Hostname: page-component-7479d7b7d-qlrfm Total loading time: 0 Render date: 2024-07-11T02:22:35.728Z Has data issue: false hasContentIssue false
  • English
  • Français

Mitochondrial genomes of parasitic arthropods: implications for studies of population genetics and evolution

Published online by Cambridge University Press:  11 October 2006

R. SHAO  and
S. C. BARKER
R. SHAO
Affiliation:
Parasitology Section, School of Molecular and Microbial Sciences, The University of Queensland, St Lucia, Brisbane, Queensland 4072, Australia
S. C. BARKER
Affiliation:
Parasitology Section, School of Molecular and Microbial Sciences, The University of Queensland, St Lucia, Brisbane, Queensland 4072, Australia
Get access Rights & Permissions [Opens in a new window]

Abstract

Over 39000 species of arthropods parasitize humans, domestic animals and wildlife. Despite their medical, veterinary and economic importance, most aspects of the population genetics and evolution of the vast majority of parasitic arthropods are poorly understood. Mitochondrial genomes are a rich source of markers for studies of population genetics and evolution. These markers include (1) nucleotide sequences of each of the 37 mitochondrial genes and non-coding regions; (2) concatenated nucleotide sequences of 2 or more genes; and (3) genomic features, such as gene duplications, gene rearrangements, and changes in gene content and secondary structures of RNAs. To date, the mitochondrial genomes of over 700 species of multi-cellular animals have been sequenced entirely, however, only 24 of these species are parasitic arthropods. Of the mitochondrial genome markers, only the nucleotide sequences of 4 mitochondrial genes, cox1, cob, rrnS and rrnL, have been well explored in population genetic and evolutionary studies of parasitic arthropods whereas the sequences of the other 33 genes, and various genomic features have not. We review current knowledge of the mitochondrial genomes of parasitic arthropods, summarize applications of mitochondrial genes and genomic features in population genetic and evolutionary studies, and highlight prospects for future research.

Keywords

mitochondrial genomeparasitic arthropodpopulation geneticssystematicsphylogeneticsgene ordergene rearrangement
Type
Review Article
Information
Parasitology , Volume 134 , Issue 2 , February 2007 , pp. 153 - 167
Copyright
2006 Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Adler, P. H. ( 2005). Black flies, the Simuliidae. In Biology of Disease Vectors ( ed. Marquardt, W. C.), pp. 127–140. Elsevier Academic Press, Boston.
Almeida, W. D. and Christoffersen, M. L. ( 1999). A cladistic approach to relationships in Pentastomida. Journal of Parasitology 85, 695–704.CrossRefGoogle Scholar
Andersson, S. G., Zomorodipour, A., Andersson, J. O., Sicheritz-Ponten, T., Alsmark, U. C., Podowski, R. M., Naslund, A. K., Eriksson, A. S., Winkler, H. H. and Kurland, C. G. ( 1998). The genome sequence of Rickettsia prowazekii and the origin of mitochondria. Nature, London 396, 133–140.CrossRefGoogle Scholar
Aranishi, F. and Okimoto, T. ( 2005). Sequence polymorphism in a novel noncoding region of Pacific oyster mitochondrial DNA. Journal of Applied Genetics 46, 201–206.Google Scholar
Arnason, U., Adegoke, J. A., Bodin, K., Born, E. W., Esa, Y. B., Gullberg, A., Nilsson, M., Short, R. V., Xu, X. F. and Janke, A. ( 2002). Mammalian mitogenomic relationships and the root of the eutherian tree. Proceedings of the National Academy of Sciences, USA 99, 8151–8156.CrossRefGoogle Scholar
Avise, J. C. ( 2004). Molecular Markers, Natural History, and Evolution, 2nd Edn. Sinauer Associates, Sunderland, Mass.
