Skip to main content
SpringerLink
Log in

The phylogenetic relationship between Astigmata and Oribatida (Acari) as indicated by molecular markers

  • Published:
Experimental and Applied Acarology Aims and scope Submit manuscript

Abstract

Astigmata comprise a diverse group of acariform mite species with a remarkable range of life histories, most of which involve parasitic or commensal relationships with other organisms. Several authors have suggested that Astigmata evolved as a paedomorphic clade from within Oribatida, and both morphology and gland-chemistry strongly suggest that their sister-clade is within the oribatid subgroup Desmonomata. The biologies of these groups contrast greatly, since oribatid mites are mostly soil-living detritivores and fungivores, and have life cycles that are much longer than those in Astigmata. We tested the hypothesis that Astigmata evolved from within Desmonomata using two molecular markers, the ribosomal 18S region (18S) and the nuclear elongation factor 1 alpha (ef1α) gene. Representative acariform mites included 28 species of Oribatida, eight of Astigmata, two of Prostigmata and two of Endeostigmata; outgroups included members of Opilioacariformes, Parasitiformes and Ricinulei. To minimize the possibility of long-branch attraction artifacts, we limited highly variable sites by removing gaps (18S) and third codon positions (ef1α) from the sequences. Maximum parsimony, neighbor-joining and Bayesian algorithms formed trees that consistently placed Astigmata outside monophyletic Oribatida, usually as sister-group of the endeostigmatid mite Alicorhagia sp. Analyses with and without outgroups resulted in similar topologies, showing no evidence for long-branch artifacts and leaving the conflict with morphological and biochemical data unexplained.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Alberti G (1991) On sperm ultrastructure and systematics of Arachnida with special emphasis on Araneae and Acari. In: Baccetti B (ed) VI Intern congr spermatology: comparative spermatology 20 years after, Siena 1990. Serono Symp Publ Raven Press, Vol 75, pp 929–936

  • Behan-Pelletier VM (1999) Oribatid mite biodiversity in agroecosystems: role for bioindication. Agri Eco Environ 74:411–423

    Article  Google Scholar 

  • Bergsten J (2005) A review of long-branch attraction. Cladistics 21:163–193

    Article  Google Scholar 

  • Berlese A (1897) Acari, Myriapoda et Scorpiones hucusque in Italia reperta. Ordo Cryptostigmata (Sarcoptidae). Portici

  • Boore JL, Brown WM (2000) Mitochondrial genomes of Galathealinum, Helobdella, and Platynereis: sequence and gene arrangement comparisons indicate that Pogonophora is not a phylum and Annelida and Arthropoda are not sister taxa. Mol Biol Evol 17:87–106

    PubMed  CAS  Google Scholar 

  • Crossley DA (1977) The roles of terrestrial saprophagous arthropods in forest soils: current status of concepts. In: Mattson WJ (ed) The role of arthropods in forest ecosystems. Springer, Berlin, pp 226–232

    Google Scholar 

  • Danforth BN, Sauquet H, Packer L (1999) Phylogeny of the bee genus Halictus (Hymenoptera: Halictidae) based on parsimon and likelihood analyses of nuclear EF-1α sequence data. Mol Phylogenet Evol 13:605–618

    Article  PubMed  CAS  Google Scholar 

  • Dobson SJ, Barker SC (1999) Phylogeny of the hard ticks (Ixodidae) inferred from 18S rRNA indicates that the genus Aponomma is paraphyletic. Mol Phylogenet Evol 11:288–295

    Article  PubMed  CAS  Google Scholar 

  • Evans GO (1992) Principles of acarology. CAB International, Wallingford

    Google Scholar 

  • Felsenstein J (1978) Cases in which parsimony or compatibility methods will be positively misleading. Syst Zool 27:401–410

    Article  Google Scholar 

  • Grandjean F (1937) Sur quelques caractères des Acaridiae libres. Bull Soc Zool Fr 62:388–398

    Google Scholar 

  • Grandjean F (1953) Essai de classification des Oribates (Acariens). Bull Soc Zool Fr 78:421–446

    Google Scholar 

  • Grandjean F (1969) Considérations sur le classement des Oribates. Leur division en 6 groupes majeurs. Acarologia 11:127–153

    Google Scholar 

  • Halanych KM (2004) The new view of animal phylogeny. Annu Rev Ecol Evol Syst 35:229–256

    Article  Google Scholar 

  • Huelsenbeck JP, Ronquist F (2001) MRBAYES: Bayesian inference of phylogeny. Bioinformatics 17:673–688

