Experimental & Applied Acarology

, Volume 33, Issue 3, pp 183–201 | Cite as

Molecular phylogeny of oribatid mites (Oribatida, Acari): evidence for multiple radiations of parthenogenetic lineages

  • Mark Maraun
  • Michael Heethoff
  • Katja Schneider
  • Stefan Scheu
  • Gerd Weigmann
  • Jennifer Cianciolo
  • Richard H. Thomas
  • Roy A. Norton


Nucleotide sequences of the D3 expansion segment and its flanking regions of the 28S rDNA gene were used to evaluate phylogenetic relationships among representative sexual and asexual oribatid mites (Oribatida, Acariformes). The aim of this study was to investigate the hypothesis that oribatid mites consist of species rich clusters of asexual species that may have radiated while being parthenogenetic. Furthermore, the systematic position of the astigmate mites (Astigmata, Acariformes) which have been hypothesised to represent a paedomorphic lineage within the oribatid mites, is investigated. This is the first phylogenetic tree for oribatid mites s.1. (incl. Astigmata) based on nucleotide sequences. Intraspecific genetic variation in the D3 region was very low, confirming the hypothesis that this region is a good species marker. Results from neighbour joining (NJ) and maximum parsimony (MP) algorithms indicate that several species rich parthenogenetic groups like Camisiidae, Nanhermanniidae and Malaconothridae are monophyletic, consistent with the hypothesis that some oribatid mite groups diversified despite being parthenogenetic. The MP and maximum likelihood (ML) method indicated that the D3 region is a good tool for elucidating the relationship of oribatid mite species on a small scale (genera, families) but is not reliable for large scale taxonomy because branches from the NJ algorithm collapsed in the MP and ML tree. In all trees calculated by different algorithms the Astigmata clustered within the oribatid mites, as proposed earlier.

Acari Ancient asexuals Astigmata D3 region Oribatida Parthenogenesis Radiation 28S rRNA 


