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RESEARCH ARTICLE
Contents Vol 19(5)

Relationships among the three major lineages of the Acari (Arthropoda : Arachnida) inferred from small subunit rRNA: paraphyly of the Parasitiformes with respect to the Opilioacariformes and relative rates of nucleotide substitution

Anna Murrell A B , Susan J. Dobson A C , David E. Walter D E , Nick J. H. Campbell A F , Renfu Shao A G and Stephen C. Barker A H
+ Author Affiliations
- Author Affiliations

A Parasitology Section, School of Molecular and Microbial Sciences, The University of Queensland, Brisbane, Queensland 4072, Australia.

B Present address: 187 Kentucky St, Armidale, NSW 2350, Australia.

C Present address: 22 Browning Road, West Moonah, Tasmania 7009, Australia.

D Department of Bioagricultural Sciences and Pest Management, Colorado State University, Fort Collins, CO 80523, USA.

E Department of Biological Sciences, University of Alberta, Edmonton, AB, T6G 2E9 Canada.

F Current address: Nature Publishing Group, The Macmillan Building, 4 Crinan St, London, N1 9XW, UK.

G Faculty of Pharmacy and Pharmaceutical Sciences, Fukuyama University, Fukuyama, Hiroshima, 729-0292, Japan.

H Corresponding author. Email: s.barker@uq.edu.au

Invertebrate Systematics 19(5) 383-389 https://doi.org/10.1071/IS05027
Submitted: 18 June 2005  Accepted: 16 September 2005   Published: 12 December 2005

Abstract

We inferred phylogeny among the three major lineages of the Acari (mites) from the small subunit rRNA gene. Our phylogeny indicates that the Opilioacariformes is the sister-group to the Ixodida+Holothyrida, not the Ixodida+Mesostigmata+Holothyrida, as previously thought. Support for this relationship increased when sites with the highest rates of nucleotide substitution, and thus the greatest potential for saturation with nucleotide substitutions, were removed. Indeed, the increase in support (and resolution) was despite a 70% reduction in the number of parsimony-informative sites from 408 to 115. This shows that rather than ‘noisy’ sites having no impact on resolution of deep branches, ‘noisy’ sites have the potential to obscure phylogenetic relationships. The arrangement, Ixodida+Holothyrida+Opilioacariformes, however, may be an artefact of long-branch attraction since relative-rate tests showed that the Mesostigmata have significantly faster rates of nucleotide substitution than other parasitiform mites. Thus, the fast rates of nucleotide substitution of the Mesostigmata might have caused the Mesostigmata to be attracted to the outgroup in our trees. We tested the hypothesis that the high rate of nucleotide substitution in some mites was related to their short generation times. The Acari species that have high nucleotide substitution rates usually have short generation times; these mites also tend to be more active and thus have higher metabolic rates than other mites. Therefore, more than one factor may affect the rate of nucleotide substitution in these mites.

Additional keywords: phylogeny, relative substitution rates, SSU rRNA.


Acknowledgments

We thank Heather Proctor for helpful discussions and Maree Schabe for help with the format of the manuscript. R.S. is a postdoctoral fellow of the Japan Society for the Promotion of Science. This work was supported by an Australian Research Council grant to S.C.B.


References


Barker S. C., Murrell A. (2004) Systematics and evolution of ticks with a list of valid genus and species names. Parasitology 129(Supplement), 15–36.
| Crossref | GoogleScholarGoogle Scholar | open url image1

Black W. C., Klompen J. S. H., Keirans J. E. (1997) Phylogenetic relationships among tick subfamilies (Ixodida: Ixodidae: Argasidae) based on the 18S nuclear rDNA gene. Molecular Phylogenetics and Evolution 7, 129–144.
| Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Bleiweiss R. (1998) Slow rate of molecular evolution in high-elevation hummingbirds. Proceedings of the National Academy of Sciences of the United States of America 95, 612–616.
| Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Bromham L. (2002) Molecular clocks in reptiles: life history influences rate of molecular evolution. Molecular Biology and Evolution 19, 302–309.
| PubMed |
open url image1

Bromham L., Rambaut A., Hendy M. D., Penny D. (2000) The power of relative rates tests depends on the data. Journal of Molecular Evolution 50, 296–301.
| PubMed |
open url image1

Coddington J. A., Giribet G., Harvey M. S., Prendini L., and Walter D. E. (2004). Arachnida. In ‘Assembling the Tree of Life’. (Eds J. Cracraft and M. J. Donoghue.) pp. 296–318. (Oxford University Press: New York, USA.)