    Article  Google Scholar 

  • Jenner RA (2004) Accepting partnership by submission? Morphological phylogenetics in a molecular millennium. Syst Biol 53:333–342

    Article  PubMed  Google Scholar 

  • Klompen H (2000) A preliminary assessment of the utility of elongation factor 1alpha in elucidating relationship among basal Mesostigmata. Exp Appl Acarol 24:805–820

    Article  PubMed  CAS  Google Scholar 

  • Klompen JSH, Black WC Jr, Keirans JE, Norris DE (2000) Systematics and biogeography of hard ticks, a total evidence approach. Cladistics 16:79–102

    Article  Google Scholar 

  • Klompen H, Lekveishvili M, Black WC (2007) Phylogeny of parasitiform mites (Acari) based on rRNA. Mol Phyl Evol 43:936–951

    Article  CAS  Google Scholar 

  • Krantz GW (1960) The Acaridae: a recapitulation. Pan Pacific Entomol 36:157–166

    Google Scholar 

  • Krantz GW (1978) A manual of acarology, 2nd edn. Oregon State University Book Stores, Corvallis

    Google Scholar 

  • Lekveishvili M, Klompen H (2004) Phylogeny of infraorder Sejina (Acari: Mesostigmata). Zootaxa 629:1–19

    Google Scholar 

  • Liana M, Witalinski W (2005) Sperm structure and phylogeny of Astigmata. J Morphol 265:318–324

    Article  PubMed  Google Scholar 

  • Lindquist EE (1976) Transfer of the Tarsocheylidae to the Heterostigmata, and reassignment of the Tarsonemina and Heterostigmata to lower hierarchic status in the Prostigmata (Acari). Can Entomol 10:23–48

    Article  Google Scholar 

  • Maraun M, Heethoff M, Schneider K, Scheu S, Weigmann G, Cianciolo J, Thomas RH, Norton RA (2004) Molecular phylogeny of oribatid mites (Oribatida, Acari): evidence for multiple radiations of parthenogenetic lineages. Exp Appl Acarol 33:183–201

    Article  PubMed  CAS  Google Scholar 

  • Murrell A, Dobson SJ, Walter DE, Campbell NJH, Shao R, Barker SC (2005) Relationships among the three major lineages of the Acari (Arthropoda: Arachnida) inferred from the small subunit rRNA: paraphyly of the Parasitiformes with respect to the Opilioacariformes and relative rates of nucleotide substitution. Invertebr Syst 19:383–389

    Article  CAS  Google Scholar 

  • Norton RA (1994) Evolutionary aspects of oribatid mites life histories and consequences for the origin of the Astigmata. In: Houck MA (ed) Mites: ecological and evolutionary analyses of life-history patterns. Chapman & Hall, New York, pp 99–135

    Google Scholar 

  • Norton RA (1998) Morphological evidence for the evolutionary origin of Astigmata (Acari: Acariformes). Exp Appl Acarol 22:559–594

    Article  Google Scholar 

  • Norton RA (2007) Holistic acarology and ultimate causes: examples from the oribatid mites. In: Morales-Malacara JB, Behan-Pelletier V, Ueckermann E, Pérez TM, Estrada-Nenegas EG and Badii M (eds) Acarology XI: Proceedings of the International Congress. Instituto de Biología, Facultad de Ciencias, Universidad Nacional Autónoma México, Sociedad Latinoamericana de Acarologia. México 2007

  • Norton RA, Palmer SC (1991) The distribution, mechanisms, and evolutionary significance of parthenogenesis in oribatid mites. In: Schuster R, Murphy PW (eds) The Acari: reproduction, development and life-history strategies. Chapman & Hall, London, pp 107–136

    Google Scholar 

  • Norton RA, Kethley JB, Johnston DE, OConnor BM (1993) Phylogenetic perspectives on genetic systems and reproductive modes in mites. In: Wrensch DL, Ebbert MA (eds) Evolution and diversity of sex ratios. Chapman & Hall, New York, pp 8–99

    Google Scholar 

  • OConnor BM (1984) Phylogenetic relationship among higher taxa in the Acariformes, with particular reference to the Astigmata. In: Grifiths DA, Bowman CE (eds) Acarology VI, Vol 1. Ellis Horwood Ltd., Chichester, pp 19–27

    Google Scholar 

  • OConnor BM (1994) Life-history modifications in astigmatid mites. In: Houck MA (ed) Mites. Ecological and evolutionary analyses of life-history pattern. Chapman & Hall, New York, pp 136–159

    Google Scholar 

  • Posada D, Crandall KA (1998) Modeltest: testing the model of DNA substitution. Bioinformatics 14:817–818