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  1. Alberti G., Norton R.A. and Kasbohm J. 2001. Fine structure and mineralisation of cuticle in Enarthronota and Lohmannioidea (Acari: Oribatida). In: Halliday R.B., Walter D.E., Proctor H.C., Norton R.A., Colloff M.J. (eds) Acarology: Proceedings of the 10th International Congress. CSIRO Publishing, Melbourne, Australia, pp. 230–241.Google Scholar
  2. Arkhipova I. and Meselson M. 2000. Transposable elements in sexual and ancient asexual taxa. Proc. Nat. Acad. Sci. USA 97: 14473–14477.Google Scholar
  3. Bell G. 1982. The Masterpiece of Nature. The Evolution and Genetics of Sexuality. University of California Press, California, USA.Google Scholar
  4. Butlin R., Schön I. and Martens K. 1998. Asexual reproduction in non-marine ostracods. Heredity 81: 473–480.Google Scholar
  5. Carta L.K., Skantar A.M. and Handoo Z.A. 2001. Molecular, morphological and thermal characters of 19 Pratylenchus spp. and relatives using the D3 segment of the nuclear LSU rRNA gene. Nematropica 31: 195–209.Google Scholar
  6. Crow J.F. 1994. Advantages of sexual reproduction. Dev. Gen. 15: 205–213.Google Scholar
  7. Cruickshank R.H. 2002. Molecular markers for the phylogenetics of mites and ticks. Syst. Appl. Acarol. 7: 3–14.Google Scholar
  8. Cruickshank R.H. and Thomas R.H. 1999. Evolution of haplodiploidy in dermanyssine mites (Acari: Mesostigmata). Evolution 53: 1796–1803.Google Scholar
  9. Ghiselin M.T. 1974. The Economy of Nature and the Evolution of Sex. University of California Press, California, USA.Google Scholar
  10. Giribet G., Carranza S., Riutort M., Baguna J. and Ribeira C. 1999a. Internal phylogeny of the Chilopoda (Myriapoda, Arthropoda) using complete 18S rDNA and partial 28S rDNA sequences. Phil. Trans. Roy. Soc. Lond. Ser. B 354: 215–222.Google Scholar
  11. Giribet G., Rambla M., Carranza S., Baguna J., Riutort M. and Ribeira C. 1999b. Phylogeny of the arachnid order opiliones (Arthropoda) inferred from a combined approach of complete 18S and partial 28S ribosomal DNA sequences and morphology. Mol. Phyl. Evol. 11: 296–307.Google Scholar
  12. Grandjean F. 1937. Sur quelques charactères des Acaridiae libres. Bull. Soc. Zool. France 62: 388–398.Google Scholar
  13. Grandjean F. 1953. Essai de classification des Oribates (Acariens). Bull. Soc. Zool. France 78: 421–446.Google Scholar
  14. Grandjean F. 1965. Complément a mon travail de 1953 sur la classification des oribates. Acarologia 7: 713–734.Google Scholar
  15. Grandjean F. 1969. Considérations sur le classement des oribates: leur division en 6 groupes majeurs. Acarologia 11: 127–153.Google Scholar
  16. Hamilton W.D. 1980. Sex versus non-sex versus parasite. Oikos 35: 282–290.Google Scholar
  17. Hammer M. and Wallwork J.A. 1979. A review of the world distribution of oribatid mites (Acari: Cryptostigmata) in relation to continental drift. Biol. Skr. Dan. Vid. Selsk. 22: 1–31.Google Scholar
  18. Haumann G. 1991. Zur Phylogenie primitiver Oribatiden (Acari: Oribatida). Verlag Technische Universität, Graz, Austria.Google Scholar
  19. Judson P.O. and Normark B.B. 1996. Ancient asexual scandals. Trends Ecol. Evol. 11: 41–46.Google Scholar
  20. Knülle W. 1957. Morphologische und entwicklungsgeschichtliche Untersuchungen zum phylogenetischen System der Acari: Acariformes Zachv. I. Oribatei: Malaconothridae. Mitt. Zool. Mus. Berlin 33: 97–213.Google Scholar
  21. Kondrashov A.S. 1993. Classification of hypotheses on the advantage of amphimixis. J. Hered. 84: 372–387.Google Scholar
  22. Litvaitis M.K., Nunn G., Thomas W.K. and Kocher T.D. 1994. A molecular approach for the identification of meiofaunal turbellarians (Platyhelminthes, Turbellaria). Mar. Biol. 120: 437–442.Google Scholar
  23. Litvaitis M.K., Bates J.W., Hope W.D. and Moens T. 2000. Inferring a classification of the Adenophorea (Nematoda) from nucleotide sequences of the D3 expansion segment (26?28S rDNA). Can. J. Zool. 78: 911–922.Google Scholar
  24. Maraun M. and Scheu S. 2000. The structure of oribatid mite communities (Acari, Oribatida): patterns, mechanisms and implications for future research. Ecography 23: 374–383.Google Scholar
  25. Maraun M., Heethoff M., Scheu S., Norton R.A., Weigmann G. and Thomas R.H. 2003. Radiation in sexual and parthenogenetic oribatid mites (Oribatida, Acari) as indicated by genetic divergence of closely related species. Exp. Appl. Acarol. 29: 175–187.Google Scholar