Azeredo-Espin, A. M. and Lessinger, A. C. ( 2006). Genetic approaches for studying myiasis-causing flies: molecular markers and mitochondrial genomics. Genetica 126, 111–131.CrossRefGoogle Scholar
Bae, J. S., Kim, I., Sohn, H. D. and Jin, B. R. ( 2004). The mitochondrial genome of the firefly, Pyrocoelia rufa: complete DNA sequence, genome organization, and phylogenetic analysis with other insects. Molecular Phylogenetics and Evolution 32, 978–985.CrossRefGoogle Scholar
Barker, S. C. and Murrell, A. ( 2004). Systematics and evolution of ticks with a list of valid genus and species names. Parasitology 129 (Suppl.), S15–S36.CrossRefGoogle Scholar
Beard, C. B. ( 2005). Kissing bugs and bedbugs, the Hemiptera. In Biology of Disease Vectors ( ed. Marquardt, W. C.), pp. 57–65. Elsevier Academic Press, Boston.
Beard, C. B., Hamm, D. M. and Collins, F. H. ( 1993). The mitochondrial genome of the mosquito Anopheles gambiae: DNA sequence, genome organization, and comparisons with mitochondrial sequences of other insects. Insect Molecular Biology 2, 103–124.CrossRefGoogle Scholar
Beati, L. and Keirans, J. E. ( 2001). Analysis of the systematic relationships among ticks of the genera Rhipicephalus and Boophilus (Acari: Ixodidae) based on mitochondrial 12S ribosomal DNA gene sequences and morphological characters. Journal of Parasitology 87, 32–48.CrossRefGoogle Scholar
Bergstrom, J. ( 1979). Morphology of fossil arthropods as a guide to phylogenetic relationships. In Arthropod Phylogeny ( ed. Gupta, A. P.), pp. 3–56. Van Nostrand Reinhold, New York.
Black, W. C. and Kondratieff, B. C. ( 2005). Evolution of arthropod disease vectors. In Biology of Disease Vectors ( ed. Marquardt, W. C.), pp. 9–23. Elsevier Academic Press, Boston.
Black, W. C. T. and Piesman, J. ( 1994). Phylogeny of hard- and soft-tick taxa (Acari: Ixodida) based on mitochondrial 16S rDNA sequences. Proceedings of the National Academy of Sciences, USA 91, 10034–10038.CrossRefGoogle Scholar
Black, W. C. T. and Roehrdanz, R. L. ( 1998). Mitochondrial gene order is not conserved in arthropods: prostriate and metastriate tick mitochondrial genomes. Molecular Biology and Evolution 15, 1772–1785.CrossRefGoogle Scholar
Boore, J. L. and Brown, W. M. ( 1998). Big trees from little genomes: mitochondrial gene order as a phylogenetic tool. Current Opinion in Genetics and Development 8, 668–674.CrossRefGoogle Scholar
Boore, J. L. and Brown, W. M. ( 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. Molecular Biology and Evolution 17, 87–106.CrossRefGoogle Scholar
Boore, J. L. and Staton, J. L. ( 2002). The mitochondrial genome of the sipunculid Phascolopsis gouldii supports its association with Annelida rather than Mollusca. Molecular Biology and Evolution 19, 127–137.CrossRefGoogle Scholar
Boore, J. L., Lavrov, D. V. and Brown, W. M. ( 1998). Gene translocation links insects and crustaceans. Nature, London 392, 667–668.CrossRefGoogle Scholar
Borkent, A. ( 2005). The biting midges, the Ceratopogonidae (Diptera). In Biology of Disease Vectors ( ed. Marquardt, W. C.), pp. 113–126. Elsevier Academic Press, Boston.