    Article  PubMed  CAS  Google Scholar 

  • Raspotnig G (2006) Chemical alarm and defence in the oribatid mite Collohmannia gigantea (Acari: Oribatida). Exp Appl Acarol 39:177–194

    Article  PubMed  CAS  Google Scholar 

  • Reuter E (1909) Zur Morphologie und Ontogonie der Acariden. Acta Soc Sci Fenn 36:1–288

    Google Scholar 

  • Robillard T, Desutter-Grandcolas L (2006) Phylogeny of the cricket subfamily Eneopterinae (Orthoptera, Grylloidea, Eneopteridae) based on four molecular loci and morphology. Mol Phylogenet Evol 40:643–661

    Article  PubMed  CAS  Google Scholar 

  • Roehrdanz RL, Degrugillier ME, Black WC (2002) Novel rearrangements of arthropod mitochondrial DNA detected with long-PCR: applications to arthropod phylogeny and evolution. Mol Biol Evol 19:841–849

    PubMed  CAS  Google Scholar 

  • Sakata T, Norton RA (2001) Opisthonoal gland chemistry of early-derivative oribatid mites (Acari) and its relevance to systematic relationships of Astigmata. Int J Acarol 27:281–292

    Article  Google Scholar 

  • Schaefer I, Domes K, Heethoff M, Schneider K, Schoen I, Norton RA, Scheu S, Maraun M (2006) No evidence for the ‘Meselson effect’ in parthenogenetic oribatid mites (Acari, Oribatida). J Evol Biol 19:184–193

    Article  PubMed  CAS  Google Scholar 

  • Swofford D (1999) PAUP*: phylogenetic analysis using parsimony (and other methods). Version 4.0. Sinauer Associates, Sunderland, MA

    Google Scholar 

  • Tamura K, Nei M (1993) Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol Biol Evol 10:512–526

    PubMed  CAS  Google Scholar 

  • Thompson JD, Higgins DG, Gibson TJ (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

    Article  PubMed  CAS  Google Scholar 

  • 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. Nucl Acids Res 24:4876–4882

    Article  Google Scholar 

  • Van der Hammen L (1972) A revised classification of the mites (Arachnidea, Acarida) with diagnoses, a key, and notes on phylogeny. Zool Meded Leiden 47:273–292

    Google Scholar 

  • Vitzthum H (1925) Acari. In: Brohmer P, Ehrmann P, Ulmer G (eds) Die Tierwelt Mitteleuropas, Band 3. Quelle & Meyer, Leipzig, pp 1–112, Taf. 1–12

  • Walter DE, Proctor HC (1999) Mites: ecology, evolution, and behaviour. University of New South Wales Press

  • Walter DE (2001) Endemism and cryptogenesis in ‘segmented’ mites: A review of Australian Alichorhagiidae, Terpnacaridae, Oehserchestidae and Grandjeanicidae (Acari: Sarcoptiformes). Austral J Entomol 40:207–218

    Article  Google Scholar 

  • Weigmann G (2006) Hornmilben (Oribatida). In: Dahl, Tierwelt Deutschlands 76. Goecke & Evers, Keltern

  • Zachvatkin AA (1953) Studies on the morphology and postembryonic development of tyroglyphids (Sarcoptiformes, Tyroglyphoidea). In: Smirnov ES, Dubinin VB (eds) A.A. Zachvatkin, collected scientific works. Moscow State Univ. Publishing House, Moscow

    Google Scholar 

Download references

Acknowledgements

We thank Jan Hubert (Czech Republic) and Stefan Wirth (Germany) for collecting and providing specimens. This study was supported by the German Research Foundation (DFG).

Author information

Authors and Affiliations

  1. Technische Universität Darmstadt, Institut für Zoologie, Schnittspahnstr. 3, 64287, Darmstadt, Germany

    Katja Domes, Max Althammer, Stefan Scheu & Mark Maraun

  2. State University of New York, College of Environmental Science and Forestry, 1 Forestry 16 Drive, Syracuse, NY, 13210, USA

    Roy A. Norton

Authors
  1. Katja Domes
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Max Althammer
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Roy A. Norton
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Stefan Scheu
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Mark Maraun
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Katja Domes.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Domes, K., Althammer, M., Norton, R.A. et al. The phylogenetic relationship between Astigmata and Oribatida (Acari) as indicated by molecular markers. Exp Appl Acarol 42, 159–171 (2007). https://doi.org/10.1007/s10493-007-9088-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10493-007-9088-8

Keywords

Search

Navigation