  26. Maynard Smith J. 1978. The Evolution of Sex. Cambridge University Press, Cambridge.Google Scholar
  27. McLain D.K., Li J. and Oliver J.H. 2001. Interspecific and geographical variation in the sequence of rDNA expansion segment D3 of Ixodes ticks (Acari, Ixodidae). Heredity 86: 234–242.Google Scholar
  28. Muller H.J. 1964. The relation of recombination to mutational advance. Mut. Res. 1: 2–9.Google Scholar
  29. Norton R.A. 1998. Morphological evidence for the evolutionary origin of Astigmata (Acari, Acariformes). Exp. App. Acarol. 22: 559–594.Google Scholar
  30. Norton R.A. 2001. Systematic relationships of Nothrolohmanniidae, and the evolutionary plasticity of body forms in Enarthronota (Acari. Oribatida). In: Halliday R.B., Walter D.E., Proctor H.C., Norton R.A., Colloff M.J. (eds) Acarology: Proceedings of the 10th International Congress. CSIRO Publishing, Melbourne, Australia, pp. 58–75.Google Scholar
  31. Norton R.A. and Metz L. 1980. Nehypochthoniidae (Acari: Oribatei), a new family from the southeastern United States. Ann. Entom. Soc. Am. 73: 54–62.Google Scholar
  32. Norton R.A. and Palmer S.C. 1991. The distribution, mechanisms, and evolutionary significance of parthenogenesis in oribatid mites. In: Schuster R. and Murphy P.W. (eds) The Acari: Reproduction, Development and Life-history Strategies. Chapman and Hall, London, pp. 107–136.Google Scholar
  33. Norton R.A., Bonamo P.M., Grierson J.D. and Shear W.A. 1988. Oribatid mite fossils from a terrestrial Devonian deposit near Gilboa, New York. J. Paleont. 62: 259–269.Google Scholar
  34. Norton R.A., Kethley J.B., Johnston D.E. and OConnor B.M. 1993. Phylogenetic perspectives on genetic systems and reproductive modes of mites. In: Wrensch D.L. and Ebbert M.A. (eds) Evolution and Diversity of Sex Ratios. Chapman and Hall, New York, pp. 8–99.Google Scholar
  35. OConnor B.M. 1984. Phylogenetic relationships among higher taxa in the Acariformes, with particular reference to the Astigmata. In: Griffith D.A. and Bowman C.E. (eds) Acarology VI, Vol. 1. Ellis Horwood Ltd, Chichester, UK, pp. 19–27.Google Scholar
  36. Okabe K. and OConnor B.M. 2001. Thelytokous reproduction in the family Acaridae (Astigmata). In: Halliday R.B., Walter D.E., Proctor H.C., Norton R.A. and Colloff M.J. (eds) Acarology: Proceedings of the 10th International Congress. CSIRO Publishing, Melbourne, Australia, pp. 170–175.Google Scholar
  37. Olson P.D., Littlewood D.T.J., Bray R.A. and Mariaux J. 2001. Interrelationships and evolution of the tapeworms (Plathyhelminthes: Cestoda). Mol. Phyl. Evol. 19: 443–467.Google Scholar
  38. Posada D. and Crandall K.A. 1998. Modeltest: testing the model of DNA substitution. Bioinformatics 14: 817–818.Google Scholar
  39. Saitou N. and Nei M. 1987. The neighbor-joining method — a new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 4: 406–425.Google Scholar
  40. Sakata T. and Norton R.A. 2001. Opisthonotal gland chemistry of early-derivative oribatid mites (Acari) and its relevance to systematic relationships of Astigmata. Int. J. Acarol. 27: 281–291.Google Scholar
  41. Schatz H. 2002. Die Oribatidenliteratur und die beschriebenen Oribatidenarten (1758-2001) — eine Analyse. Abh. Ber. Naturkundemus. Görlitz 74: 37–45.Google Scholar
  42. Schluter D. 2000. The Ecology of Adaptive Radiation. Oxford University Press, Oxford.Google Scholar
  43. Schön I. and Butlin R.K. 1998. Genetic diversity and molecular phylogeny. In: Martens K. (ed) Sex and Parthenogenesis. Evolutionary Ecology of Reproductive Modes in Non-marine Ostracods. Backhuys Publishers, Leiden, The Netherlands, pp. 275–293.Google Scholar
  44. Shear W.A., Bonamo M., Grierson J.D., Rolfe W.D.I., Smith E.L. and Norton R.A. 1984. Early land animals in North America: evidence from Devonian age arthropods from Gilboa, New York. Science 224: 492–494.Google Scholar
  45. Simmons M.P., Savolainen V., Clevinger C.C., Archer R.H. and Davis J.I. 2001. Phylogeny of the Celastraceae inferred from 26S nuclear ribosomal DNA, phytochrom B, rbcL, atpB, and morphology. Mol. Phyl. Evol. 19: 353–366.Google Scholar
  46. Suomalainen E., Saura A. and Lokki J. 1987. Cytology and Evolution in Parthenogenesis. CRC Press Inc, Boca Raton, Florida, USA.Google Scholar
  47. Swofford D. 1999. PAUP*: Phylogenetic Analysis Using Parsimony (and other methods). Version 4.0. Sinauer Associates, Sunderland, Mass, USA.Google Scholar