Cruickshank R. H. (2002) Molecular markers for the phylogenetics of mites and ticks. Systematic and Applied Acarology 7, 3–14. open url image1

Dobson S. J., Barker S. C. (1999) Phylogeny of the hard ticks (Ixodidae) inferred from 18S rRNA indicates that the genus Aponomma is paraphyletic. Molecular Phylogenetics and Evolution 11, 288–295.
| Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Dunlop J. A., Wunderlich J., Poinar G. O. (2004) The first fossil opilioacariform mite (Acari: Opilioacariformes) and the first Baltic amber camel spider (Solifugae). Transactions of the Royal Society of Edinburgh: Earth Sciences 94, 261–273. open url image1

Fan Q. H., and Zhang Z. Q. (2004). ‘Revision of Rhizoglyphus Claparède (Acari: Acaridae) of Australasia and Oceania.’ (Systematic and Applied Acarology Society: London, UK.)

Felsenstein J. (1978) Cases in which parsimony or compatibility methods will be positively misleading. Systematic Zoology 27, 401–410. open url image1

Felsenstein J. (1993). ‘PHYLIP (Phylogeny Inference Package) version 3.5c.’ Distributed by the author. (Department of Genetics, University of Washington, Seattle, WA, USA.)

Giribet G., Edgecombe G. D., Wheeler W. C., Babbitt C. (2002) Phylogeny and systematic position of Opiliones:a combined analysis of chelicerate relationshipsusing morphological and molecular data. Cladistics 18, 5–70.
| PubMed |
open url image1

Grandjean F. (1936) Un acarien synthetique: Opilioacarus segmentatus With. Bulletin de la Société d’Historie Naturelle de l’Afrique du Nord Alger 27, 413–444. open url image1

Hubbard M. J., Cann K. J., Wright D. J. (1995) Validation and rapid extraction of nucleic acids from alcohol-preserved ticks. Experimental and Applied Acarology 19, 473–478. open url image1

Klompen J. S. H. (2000) Prelarva and larva of Opilioacarus (Neocarus) texanus (Chamberlin and Mulaik) (Acari: Opilioacarida) with notes on the patterns of setae and lyrifissures. Journal of Natural History 34, 1977–1992.
| Crossref | GoogleScholarGoogle Scholar | open url image1

Li W.-H., Tanimura M., Sharp P. M. (1987) An evaluation of the molecular clock hypothesis using mammalian DNA sequences. Journal of Molecular Evolution 25, 330–342.
| PubMed |
open url image1

Lindquist E. E. (1984). Current theories on the evolution of major groups of Acari and on their relationships with other groups of Arachnida, with consequent implications for their classification. In ‘Acarology VI, Vol. 1’. (Eds D. A. Griffiths and C. E. Bowman.) pp. 28–62. (John Wiley & Sons, New York, USA.)

Martin A. P., Palumbi S. R. (1993) Body size, metabolic rate, generation-time, and the molecular clock. Proceedings of the National Academy of Sciences of the United States of America 90, 4087–4091.
| PubMed |
open url image1

Mindell D. P., Thacker C. E. (1996) Rates of molecular evolution: phylogenetic issues and applications. Annual Review of Ecology and Systematics 27, 279–303.
| Crossref | GoogleScholarGoogle Scholar | open url image1

Norton R. A. (1998) Morphological evidence for the evolutionary origin of Astigmata (Acari: Acariformes). Experimental and Applied Acarology 22, 559–594.
| Crossref | GoogleScholarGoogle Scholar | open url image1

Norton R. A., Bonamo P. M., Grierson J. D., Shear W. A. (1988) Oribatid mite fossils from a terrestrial Devonian deposit near Gilboa, New York (USA). Journal of Paleontology 62, 259–269. open url image1

