Journal of Molecular Evolution

, Volume 74, Issue 1–2, pp 81–95 | Cite as

Nucleotide Composition of CO1 Sequences in Chelicerata (Arthropoda): Detecting New Mitogenomic Rearrangements

  • Juliette Arabi
  • Mark L. I. Judson
  • Louis Deharveng
  • Wilson R. Lourenço
  • Corinne Cruaud
  • Alexandre Hassanin
Article

Abstract

Here we study the evolution of nucleotide composition in third codon-positions of CO1 sequences of Chelicerata, using a phylogenetic framework, based on 180 taxa and three markers (CO1, 18S, and 28S rRNA; 5,218 nt). The analyses of nucleotide composition were also extended to all CO1 sequences of Chelicerata found in GenBank (1,701 taxa). The results show that most species of Chelicerata have a positive strand bias in CO1, i.e., in favor of C nucleotides, including all Amblypygi, Palpigradi, Ricinulei, Solifugae, Uropygi, and Xiphosura. However, several taxa show a negative strand bias, i.e., in favor of G nucleotides: all Scorpiones, Opisthothelae spiders and several taxa within Acari, Opiliones, Pseudoscorpiones, and Pycnogonida. Several reversals of strand-specific bias can be attributed to either a rearrangement of the control region or an inversion of a fragment containing the CO1 gene. Key taxa for which sequencing of complete mitochondrial genomes will be necessary to determine the origin and nature of mtDNA rearrangements involved in the reversals are identified. Acari, Opiliones, Pseudoscorpiones, and Pycnogonida were found to show a strong variability in nucleotide composition. In addition, both mitochondrial and nuclear genomes have been affected by higher substitution rates in Acari and Pseudoscorpiones. The results therefore indicate that these two orders are more liable to fix mutations of all types, including base substitutions, indels, and genomic rearrangements.

Keywords

Chelicerata Mitochondrial genome Strand bias Rearrangements Inversion Control region Phylogeny 

Notes

Acknowledgments

We are grateful to the following colleagues who kindly provided samples and/or contributed to chelicerate identification: Michel Baylac, Michel Bertrand, Renaud Boistel, Magalie Castelin, Régis Cleva, Cyrille d’Haese, Arnaud Faille, Reinhard Gerecke, Clément Gilbert, Pedroso Giupponi, Ton van Haaren, Céline Houssin, Michaël Manuel, Patrick Maréchal, Bertrand Margat, Aurélien Miralles, Piotr Naskrecki, Eric Ollivier, Eric Quéinnec, Christine Rollard, Anne Ropiquet, Harry Smit, Christian Vanderbergh and Peter Weygoldt. We also thank members of the “Groupe d’Etude des Arachnides”, directed by Olivier Dupont, for their contribution to the sampling. This work was supported by the MNHN programs “Etat et Structure de la Biodiversité Actuelle et Fossile” and “Cordillère Annamitique”, and the “Consortium National de Recherche en Génomique”. It forms part of agreement no. 2005/67 between the Genoscope and the MNHN on the project “Macrophylogeny of life”, directed by Guillaume Lecointre.

