316-2 CrossRefGoogle Scholar
  22. Kumar S, Tamura K, Nei M (2004) MEGA3: integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief Bioinform 5:150–163. doi:10.1093/bib/5.2.150 PubMedCrossRefGoogle Scholar
  23. Ladoukakis ED, 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 11:755–769. doi:10.1046/j.1365-294X.2002.01473.x PubMedCrossRefGoogle Scholar
  24. Mantel N (1967) The detection of disease clustering and a generalized regression approach. Cancer Res 27:209–220PubMedGoogle Scholar
  25. Martin DP, Williamson C, Posada D (2005) RDP2: recombination detection and analysis from sequence alignments. Bioinformatics 21:260–262. doi:10.1093/bioinformatics/bth490 PubMedCrossRefGoogle Scholar
  26. McDonald JH, Kreitman M (1991) Adaptive protein evolution at the Adh locus in Drosophila. Nature 351:652–654. doi:10.1038/351652a0 PubMedCrossRefGoogle Scholar
  27. McDonald JH, Seed HR, Koehn RK (1991) Allozyme and morphometric characters of three species of Mytilus in the Northern and Southern Hemispheres. Mar Biol (Berl) 111:323–335. doi:10.1007/BF01319403 CrossRefGoogle Scholar
  28. Mizi A, Zouros E, Moschonas N, Rodakis GC (2005) The complete maternal and paternal mitochondrial genomes of the Mediterranean mussel Mytilus galloprovincialis: implications for the doubly uniparental inheritance mode of mtDNA. Mol Biol Evol 22:952–967. doi:10.1093/molbev/msi079 PubMedCrossRefGoogle Scholar
  29. Ort BS, Pogson GH (2007) Molecular population genetics of the male and female mitochondrial DNA molecules of the California sea mussel, Mytilus californianus. Genetics 177:1087–1099. doi:10.1534/genetics.107.072934 PubMedCrossRefGoogle Scholar
  30. Passamonti M (2007) An unusual case of gender-associated mitochondrial DNA heteroplasmy: the mytilid Musculista senhousia (Mollusca Bivalvia). BMC Evol Biol 7(Suppl 2):S7. doi:10.1186/1471-2148-7-S2-S7 PubMedCrossRefGoogle Scholar
  31. 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
  32. Quesada H, Beynon CM, Skibinski DOF (1995) A mitochondrial DNA discontinuity in the mussel Mytilus galloprovincialis Lmk: pleistocene vicariance biogeography and secondary intergradation. Mol Biol Evol 12:521–524PubMedGoogle Scholar
  33. Quesada H, Skibinski DA, Skibinski DOF (1996) Sex-biased heteroplasmy and mitochondrial DNA inheritance in the mussel Mytilus galloprovincialis Lmk. Curr Genet 29:423–426. doi:10.1007/BF02221509 PubMedCrossRefGoogle Scholar
  34. Quesada H, Warren M, Skibinski DOF (1998a) Nonneutral evolution and differential mutation rate of gender-associated mitochondrial DNA lineages in the marine mussel Mytilus. Genetics 149:1511–1526PubMedGoogle Scholar
  35. Quesada H, Gallagher C, Skibinski DAG, Skibinski DOF (1998b) Patterns of polymorphism and gene flow of gender-associated mitochondrial DNA lineages in European mussel populations. Mol Ecol 7:1041–1051. doi:10.1046/j.1365-294x.1998.00428.x CrossRefGoogle Scholar
  36. Quesada H, Wenne R, Skibinski DOF (1999) Interspecies transfer of female mitochondrial DNA is coupled with role-reversals and departure from neutrality in the mussel Mytilus trossulus. Mol Biol Evol 16:655–665PubMedGoogle Scholar
  37. Rawson PD, Hilbish TJ (1995) Distribution of male and female mtDNA lineages in populations of blue mussels, Mytilus trossulus and M. galloprovincialis, along the Pacific coast of North America. Mar Biol (Berl) 124:245–250. doi:10.1007/BF00347128 CrossRefGoogle Scholar
  38. Rawson PD, Hilbish TJ (1998) Asymmetric introgression of mitochondrial DNA among European population 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(Pt 6):599–607. doi:10.1038/hdy.1996.187 PubMedCrossRefGoogle Scholar
  40. 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 (Berl) 134:201–211. doi:10.1007/s002270050538 CrossRefGoogle Scholar
  41. Rice WR (1989) Analyzing tables of statistical tests. Evol Int J Org Evol 43:223–225. doi:10.2307/2409177 Google 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, Sukhdeo K, Cunningham CW (2002) Evidence for selection at multiple allozyme loci across a mussel hybrid zone. Mol Biol Evol 19:347–351PubMedGoogle Scholar
