Journal of Molecular Evolution

, Volume 65, Issue 6, pp 651–659 | Cite as

Structure and Evolution of the Atypical Mitochondrial Genome of Armadillidium vulgare (Isopoda, Crustacea)

  • Isabelle Marcadé
  • Richard Cordaux
  • Vincent Doublet
  • Catherine Debenest
  • Didier Bouchon
  • Roland Raimond


The crustacean isopod Armadillidium vulgare is characterized by an unusual ∼42-kb-long mitochondrial genome consisting of two molecules co-occurring in mitochondria: a circular ∼28-kb dimer formed by two ∼14-kb monomers fused in opposite polarities and a linear ∼14-kb monomer. Here we determined the nucleotide sequence of the fundamental monomeric unit of A. vulgare mitochondrial genome, to gain new insight into its structure and evolution. Our results suggest that the junction zone between monomers of the dimer structure is located in or near the control region. Direct sequencing indicated that the nucleotide sequences of the different monomer units are virtually identical. This suggests that gene conversion and/or replication processes play an important role in shaping nucleotide sequence variation in this mitochondrial genome. The only heteroplasmic site we identified predicts an alloacceptor tRNA change from tRNAAla to tRNAVal. Therefore, in A. vulgare, tRNAAla and tRNAVal are found at the same locus in different monomers, ensuring that both tRNAs are present in mitochondria. The presence of this heteroplasmic site in all sequenced individuals suggests that the polymorphism is selectively maintained, probably because of the necessity of both tRNAs for maintaining proper mitochondrial functions. Thus, our results provide empirical evidence for the tRNA gene recruitment model of tRNA evolution. Moreover, interspecific comparisons showed that the A. vulgare mitochondrial gene order is highly derived compared to the putative ancestral arthropod type. By contrast, an overall high conservation of mitochondrial gene order is observed within crustacean isopods.


Atypical mitochondrial genome Armadillidium vulgare Trimeric structure Linear monomer Gene conversion Heteroplasmy tRNA gene recruitment Gene rearrangements Isopod 



We thank Nicolas Galtier and two anonymous reviewers for comments on an early version of the manuscript, Pierre Grève and Mathieu Sicard for constructive discussions, Yves Caubet and Sébastien Verne for providing samples, and Daniel Guyonnet for technical assistance. This research was funded by the Centre National de la Recherche Scientifique (CNRS) and the French Ministère de l’Education Nationale, de l’Enseignement Supérieur et de la Recherche.