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

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References

  1. Arabi J, Cruaud C, Couloux A, Hassanin A (2010) Studying sources of incongruence in arthropod molecular phylogenies: sea spiders (Pycnogonida) as a case study. CR Biol 333:438–453. doi:10.1016/j.crvi.2010.01.018 CrossRefGoogle Scholar
  2. Arango CP, Wheeler WC (2007) Phylogeny of the sea spider (Arthropoda, Pycnogonida) based on direct optimization of six loci and morphology. Cladistics 23:255–293. doi:10.1111/j.1096-0031.2007.00143.x CrossRefGoogle Scholar
  3. Black WC, Roehrdanz RL (1998) Mitochondrial gene order is not conserved in arthropods: prostriate and metastriate tick mitochondrial genomes. Mol Biol Evol 15:1772–1785PubMedGoogle Scholar
  4. Brown TA, Clayton DA (2006) Genesis and wandering: origins and migrations in asymmetrically replicating mitochondrial DNA. Cell Cycle 5:917–921. doi:10.4161/cc.5.9.2710 PubMedCrossRefGoogle Scholar
  5. Brusca RC, Brusca GJ (2003) Invertebrates, 2nd edn. Sinauer Press, SunderlandGoogle Scholar
  6. Cameron LS, Johnson K, Whiting M (2007) The mitochondrial genome of the screamer louse Bothriometopus (Phthiraptera: Ischnocera): effects of extensive gene rearrangements on the evolution of the genome. J Mol Evol 65:589–604. doi:10.1007/s00239-007-9042-8 PubMedCrossRefGoogle Scholar
  7. Chiu HMC, Morton B (2003) The morphological differentiation of two horseshoe crab species, Tachypleus tridentatus and Carcinoscorpius rotundicauda (Xiphosura), in Hong Kong with a regional Asian comparison. J Nat Hist 37:2369–2382. doi:10.1080/00222930210149753 CrossRefGoogle Scholar
  8. Coddington JA, Giribet G, Harvey MS, Prendini L, Walter DE (2004) Arachnida. In: Cracraft J, Donoghue MJ (eds) Assembling the tree of life. Oxford University Press, Oxford, pp 296–318Google Scholar
  9. Dabert M, Witalinski W, Kazmierski A, Olszanowski Z, Dabert J (2010) Molecular phylogeny of acariform mites (Acari, Arachnida): strong conflict between phylogenetic signal and long-branch attraction artifacts. Mol Phylogenet Evol 56:222–241. doi:10.1016/j.ympev.2009.12.020 PubMedCrossRefGoogle Scholar
  10. Dermauw W, Van Leeuwen T, Vanholme B, Tirry L (2009). The complete mitochondrial genome of the house dust mite Dermatophagoides pteronyssinus (Trouessart): a novel gene arrangement among arthropods. BMC Genomics. doi:10.1186/1471-2164-10-107
  11. Dermauw W, Vanholme B, Tirry L, Van Leeuwen T (2010) Mitochondrial genome analysis of the predatory mite Phytoseiulus persimilis and a revisit of the Metaseiulus occidentalis mitochondrial genome. Genome 53:285–301. doi:10.1139/G10-004 PubMedCrossRefGoogle Scholar
  12. Dietz L, Mayer C, Arango C, Leese F (2011) The mitochondrial genome of Colossendeis megalonyx supports a basal position of Colossendeidae within the Pycnogonida. Mol Phylogenet Evol 58:553–558. doi:10.1016/j.ympev.2010.12.016 PubMedCrossRefGoogle Scholar
  13. Domes K, Maraun M, Scheu S, Cameron SL (2008) The complete mitochondrial genome of the sexual oribatid mite Steganacarus magnus: genome rearrangements and loss of tRNAs. BMC Genomics. doi:10.1186/1471-2164-9-532
  14. Dunlop JA (2010) Geological history and phylogeny of Chelicerata. Arthropod Struc Dev 39:124–142. doi:10.1016/j.asd.2010.01.003 CrossRefGoogle Scholar
  15. Ernsting BR, Edwards DD, Aldred KJ, Fites JS, Neff CR (2009) Mitochondrial genome sequence of Unionicola foili (Acari: Unionicolidae): a unique order with implications for phylogenetic inference. Exp Appl Acarol 49:305–316. doi:10.1007/s10493-009-9263-1 PubMedCrossRefGoogle Scholar