Nunn G. B., Stanley S. E. (1998) Body size effects and rates of cytochrome b evolution in tube-nosed seabirds. Molecular Biology and Evolution 15, 1360–1371.
| PubMed |
open url image1

Philippe H., Laurent J. (1998) How good are deep phylogenetic trees? Current Opinions in Genetics and Evolution 8, 616–623.
| Crossref | GoogleScholarGoogle Scholar | open url image1

Poe S., Swofford D. L. (1999) Taxon sampling revisited. Nature 398, 299–300.
| Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Poinar G., Brown A. E. (2003) A new genus of hard ticks in Cretaceous Burmese amber (Acari: Ixodida: Ixodidae). Systematic Parasitology 54, 199–205.
| Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Rand D. M. (1994) Thermal habit, metabolic rate and the evolution of mitochondrial DNA. Trends in Ecology & Evolution 9, 125–131.
| Crossref | GoogleScholarGoogle Scholar | open url image1

Robinson M., Gouy M., Gautier C., Mouchiroud D. (1998) Sensitivity of the relative-rates test to taxonomic sampling. Molecular Biology and Evolution 15, 1091–1098.
| PubMed |
open url image1

Robinson-Rechavi M., Huchon D. (2000) RRTree: Relative-Rate Tests between groups of sequences on a phylogenetic tree. Bioinformatics (Oxford, England) 16, 296–297.
| Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Ruiz-Trillo I., Riutort M., Littlewood D. T., Herniou E. A., Baguna J. (1999) Acoel flatworms: earliest extant bilaterian Metazoans, not members of Platyhelminthes. Science 283, 1919–1923.
| Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Shao R., Dowton M., Murrell A., Barker S. C. (2003) Rates of gene rearrangement and nucleotide substitution are correlated in the mitochondrial genomes of insects. Molecular Biology and Evolution 20, 1612–1619.
| Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Sonenshine D. E. (1991). ‘Biology of Ticks, Vol. 1.’ (Oxford University Press, New York, USA.)

Strimmer K., Von Haeseler A. (1996) Quartet puzzling: A quartet maximum likelihood method for reconstructing tree topologies. Molecular Biology and Evolution 13, 964–969. open url image1

Swofford D. L. (2002). ‘PAUP*. Phylogenetic Analysis Using Parsimony (*and Other Methods). Version 4.’ (Sinauer Associates: Sunderland, MA, USA.)

Vazquez M. M., Klompen H. (2003) The family Opilioacaridae (Acari: Parasitiformes) in North and Central America, with description of four new species. Acarologia 42, 299–322. open url image1

Walter D. E., Proctor H. C. (1998) Feeding behaviour and phylogeny: observations on early derivative Acari. Experimental and Applied Acarology 22, 39–50.
| Crossref | GoogleScholarGoogle Scholar | open url image1

Walter D. E., and Proctor H. C. (1999). ‘Mites: Ecology, Evolution and Behaviour.’ (CABI: Wallingford, UK.)

Walter D. E. (2000) A jumping mesostigmatan: Saltiseius hunteri, n.g., n. sp. (Acari: Mesostigmata: Trigynaspida: Saltiseiidae, n. fam.). International Journal of Acarology 26, 25–31. open url image1

Wheeler W. C., Hayashi C. Y. (1998) The phylogeny of the extant Chelicerate orders. Cladistics 14, 173–192.
| Crossref | GoogleScholarGoogle Scholar | open url image1

Whiting M. F., Carpenter J. C., Wheeler Q. D., Wheeler W. C. (1997) The Strepsiptera problem: phylogeny of the holometabolous insect orders inferred from 18S and 28S ribosomal DNA sequences and morphology. Systematic Biology 1, 1–68. open url image1

Witalinski W. (2000) Aclerogamasus stenocornis sp. n., a fossil mite from the Baltic amber (Acari: Gamasida: Parasitidae). Genus (Wroclaw) 11, 619–626. open url image1

Wu C. I., Li W.-H. (1985) Evidence for higher rates of nucleotide substitution in rodents than in man. Proceedings of the National Academy of Sciences of the United States of America 82, 1741–1745.
| PubMed |
open url image1