  1. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402PubMedCrossRefGoogle Scholar
  2. Boore JL (1999) Animal mitochondrial genomes. Nucleic Acids Res 27:1767–1780PubMedCrossRefGoogle Scholar
  3. Boore JL, Brown WM (1998) Big trees from little genomes: mitochondrial gene order as a phylogenetic tool. Curr Opin Genet Dev 8:668–674PubMedCrossRefGoogle Scholar
  4. Boore JL, Collins TM, Stanton D, Daehler LL, Brown WM (1995) Deducing the pattern of arthropod phylogeny from mitochondrial DNA rearrangements. Nature 376:163–165PubMedCrossRefGoogle Scholar
  5. Boore JL, Lavrov DV, Brown WM (1998) Gene translocation links insects and crustaceans. Nature 392:667–668PubMedCrossRefGoogle Scholar
  6. Bouchon D, Rigaud T, Juchault P (1998) Evidence for widespread Wolbachia infection in isopod crustaceans: molecular identification and host feminization. Proc Biol Sci 265:1081–1090PubMedCrossRefGoogle Scholar
  7. Boyce TM, Zwick ME, Aquadro CF (1989) Mitochondrial DNA in the bark weevils: size, structure and heteroplasmy. Genetics 123:825–836PubMedGoogle Scholar
  8. Cook CE, Yue Q, Akam M (2005) Mitochondrial genomes suggest that hexapods and crustaceans are mutually paraphyletic. Proc Biol Sci 272:1295–1304PubMedCrossRefGoogle Scholar
  9. Cordaux R, Michel-Salzat A, Bouchon D (2001) Wolbachia infection in crustaceans: novel hosts and potential routes for horizontal transmission. J Evol Biol 14:237–243CrossRefGoogle Scholar
  10. Cordaux R, Michel-Salzat A, Frelon-Raimond M, Rigaud T, Bouchon D (2004) Evidence for a new feminizing Wolbachia strain in the isopod Armadillidium vulgare: evolutionary implications. Heredity 93:78–84PubMedCrossRefGoogle Scholar
  11. Grandjean F, Rigaud T, Raimond R, Juchault P, Souty-Grosset C (1993) Mitochondrial DNA polymorphism and feminizing sex factors dynamics in a natural population of Armadillidium vulgare (Crustacea, Isopoda). Genetica 92:55–60PubMedCrossRefGoogle Scholar
  12. Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98Google Scholar
  13. Hickerson MJ, Cunningham CW (2000) Dramatic mitochondrial gene rearrangements in the hermit crab Pagurus longicarpus (Crustacea, anomura). Mol Biol Evol 17:639–644PubMedGoogle Scholar
  14. Higgs PG, Jameson D, Jow H, Rattray M (2003) The evolution of tRNA-Leu genes in animal mitochondrial genomes. J Mol Evol 57:435–445PubMedCrossRefGoogle Scholar
  15. Hwang UW, Friedrich M, Tautz D, Park CJ, Kim W (2001) Mitochondrial protein phylogeny joins myriapods with chelicerates. Nature 413:154–157PubMedCrossRefGoogle Scholar
  16. Ivey JL, Santos SR (2007) The complete mitochondrial genome of the Hawaiian anchialine shrimp Halocaridina rubra Holthuis, 1963 (Crustacea: Decapoda: Atyidae). Gene 394:35–44PubMedCrossRefGoogle Scholar
  17. Kilpert F, Podsiadlowski L (2006) The complete mitochondrial genome of the common sea slater, Ligia oceanica (Crustacea, Isopoda) bears a novel gene order and unusual control region features. BMC Genomics 7:241PubMedCrossRefGoogle Scholar
  18. Lavrov DV, Lang BF (2005) Transfer RNA gene recruitment in mitochondrial DNA. Trends Genet 21:129–133PubMedCrossRefGoogle Scholar
  19. Lavrov DV, Brown WM, Boore JL (2004) Phylogenetic position of the Pentastomida and (pan)crustacean relationships. Proc Biol Sci 271:537–544PubMedCrossRefGoogle Scholar
  20. Lowe TM, Eddy SR (1997) tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res 25:955–964PubMedCrossRefGoogle Scholar
  21. Machida RJ, Miya MU, Nishida M, Nishida S (2002) Complete mitochondrial DNA sequence of Tigriopus japonicus (Crustacea: Copepoda). Mar Biotechnol (NY) 4:406–417CrossRefGoogle Scholar
  22. Michel-Salzat A, Bouchon D (2000) Phylogenetic analysis of mitochondrial LSU rRNA in oniscids. CR Acad Sci III 323:827–837Google Scholar
  23. Miller AD, Nguyen TT, Burridge CP, Austin CM (2004) Complete mitochondrial DNA sequence of the Australian freshwater crayfish, Cherax destructor (Crustacea: Decapoda: Parastacidae): a novel gene order revealed. Gene 331:65–72PubMedCrossRefGoogle Scholar
  24. Miller AD, Murphy NP, Burridge CP, Austin CM (2005) Complete mitochondrial DNA sequences of the decapod crustaceans Pseudocarcinus gigas (Menippidae) and Macrobrachium rosenbergii (Palaemonidae). Mar Biotechnol (NY) 7:339–349CrossRefGoogle Scholar