Brinkmann, H., Denk, A., Zitzler, J., Joss, J. J. and Meyer, A. ( 2004). Complete mitochondrial genome sequences of the South american and the Australian lungfish: testing of the phylogenetic performance of mitochondrial data sets for phylogenetic problems in tetrapod relationships. Journal of Molecular Evolution 59, 834–848.CrossRefGoogle Scholar
Brown, W. M., George, M., Jr. and Wilson, A. C. ( 1979). Rapid evolution of animal mitochondrial DNA. Proceedings of the National Academy of Sciences, USA 76, 1967–1971.CrossRefGoogle Scholar
Campbell, N. J. H. and Barker, S. C. ( 1998). An unprecedented major rearrangement in an arthropod mitochondrial genome. Molecular Biology and Evolution 15, 1786–1787.CrossRefGoogle Scholar
Cockburn, A. F., Mitchell, S. E. and Seawright, J. A. ( 1990). Cloning of the mitochondrial genome of Anopheles quadrimaculatus. Archives of Insect Biochemistry and Physiology 14, 31–36.CrossRefGoogle Scholar
Colless, D. H. and McAlpine, D. K. ( 1991). Diptera (Flies). In The Insects of Australia ( ed. CSIRO), pp. 717–789. Melbourne University Press, Melbourne.
Covacin, C., Shao, R., Cameron, S. and Barker, S. C. ( 2006). Extraordinary number of gene rearrangements in the mitochondrial genomes of lice (Phthiraptera: Insecta). Insect Molecular Biology 15, 63–68.CrossRefGoogle Scholar
Crozier, R. H. and Crozier, Y. C. ( 1993). The mitochondrial genome of the honeybee Apis mellifera: complete sequence and genome organization. Genetics 133, 97–117.Google Scholar
Davis, C. S., Delisle, I., Stirling, I., Siniff, D. B. and Strobeck, C. ( 2004). A phylogeny of the extant Phocidae inferred from complete mitochondrial DNA coding regions. Molecular Phylogenetics and Evolution 33, 363–377.CrossRefGoogle Scholar
Dimauro, S. and Davidzon, G. ( 2005). Mitochondrial DNA and disease. Annals of Medicine 37, 222–232.CrossRefGoogle Scholar
Dong, S. and Kumazawa, Y. ( 2005). Complete mitochondrial DNA sequences of six snakes: phylogenetic relationships and molecular evolution of genomic features. Journal of Molecular Evolution 61, 12–22.CrossRefGoogle Scholar
Dotson, E. M. and Beard, C. B. ( 2001). Sequence and organization of the mitochondrial genome of the Chagas disease vector, Triatoma dimidiata. Insect Molecular Biology 10, 205–215.CrossRefGoogle Scholar
Dowton, M., Castro, L. R. and Austin, A. D. ( 2002). Mitochondrial gene rearrangements as phylogenetic characters in the invertebrates: the examination of genome ‘morphology’. Invertebrate Systematics 16, 345–356.CrossRefGoogle Scholar
Drovetski, S. V. ( 2002). Molecular phylogeny of grouse: individual and combined performance of W-linked, autosomal, and mitochondrial loci. Systematic Biology 51, 930–945.CrossRefGoogle Scholar
Dudaniec, R. Y. and Kleindorfer, S. ( 2006). Effects of the parasitic flies of the genus Philornis (Diptera: Muscidae) on birds. Emu 106, 13–20.CrossRefGoogle Scholar
Durden, L. A. and Musser, G. G. ( 1994). The sucking lice (Insecta, Anoplura) of the world – a taxonomic checklist with records of mammalian hosts and geographical distributions. Bulletin of the American Museum of Natural History 218, 1–90.Google Scholar
Eldridge, B. F. ( 2005). Mosquitoes, the Culicidae. In Biology of Disease Vectors ( ed. Marquardt, W. C.), pp. 95–111. Elsevier Academic Press, Boston.