  16. Fahrein K, Masta SE, Podsiadlowski L (2009) The first complete mitochondrial genome sequences of Amblypygi (Chelicerata: Arachnida) reveal conservation of the ancestral arthropod gene order. Genome 52:456–466. doi:10.1139/G09-023 PubMedCrossRefGoogle Scholar
  17. Fonseca MM, Posada D, Harris DJ (2008) Inverted replication of vertebrate mitochondria. Mol Biol Evol 25:805–808. doi:10.1093/molbev/msn050 PubMedCrossRefGoogle Scholar
  18. Fontanillas E, Welch JJ, Thomas JA, Bromham L (2007) The influence of body size and diversification rate on molecular evolution during the Cambrian explosion of animal phyla. BMC Evol Biol. doi:10.1186/1471-2148-7-95
  19. Gillooly JF, McCoy MW, Allen AP (2007) Effects of metabolic rate on protein evolution. Biol Lett 3:655–659. doi:10.1098/rsbl.2007.0403 PubMedCrossRefGoogle Scholar
  20. Gissi C, Iannelli F, Pesole G (2008) Evolution of the mitochondrial genome of Metazoa as exemplified by comparison of congeneric species. Heredity 101:301–320. doi:10.1038/hdy.2008.62 PubMedCrossRefGoogle Scholar
  21. Glazier DS (2008) Effects of metabolic level on the body size scaling of metabolic rate in birds and mammals. Proc R Soc B 275:1405–1410. doi:10.1098/rspb.2008.0118 PubMedCrossRefGoogle Scholar
  22. Goddard JM, Wolstenholme DR (1978) Origin and direction of replication in mitochondrial DNA molecules from Drosophila melanogaster. Proc Natl Acad Sci USA 75:3886–3890PubMedCrossRefGoogle Scholar
  23. Goddard JM, Wolstenholme DR (1980) Origin and direction of replication in mitochondrial DNA molecules from the genus Drosophila. Nucleic Acids Res 8:741–757PubMedGoogle Scholar
  24. Harvey MS (1992) The phylogeny and classification of the Pseudoscorpionida (Chelicerata: Arachnida). Invertebr Taxon 6:1373–1435. doi:10.1071/IT9921373 CrossRefGoogle Scholar
  25. Harvey MS (2007) The smaller arachnid orders: diversity, descriptions and distributions from Linnaeus to the present (1758 to 2007). Zootaxa 1668:363–380Google Scholar
  26. Hassanin A (2006) Phylogeny of Arthropoda inferred from mitochondrial sequences: strategies for limiting the misleading effects of multiple changes in pattern and rates of substitution. Mol Phylogenet Evol 38:100–116. doi:10.1016/j.ympev.2005.09.012 PubMedCrossRefGoogle Scholar
  27. Hassanin A, Léger N, Deutsch J (2005) Evidence for multiple reversals of asymmetric mutational constraints during the evolution of the mitochondrial genome of Metazoa, and consequences for the phylogenetic inferences. Syst Biol 54:277–298. doi:10.1080/10635150590947843 PubMedCrossRefGoogle Scholar
  28. Hebert PD, Cywinska A, Ball SL, deWaard JR (2003) Biological identifications through DNA barcodes. Proc R Soc Lond B 270:313–321. doi:10.1098/rspb.2002.2218 CrossRefGoogle Scholar
  29. Kury AB (2010) Classification of Opiliones. National Museum, Rio. http://www.museunacional.ufrj.br/mndi/Aracnologia/opiliones.html. Accessed December 2010
  30. Lourenço WR (2007) First record of the family Pseudochactidae Gromov (Chelicerata, Scorpiones) from Laos and new biogeographic evidence of a Pangaean paleodistribution. CR Biol 330:770–777. doi:10.1016/j.crvi.2007.07.006 CrossRefGoogle Scholar
  31. Lourenço WR, Gall JC (2004) Fossil scorpions from the Buntsandstein (Early Triassic) of France. CR Palevol 3:369–378. doi:10.1016/j.crpv.2004.06.006 CrossRefGoogle Scholar