  25. Nosek J, Tomaska L (2003) Mitochondrial genome diversity: evolution of the molecular architecture and replication strategy. Curr Genet 44:73–84PubMedCrossRefGoogle Scholar
  26. Nosek J, Tomaska L, Fukuhara H, Suyama Y, Kovac L (1998) Linear mitochondrial genomes: 30 years down the line. Trends Genet 14:184–188PubMedCrossRefGoogle Scholar
  27. Ogoh K, Ohmiya Y (2004) Complete mitochondrial DNA sequence of the sea-firefly, Vargula hilgendorfii (Crustacea, Ostracoda) with duplicate control regions. Gene 327:131–139PubMedCrossRefGoogle Scholar
  28. Oldenburg DJ, Bendich AJ (2001) Mitochondrial DNA from the liverwort Marchantia polymorpha: circularly permuted linear molecules, head-to-tail concatemers, and a 5′ protein. J Mol Biol 310:549–562PubMedCrossRefGoogle Scholar
  29. Podsiadlowski L, Bartolomaeus T (2006) Major rearrangements characterize the mitochondrial genome of the isopod Idotea baltica (Crustacea: Peracarida). Mol Phylogenet Evol 40:893–899PubMedCrossRefGoogle Scholar
  30. Raimond R, Marcade I, Bouchon D, Rigaud T, Bossy JP, Souty-Grosset C (1999) Organization of the large mitochondrial genome in the isopod Armadillidium vulgare. Genetics 151:203–210PubMedGoogle Scholar
  31. Rigaud T, Juchault P, Mocquard JP (1997) The evolution of sex determination in isopod crustaceans. Bioessays 19:409–416CrossRefGoogle Scholar
  32. Rigaud T, Bouchon D, Souty-Grosset C, Raimond R (1999) Mitochondrial DNA polymorphism, sex ratio distorters and population genetics in the isopod Armadillidium vulgare. Genetics 152:1669–1677PubMedGoogle Scholar
  33. Rozen S, Skaletsky H (2000) Primer3 on the WWW for general users and for biologist programmers. Methods Mol Biol 132:365–386PubMedGoogle Scholar
  34. Segawa RD, Aotsuka T (2005) The mitochondrial genome of the Japanese freshwater crab, Geothelphusa dehaani (Crustacea: Brachyura): evidence for its evolution via gene duplication. Gene 355:28–39PubMedCrossRefGoogle Scholar
  35. Shao R, Dowton M, Murrell A, Barker SC (2003) Rates of gene rearrangement and nucleotide substitution are correlated in the mitochondrial genomes of insects. Mol Biol Evol 20:1612–1619PubMedCrossRefGoogle Scholar
  36. Signorovitch AY, Buss LW, Dellaporta SL (2007) Comparative genomics of large mitochondria in placozoans. PLoS Genet 3:e13PubMedCrossRefGoogle Scholar
  37. Souty-Grosset C, Raimond R, Tourte M (1992) Déterminisme épigénétique du sexe et divergence génétique de l’ADN mitochondrial chez Armadillidium vulgare Latr. (Crustacé Oniscoïde): variabilité inter et intrapopulations. CR Acad Sci Paris 314:119–125Google Scholar
  38. Sun H, Zhou K, Song D (2005) Mitochondrial genome of the Chinese mitten crab Eriocheir japonica sinenesis (Brachyura: Thoracotremata: Grapsoidea) reveals a novel gene order and two target regions of gene rearrangements. Gene 349:207–217PubMedCrossRefGoogle Scholar
  39. Suyama Y, Miura K (1968) Size and Structural Variations of Mitochondrial DNA. Proc Natl Acad Sci USA 60:235–242PubMedCrossRefGoogle Scholar
  40. Tatarenkov A, Avise JC (2007) Rapid concerted evolution in animal mitochondrial DNA. Proc Biol Sci 274:1795–1798PubMedCrossRefGoogle Scholar
  41. Tjensvoll K, Hodneland K, Nilsen F, Nylund A (2005) Genetic characterization of the mitochondrial DNA from Lepeophtheirus salmonis (Crustacea; Copepoda). A new gene organization revealed. Gene 353:218–230PubMedCrossRefGoogle Scholar
  42. Vahrenholz C, Riemen G, Pratje E, Dujon B, Michaelis G (1993) Mitochondrial DNA of Chlamydomonas reinhardtii: the structure of the ends of the linear 15.8-kb genome suggests mechanisms for DNA replication. Curr Genet 24:241–247PubMedCrossRefGoogle Scholar
  43. Wolstenholme DR (1992) Animal mitochondrial DNA: structure and evolution. Int Rev Cytol 141:173–216PubMedCrossRefGoogle Scholar
  44. Zouros E (2000) The exceptional mitochondrial DNA system of the mussel family Mytilidae. Genes Genet Syst 75:313–318PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2007

Authors and Affiliations

  • Isabelle Marcadé
    • 1
  • Richard Cordaux
    • 1
  • Vincent Doublet
    • 1
  • Catherine Debenest
    • 1
  • Didier Bouchon
    • 1
  • Roland Raimond
    • 1
  1. 1.Laboratoire de Génétique et Biologie des Populations de Crustacés, UMR CNRS 6556Université de PoitiersPoitiersFrance

Personalised recommendations