Elmerot, C., Arnason, U., Gojobori, T. and Janke, A. ( 2002). The mitochondrial genome of the pufferfish, Fugu rubripes, and ordinal teleostean relationships. Gene 295, 163–172.CrossRefGoogle Scholar
Evans, J. D. and Lopez, D. L. ( 2002). Complete mitochondrial DNA sequence of the important honey bee pest, Varroa destructor (Acari: Varroidae). Experimental and Applied Acarology 27, 69–78.CrossRefGoogle Scholar
Flook, P. K., Rowell, C. H. and Gellissen, G. ( 1995). The sequence, organization, and evolution of the Locusta migratoria mitochondrial genome. Journal of Molecular Evolution 41, 928–941.CrossRefGoogle Scholar
Goddard, J. M. and Wolstenholme, D. R. ( 1980). Origin and direction of replication in mitochondrial DNA molecules from the genus Drosophila. Nucleic Acids Research 8, 741–757.Google Scholar
Gray, M. W. ( 1989). Origin and evolution of mitochondrial DNA. Annual Review of Cell Biology 5, 25–50.CrossRefGoogle Scholar
Gray, M. W., Burger, G. and Lang, B. F. ( 1999). Mitochondrial evolution. Science 283, 1476–1481.CrossRefGoogle Scholar
Haring, E., Kruckenhauser, L., Gamauf, A., Riesing, M. J. and Pinsker, W. ( 2001). The complete sequence of the mitochondrial genome of Buteo buteo (Aves, Accipitridae) indicates an early split in the phylogeny of raptors. Molecular Biology and Evolution 18, 1892–1904.CrossRefGoogle Scholar
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. Molecular Phylogenetics and Evolution 38, 100–116.CrossRefGoogle Scholar
Holt, R. A., Subramanian, G. M., Halpern, A., Sutton, G. G., Charlab, R., Nusskern, D. R., Wincker, P., Clark, A. G., Ribeiro, J. M., Wides, R., Salzberg, S. L., Loftus, B., Yandell, M., Majoros, W. H., Rusch, D. B., Lai, Z., Kraft, C. L., Abril, J. F., Anthouard, V., Arensburger, P., Atkinson, P. W., Baden, H., De Berardinis, V., Baldwin, D., Benes, V., Biedler, J., Blass, C., Bolanos, R., Boscus, D., Barnstead, M., Cai, S., Center, A., Chaturverdi, K., Christophides, G. K., Chrystal, M. A., Clamp, M., Cravchik, A., Curwen, V., Dana, A., Delcher, A., Dew, I., Evans, C. A., Flanigan, M., Grundschober-Freimoser, A., Friedli, L., Gu, Z., Guan, P., Guigo, R., Hillenmeyer, M. E., Hladun, S. L., Hogan, J. R., Hong, Y. S., Hoover, J., Jaillon, O., Ke, Z., Kodira, C., Kokoza, E., Koutsos, A., Letunic, I., Levitsky, A., Liang, Y., Lin, J. J., Lobo, N. F., Lopez, J. R., Malek, J. A., McIntosh, T. C., Meister, S., Miller, J., Mobarry, C., Mongin, E., Murphy, S. D., O'brochta, D. A., Pfannkoch, C., Qi, R., Regier, M. A., Remington, K., Shao, H., Sharakhova, M. V., Sitter, C. D., Shetty, J., Smith, T. J., Strong, R., Sun, J., Thomasova, D., Ton, L. Q., Topalis, P., Tu, Z., Unger, M. F., Walenz, B., Wang, A., Wang, J., Wang, M., Wang, X., Woodford, K. J., Wortman, J. R., Wu, M., Yao, A., Zdobnov, E. M., Zhang, H., Zhao, Q., Zhao, S., Zhu, S. C., Zhimulev, I., Coluzzi, M., Della Torre, A., Roth, C. W., Louis, C., Kalush, F., Mural, R. J., Myers, E. W., Adams, M. D., Smith, H. O., Broder, S., Gardner, M. J., Fraser, C. M., Birney, E., Bork, P., Brey, P. T., Venter, J. C., Weissenbach, J., Kafatos, F. C., Collins, F. H. and Hoffman, S. L. ( 2002). The genome sequence of the malaria mosquito Anopheles gambiae. Science 298, 129–149.CrossRefGoogle Scholar
Hu, M. and Gasser, R. B. ( 2006). Mitochondrial genomes of parasitic nematodes-progress and perspectives. Trends in Parasitology 22, 78–84.CrossRefGoogle Scholar