  48. Taberly G. 1987a. Recherches sur la parthénogenèse thélytoque de deux espèces d'acariens oribatides: Trhypochthonius tectorum (Berlese) et Platynothrus peltifer (Koch). II: Étude anatomique, histologique et cytologique des femelles parthénogénétiques. 1re partie. Acarologia 28: 285–293.Google Scholar
  49. Taberly G. 1987b. Recherches sur la parthénogenèse thélytoque de deux espèces d'acariens oribatides: Trhypochthonius tectorum (Berlese) et Platynothrus peltifer (Koch). III: Étude anatomique, histologique et cytologique des femelles parthénogenétiques. 2eme partie. Acarologia 28: 389–403.Google Scholar
  50. Thompson J.D., Higgins D.G. and Gibson T.J. 1994. CLUSTAL W: improving the sensitivity of progressive multiple alignment through sequence weighting, position specific gap penalties and weight matrix choice. Nucl. Acids Res. 22: 4673–4680.Google Scholar
  51. Thompson J.D., Gibson T.J., Plewniak F., Jeanmougin F. and Higgins D.G. 1997. The ClustalX windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucl. Acids Res. 24: 4876–4882.Google Scholar
  52. Travé J., André H.M., Taberly G. and Bernini F. 1996. Les Acariens Oribates. Éditions AGAR and SIALF, Belgium.Google Scholar
  53. Van Valen L.M. 1973. A new evolutionary law. Evol. Theory 1: 1–30.Google Scholar
  54. Walter D.E. and Proctor H.C. 1999. Mites. Ecology, Evolution and Behaviour. CABI Publishing, Sydney, Australia.Google Scholar
  55. Weeks S.C. 1993. The effects of recurrent clonal formation on clonal invasion patterns and sexual persistence — a Monte-Carlo simulation of the frozen niche-variation model. Am. Nat. 141: 409–427.Google Scholar
  56. Weigmann G. 1996. Hypostome morphology of Malaconothridae and phylogenetic conclusions on primitive Oribatida. In: Mitchell R., Horn D.J., Needham G.J., Welbourn W.C. (eds) Acarology IX, Vol. 1, Proceedings, Ohio Biological Survey, Columbus, Ohio, USA, pp. 273–276.Google Scholar
  57. Welsh D.M. and Meselson M. 2000. Evidence for the evolution of bdelloid rotifers without sexual reproduction or genetic exchange. Science 288: 1211–1215.Google Scholar
  58. Wheeler W.C. and Hayashi C.Y. 1998. The phylogeny of the extant chelicerate orders. Cladistics 14: 173–192.Google Scholar
  59. Whiting M.F., Carpenter J.C., Wheeler Q.D. and Wheeler W.C. 1997. The strepsiptera problem: phylogeny of the holometabolous insect orders inferred from 18S and 28S ribosomal DNA sequences and morphology. Syst. Biol. 46: 1–68.Google Scholar
  60. Woas S. 1990. Die phylogenetische Entwicklungslinien der Höheren Oribatiden (Acari). I. Zur Monophylie der Poronota Grandjean, 1953. Andrias 7: 91–168.Google Scholar
  61. Woas S. 2002. Acari: Oribatida. In: Adis J. (ed) Amazonian Arachnida and Myriapoda. Pensoft Publishers. Sofia, Bulgaria, pp. 21–291.Google Scholar
  62. Wrensch D.L., Kethley J.B. and Norton R.A. 1994. Cytogenetics of holokinetic chromosomes and inverted meiosis: keys to the evolutionary success of mites, with generalizations on eukaryotes. In: Houck M.A. (ed) Mites: Ecological and Evolutionary Analyses of Life-History Pattern. Chapman and Hall, New York, pp. 282–343.Google Scholar
  63. Zachvatkin A.A. 1953. [Studies on the morphology and postembryonic development of tyroglyphids (Sarcoptiformes, Tyroglyphoidea).] In: Smirnov E.S. and Dubinin V.B. (eds) A.A. Zachvatkin, Collected Scientific Works. Moscow State University Publishing House, Moscow pp. 19–120. (in Russian).Google Scholar
  64. Zuker M., Mathews D.H. and Turner D.H. 1999. Alogorithms and thermodynamics for RNA secondary structure prediction: a practical guide. In: Barciszewski J. and Clark B.F.C. (eds) RNA Biochemistry and Biotechnology. NATO ASI Series, Kluwer Academic Publishers, The Netherlands.Google Scholar

Copyright information

© Kluwer Academic Publishers 2004

Authors and Affiliations

  • Mark Maraun
    • 1
  • Michael Heethoff
    • 1
  • Katja Schneider
    • 1
  • Stefan Scheu
    • 1
  • Gerd Weigmann
    • 2
  • Jennifer Cianciolo
    • 3
  • Richard H. Thomas
    • 4
  • Roy A. Norton
    • 5
  1. 1.Institut für ZoologieTechnische Universität DarmstadtDarmstadtGermany
  2. 2.Institut für Bodenzoologie und ÖkologieFreie Universität BerlinBerlinGermany
  3. 3.Department of Evolution, Ecology and BehaviourIndiana UniversityBloomingtonUSA
  4. 4.Department of ZoologyThe Natural History Museum LondonLondonUK
  5. 5.Faculty of Environmental and Forest Biology, College of Environmental Science and ForestryState University of New YorkSyracuseUSA

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