  44. 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
  45. Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574. doi:10.1093/bioinformatics/btg180 PubMedCrossRefGoogle Scholar
  46. Rozas J, Sánchez-DelBarrio JC, Messeguer X, Rozas R (2003) DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19:2496–2497. doi:10.1093/bioinformatics/btg359 PubMedCrossRefGoogle Scholar
  47. 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 M. trossulus) hybridize. Genetics 143:1359–1367PubMedGoogle Scholar
  48. Skibinski DOF, Gallagher C, Beynon CM (1994a) Sex-limited mitochondrial DNA transmission in the marine mussel Mytilus edulis. Genetics 138:801–809PubMedGoogle Scholar
  49. Skibinski DOF, Gallagher C, Beynon CM (1994b) Mitochondrial DNA inheritance. Nature 368:817–818. doi:10.1038/368817b0 PubMedCrossRefGoogle Scholar
  50. Skibinski DOF, Gallagher C, Quesada H (1999) On the roles of selection, mutation and drift in the evolution of mitochondrial DNA diversity in British Mytilus edulis (Mytilidae; Mollusca) populations. Biol J Linn Soc Lond 68:195–213. doi:10.1111/j.1095-8312.1999.tb01166.x CrossRefGoogle Scholar
  51. Śmietanka B, Zbawicka M, Wołowicz M, Wenne R (2004) Mitochondrial DNA lineages in the European populations of mussels (Mytilus spp.). Mar Biol (Berl) 146:79–92. doi:10.1007/s00227-004-1418-3 CrossRefGoogle Scholar
  52. Staden R, Judge DP, Bonfield JK (2001) Sequence assembly and finishing methods. In: Baxevanis AD, Ouellette BFF (eds) Bioinformatics. A practical guide to the analysis of genes and proteins. Wiley, New York, pp 323–357Google Scholar
  53. Stewart DT, Saavedra C, Stanwood RR, Ball AO, Zouros E (1995) Male and female mitochondrial DNA lineages in the blue mussel (Mytilus edulis) species group. Mol Biol Evol 12:735–747PubMedGoogle Scholar
  54. Stewart DT, Kenchington ER, Singh RK, Zouros E (1996) Degree of selective constraint as an explanation of the different rates of evolution of gender-specific mitochondrial DNA lineages in the mussel Mytilus. Genetics 143:1349–1357PubMedGoogle Scholar
  55. Swofford DL (2003) PAUP*. Phylogenetic analysis using parsimony (*and other methods). Version 4. Sinauer Associates, Sunderland, MAGoogle Scholar
  56. Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585–595PubMedGoogle Scholar
  57. 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 25:4876–4882. doi:10.1093/nar/25.24.4876 PubMedCrossRefGoogle Scholar
  58. Tintore J, La Violette PE, Blade I, Cruzado A (1988) A study of an intense density front in the eastern Alboran sea: the Almeria-Oran front. J Phys Oceanogr 18:1384–1397. doi:10.1175/1520-0485(1988)018<1384:ASOAID>2.0.CO;2 CrossRefGoogle Scholar
  59. Varvio SL, Koehn RK, Väinölä R (1988) Evolutionary genetics of the Mytilus edulis complex in the North Atlantic region. Mar Biol (Berl) 98:51–60. doi:10.1007/BF00392658 CrossRefGoogle Scholar
  60. Venetis C, Theologidis I, Zouros E, Rodakis GC (2007) A mitochondrial genome with a reversed transmission route in the Mediterranean mussel Mytilus galloprovincialis. Gene 406:79–90PubMedGoogle Scholar
  61. Wenne R, Skibinski DOF (1995) Mitochondrial DNA heteroplasmy in European populations of the mussel Mytilus trossulus. Mar Biol (Berl) 122:619–624. doi:10.1007/BF00350683 CrossRefGoogle Scholar
  62. Zouros E, Oberhauser Ball A, Saavedra C, Freeman KR (1994) An unusual type of mitochondrial DNA inheritance in the blue mussel Mytilus. Proc Natl Acad Sci USA 91:7463–7467. doi:10.1073/pnas.91.16.7463 PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2009

Authors and Affiliations

  • Beata Śmietanka
    • 1
  • Artur Burzyński
    • 1
  • Roman Wenne
    • 1
  1. 1.Department of Genetics and Marine Biotechnology, Institute of OceanologyPolish Academy of SciencesSopotPoland

Personalised recommendations