Hu, M., Chilton, N. B., Abs El-Osta, Y. G. and Gasser, R. B. ( 2003). Comparative analysis of mitochondrial genome data for Necator americanus from two endemic regions reveals substantial genetic variation. International Journal for Parasitology 33, 955–963.CrossRefGoogle Scholar
Ingman, M. and Gyllensten, U. ( 2003). Mitochondrial genome variation and evolutionary history of Australian and New Guinean aborigines. Genome Research 13, 1600–1606.CrossRefGoogle Scholar
Ingman, M., Kaessmann, H., Paabo, S. and Gyllensten, U. ( 2000). Mitochondrial genome variation and the origin of modern humans. Nature, London 408, 708–713.CrossRefGoogle Scholar
Janke, A., Erpenbeck, D., Nilsson, M. and Arnason, U. ( 2001). The mitochondrial genomes of the iguana (Iguana iguana) and the caiman (Caiman crocodylus): implications for amniote phylogeny. Proceedings of the Royal Society of London, B 268, 623–631.CrossRefGoogle Scholar
Jordan, A. M. ( 1993). Tsetse flies (Glossinidae). In Medical Insects and Arachnids ( ed. Lane, R. P. and Crosskey, R. W.), pp. 333–388. Chapman and Hall, London.CrossRef
Junqueira, A. C. M., Lessinger, A. C., Torres, T. T., Da Silva, F. R., Vettore, A. L., Arruda, P. and Espin, A. M. L. A. ( 2004). The mitochondrial genome of the blowfly Chrysomya chloropyga (Diptera: Calliphoridae). Gene 339, 7–15.CrossRefGoogle Scholar
Kittler, R., Kayser, M. and Stoneking, M. ( 2003). Molecular evolution of Pediculus humanus and the origin of clothing. Current Biology 13, 1414–1417.CrossRefGoogle Scholar
Kumazawa, Y. and Nishida, M. ( 1993). Sequence evolution of mitochondrial tRNA genes and deep-branch animal phylogenetics. Journal of Molecular Evolution 37, 380–398.CrossRefGoogle Scholar
Kumazawa, Y. and Nishida, M. ( 1995). Variations in mitochondrial tRNA gene organization of reptiles as phylogenetic markers. Molecular Biology and Evolution 12, 759–772.Google Scholar
Kumazawa, Y. and Nishida, M. ( 1999). Complete mitochondrial DNA sequences of the green turtle and blue-tailed mole skink: statistical evidence for archosaurian affinity of turtles. Molecular Biology and Evolution 16, 784–792.CrossRefGoogle Scholar
Lang, B. F., Gray, M. W. and Burger, G. ( 1999). Mitochondrial genome evolution and the origin of eukaryotes. Annual Review of Genetics 33, 351–397.CrossRefGoogle Scholar
Lavrov, D. V. and Brown, W. M. ( 2001). Trichinella spiralis mtDNA: a nematode mitochondrial genome that encodes a putative ATP8 and normally structured tRNAS and has a gene arrangement relatable to those of coelomate metazoans. Genetics 157, 621–637.Google Scholar
Lavrov, D. V., Brown, W. M. and Boore, J. L. ( 2004). Phylogenetic position of the Pentastomida and (pan)crustacean relationships. Proceedings of the Royal Society of London, B 271, 537–544.CrossRefGoogle Scholar
Le, T. H., Blair, D. and McManus, D. P. ( 2002). Mitochondrial genomes of parasitic flatworms. Trends in Parasitology 18, 206–213.CrossRefGoogle Scholar
Leo, N. P., Campbell, N. J., Yang, X., Mumcuoglu, K. and Barker, S. C. ( 2002). Evidence from mitochondrial DNA that head lice and body lice of humans (Phthiraptera: Pediculidae) are conspecific. Journal of Medical Entomology 39, 662–666.CrossRefGoogle Scholar
Lessinger, A. C., Junqueira, A. C. M., Conte, F. F. and Espin, A. M. L. A. ( 2004). Analysis of a conserved duplicated tRNA gene in the mitochondrial genome of blowflies. Gene 339, 1–6.CrossRefGoogle Scholar