  32. Mallatt J, Giribet G (2006) Further use of nearly complete 28S and 18S rRNA genes to classify Ecdysozoa: 37 more arthropods and a kinorhynch. Mol Phylogenet Evol 40:772–794. doi:10.1016/j.ympev.2006.04.021 PubMedCrossRefGoogle Scholar
  33. Masta SE, Longhorn SJ, Boore JL (2009) Arachnid relationships based on mitochondrial genomes: asymmetric nucleotide and amino acid bias affects phylogenetic analyses. Mol Phylogenet Evol 50:117–128. doi:10.1016/j.ympev.2008.10.010 PubMedCrossRefGoogle Scholar
  34. Masta SE, McCall A, Longhorn SJ (2010) Rare genomic changes and mitochondrial sequences provide independent support for congruent relationships among sea spiders (Arthropoda, Pycnogonida). Mol Phylogenet Evol 57:59–70. doi:10.1016/j.ympev.2010.06.020 PubMedCrossRefGoogle Scholar
  35. Murienne J, Harvey MS, Giribet G (2008) First molecular phylogeny of the major clades of Pseudoscorpiones (Arthropoda: Chelicerata). Mol Phylogenet Evol 49:170–184. doi:10.1016/j.ympev.2008.06.002 PubMedCrossRefGoogle Scholar
  36. Naskrecki P (2008) A new ricinuleid of the genus Ricinoides Ewing (Arachnida, Ricinulei) from Ghana. Zootaxa 1698:57–64Google Scholar
  37. Park SJ, Lee YS. Hwang UW (2007) The complete mitochondrial genome of the sea spider Achelia bituberculata (Pycnogonida, Ammotheidae): arthropod ground pattern of gene arrangement. BMC Genomics. doi:10.1186/1471-2164-8-343
  38. Pepato AR, da Rocha CEF, Dunlop JA (2010) Phylogenetic position of the acariform mites: sensitivity to homology assessment under total evidence. BMC Evol Biol. doi:10.1186/1471-2148-10-235
  39. Perna NT, Kocher TD (1995) Patterns of nucleotide composition at fourfold degenerate sites of animal mitochondrial genomes. J Mol Evol 41:353–358. doi:10.1007/BF01215182 PubMedCrossRefGoogle Scholar
  40. Pinto-da-Rocha R, Machado G, Giribet G (2007) Harvestmen: the biology of Opiliones. Harvard University Press, CambridgeGoogle Scholar
  41. Platnick NI (2011) The world spider catalog, version 11.5. The American Museum of Natural History. http://research.amnh.org/iz/spiders/catalog/. Accessed January 2011
  42. Podsiadlowski L, Braband A (2006) The complete mitochondrial genome of the sea spider Nymphon gracile (Arthropoda: Pycnogonida). BMC Genomics. doi:10.1186/1471-2164-7-284
  43. Ratnasingham S, Hebert PD (2007) Bold: the Barcode of Life Data System. Mol Ecol Notes 7:355–364. doi:10.1111/j.1471-8286.2007.01678.x. http://www.barcodinglife.org Google Scholar
  44. Regier JC, Shultz JW, Zwick A, Hussey A, Ball B, Wetzer R, Martin JW, Cunningham CW (2010) Arthropod relationships revealed by phylogenomic analysis of nuclear protein-coding sequences. Nature 25:1079–1083. doi:10.1038/nature08742 CrossRefGoogle Scholar
  45. Reyes A, Gissi C, Pesole G, Saccone C (1998) Asymmetrical directional mutation pressure in the mitochondrial genome of mammals. Mol Biol Evol 15:957–966PubMedGoogle Scholar
  46. Roberti M, Bruni F, Polosa PL, Gadaleta MN, Cantatore P (2006) The Drosophila termination factor DmTTF regulates in vivo mitochondrial transcription. Nucleic Acids Res 34:2109–2116. doi:10.1093/nar/gkl181 PubMedCrossRefGoogle Scholar
  47. Saito S, Tamura K, Aotsuka T (2005) Replication origin of mitochondrial DNA in insects. Genetics 171:1695–1705. doi:10.1534/genetics.105.046243 PubMedCrossRefGoogle Scholar
  48. Shao R, Dowton M, Murrell A, Barker SC (2003) Rates of gene rearrangement and nucleotide substitution are correlated in the mitochondrial genome of insects. Mol Biol Evol 20:1612–1619. doi:10.1093/molbev/msg176 PubMedCrossRefGoogle Scholar