Lessinger, A. C., Martins Junqueira, A. C., Lemos, T. A., Kemper, E. L., Da Silva, F. R., Vettore, A. L., Arruda, P. and Azeredo-Espin, A. M. ( 2000). The mitochondrial genome of the primary screwworm fly Cochliomyia hominivorax (Diptera: Calliphoridae). Insect Molecular Biology 9, 521–529.CrossRefGoogle Scholar
Lewis, R. E. and Lewis, J. H. ( 1985). Notes on the geographical-distribution and host preferences in the order Siphonaptera. Part 7. New taxa described between 1972 and 1983, with a supraspecific classification of the order. Journal of Medical Entomology 22, 134–152.Google Scholar
Liu, Y. P., Wu, G. S., Yao, Y. G., Miao, Y. W., Luikart, G., Baig, M., Beja-Pereira, A., Ding, Z. L., Palanichamy, M. G. and Zhang, Y. P. ( 2006). Multiple maternal origins of chickens: out of the Asian jungles. Molecular Phylogenetics and Evolution 38, 12–19.CrossRefGoogle Scholar
Macaulay, V., Hill, C., Achilli, A., Rengo, C., Clarke, D., Meehan, W., Blackburn, J., Semino, O., Scozzari, R., Cruciani, F., Taha, A., Shaari, N. K., Raja, J. M., Ismail, P., Zainuddin, Z., Goodwin, W., Bulbeck, D., Bandelt, H. J., Oppenheimer, S., Torroni, A. and Richards, M. ( 2005). Single, rapid coastal settlement of Asia revealed by analysis of complete mitochondrial genomes. Science 308, 1034–1036.CrossRefGoogle Scholar
Macey, J. R., Papenfuss, T. J., Kuehl, J. V., Fourcade, H. M. and Boore, J. L. ( 2004). Phylogenetic relationships among amphisbaenian reptiles based on complete mitochondrial genomic sequences. Molecular Phylogenetics and Evolution 33, 22–31.CrossRefGoogle Scholar
Macey, J. R., Schulte, J. A. and Larson, A. ( 2000). Evolution and phylogenetic information content of mitochondrial genomic structural features illustrated with acrodont lizards. Systematic Biology 49, 257–277.CrossRefGoogle Scholar
Macey, J. R., Wang, Y. Z., Ananjeva, N. B., Larson, A. and Papenfuss, T. J. ( 1999). Vicariant patterns of fragmentation among gekkonid lizards of the genus Teratoscincus produced by the Indian collision: A molecular phylogenetic perspective and an area cladogram for Central Asia. Molecular Phylogenetics and Evolution 12, 320–332.CrossRefGoogle Scholar
Mangold, A. J., Bargues, M. D. and Mas-Coma, S. ( 1998). Mitochondrial 16S rDNA sequences and phylogenetic relationships of species of Rhipicephalus and other tick genera among Metastriata (Acari: Ixodidae). Parasitology Research 84, 478–484.CrossRefGoogle Scholar
Masta, S. E. and Boore, J. L. ( 2004). The complete mitochondrial genome sequence of the spider Habronattus oregonensis reveals rearranged and extremely truncated tRNAs. Molecular Biology and Evolution 21, 893–902.CrossRefGoogle Scholar
May, R. M. ( 1990). How many species? Philosophical Transactions of the Royal Society of London, B 330, 293–304.Google Scholar
McCosker, P. J. ( 1979). Global aspects of the management and control of ticks of veterinary importance. In Recent Advances in Acarology ( ed. Rodriguez, J.), pp. 45–53. Academic Press, New York.CrossRef
McFadden, C. S., Tullis, I. D., Hutchinson, M. B., Winner, K. and Sohm, J. A. ( 2004). Variation in coding (NADH dehydrogenase subunits 2, 3, and 6) and noncoding intergenic spacer regions of the mitochondrial genome in Octocorallia (Cnidaria: Anthozoa). Marine Biotechnology 6, 516–526.CrossRefGoogle Scholar