  49. Shao R, Barker SC, Mitani H, Aoki Y, Fukunaga M (2005) Evolution of duplicate control regions in the mitochondrial genomes of Metazoa: a case study with Australian Ixodes ticks. Mol Biol Evol 22:620–629. doi:10.1093/molbev/msi047 PubMedCrossRefGoogle Scholar
  50. Shao R, Barker SC, Mitani H, Takahashi M, Fukunaga M (2006) Molecular mechanisms for the variation of the mitochondrial gene content and gene arrangement among chigger mites of the genus Leptotrombidium (Acari: Acariformes). J Mol Evol 63:251. doi:10.1007/s00239-005-0196-y PubMedCrossRefGoogle Scholar
  51. Shultz JW (1990) Evolutionary morphology and phylogeny of Arachnida. Cladistics 6:1–31. doi:10.1111/j.1096-0031.1990.tb00523.x CrossRefGoogle Scholar
  52. Shultz JW (2007) A phylogenetic analysis of the arachnid orders based on morphological characters. Zool J Linn Soc 150:221–265. doi:10.1111/j.1096-3642.2007.00284.x CrossRefGoogle Scholar
  53. Soleglad ME, Fet V (2003) High-level systematics and phylogeny of the extant scorpions (Scorpiones: Orthosterni). Euscorpius 11:1–175Google Scholar
  54. Stamatakis A (2006) RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22:2688–2690. doi:10.1093/bioinformatics/btl446 PubMedCrossRefGoogle Scholar
  55. Staton JL, Daehler LL, Brown WM (1997) Mitochondrial gene arrangement of the horseshoe crab Limulus polyphemus L.: conservation of major features among arthropod classes. Mol Biol Evol 14:867–874PubMedGoogle Scholar
  56. Taanman JW (1999) The mitochondrial genome: structure, transcription, translation and replication. Biochim Biophys Acta 1410:103–123. doi:10.1016/S0005-2728(98)00161-3 PubMedCrossRefGoogle Scholar
  57. Tanaka M, Ozawa T (1994) Strand asymmetry in human mitochondrial DNA mutations. Genomics 22:327–335. doi:10.1006/geno.1994.1391 PubMedCrossRefGoogle Scholar
  58. Villarreal-Manzanilla O, Giupponi APL, Tourinho AL (2008) New Venezuelan genus of Hubardiidae (Arachnida: Schizomida). Zootaxa 1860:60–68Google Scholar
  59. Welch JJ, Bininda-Emonds OR, Bromham L (2008) Correlates of substitution rate variation in mammalian protein-coding sequences. BMC Evol Biol 8:53PubMedCrossRefGoogle Scholar
  60. Weygoldt P (1971) Vergleichend-embryologische Untersuchungen an Pseudoscorpionen V. Das Embryonalstadium mit seinem Pumporgan bei verschiedenen Arten und sein Wert als taxonomisches Merkmal. Z Zool Syst Evolut Forsch 9:3–29CrossRefGoogle Scholar
  61. Weygoldt P, Paulus HF (1979) Untersuchungen zur morphologie, taxonomie und phylogenie der Chelicerata. Z Zool Syst Evolut Forsch 17(85–116):177–200Google Scholar
  62. Xu W, Jameson D, Tang B, Higgs PG (2006) The relationship between the rate of molecular evolution and the rate of genome rearrangement in animal mitochondrial genomes. J Mol Evol 63:375–392. doi:10.1007/s00239-005-0246-5 PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2012

Authors and Affiliations

  • Juliette Arabi
    • 1
    • 2
  • Mark L. I. Judson
    • 1
  • Louis Deharveng
    • 1
  • Wilson R. Lourenço
    • 1
  • Corinne Cruaud
    • 3
  • Alexandre Hassanin
    • 1
    • 2
  1. 1.Département Systématique et Evolution, UMR 7205, Origine, Structure et Evolution de la BiodiversitéMuséum national d’Histoire naturelleParisFrance
  2. 2.Département Systématique et Evolution, Service de Systématique MoléculaireMuséum national d’Histoire naturelleParisFrance
  3. 3.Centre National de SéquençageGenoscopeEvry CedexFrance

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