Mirabello, L. and Conn, J. E. ( 2006). Molecular population genetics of the malaria vector Anopheles darlingi in Central and South America. Heredity 96, 311–321.CrossRefGoogle Scholar
Mitani, H., Talbert, A. and Fukunaga, M. ( 2004). New World relapsing fever Borrelia found in Ornithodoros porcinus ticks in central Tanzania. Microbiology and Immunology 48, 501–505.CrossRefGoogle Scholar
Morrison, C. L., Harvey, A. W., Lavery, S., Tieu, K., Huang, Y. and Cunningham, C. W. ( 2002). Mitochondrial gene rearrangements confirm the parallel evolution of the crab-like form. Proceedings of the Royal Society of London, B 269, 345–350.CrossRefGoogle Scholar
Mueller, R. L., Macey, J. R., Jaekel, M., Wake, D. B. and Boore, J. L. ( 2004). Morphological homoplasy, life history evolution, and historical biogeography of plethodontid salamanders inferred from complete mitochondrial genomes. Proceedings of the National Academy of Sciences, USA 101, 13820–13825.CrossRefGoogle Scholar
Munstermann, L. E. ( 2005). Phlebotomine sand flies, the Psychodidae. In Biology of Disease Vectors ( ed. Marquardt, W. C.), pp. 141–151. Elsevier Academic Press, Boston.
Murrell, A., Campbell, N. J. and Barker, S. C. ( 1999). Mitochondrial 12S rDNA indicates that the Rhipicephalinae (Acari: Ixodida) is paraphyletic. Molecular Phylogenetics and Evolution 12, 83–86.CrossRefGoogle Scholar
Mustafa, A., Rankaduwa, W. and Campbell, P. ( 2001). Estimating the cost of sea lice to salmon aquaculture in eastern Canada. Canadian Veterinary Journal 42, 54–56.Google Scholar
Nardi, F., Spinsanti, G., Boore, J. L., Carapelli, A., Dallai, R. and Frati, F. ( 2003). Hexapod origins: monophyletic or paraphyletic? Science 299, 1887–1889.Google Scholar
Nass, M. M. and Nass, S. ( 1962). Fibrous structures within the matrix of developing chick embryo mitochondria. Experimental Cell Research 26, 424–427.CrossRefGoogle Scholar
Navajas, M., Le Conte, Y., Solignac, M., Cros-Arteil, S. and Cornuet, J. M. ( 2002). The complete sequence of the mitochondrial genome of the honeybee ectoparasite mite Varroa destructor (Acari: Mesostigmata). Molecular Biology and Evolution 19, 2313–2317.CrossRefGoogle Scholar
Nikaido, M., Harada, M., Cao, Y., Hasegawa, M. and Okada, N. ( 2000). Monophyletic origin of the order Chiroptera and its phylogenetic position among mammalia, as inferred from the complete sequence of the mitochondrial DNA of a Japanese megabat, the Ryukyu flying fox (Pteropus dasymallus). Journal of Molecular Evolution 51, 318–328.CrossRefGoogle Scholar
Norris, D. E., Klompen, J. S., Keirans, J. E. and Black, W. C. T. ( 1996). Population genetics of Ixodes scapularis (Acari: Ixodidae) based on mitochondrial 16S and 12S genes. Journal of Medical Entomology 33, 78–89.CrossRefGoogle Scholar
Okimoto, R., Macfarlane, J. L., Clary, D. O. and Wolstenholme, D. R. ( 1992). The mitochondrial genomes of two nematodes, Caenorhabditis elegans and Ascaris suum. Genetics 130, 471–498.Google Scholar
Philippe, H. and Laurent, J. ( 1998). How good are deep phylogenetic trees? Current Opinion in Genetics and Development 8, 616–623.Google Scholar
Philippe, H., Delsuc, F., Brinkmann, H. and Lartillot, N. ( 2005). Phylogenomics. Annual Review of Ecology, Evolution and Systematics 36, 541–562.CrossRefGoogle Scholar
Price, R. D., Hellenthal, R. A., Palma, R. L., Johnson, K. P. and Clayton, D. H. ( 2003). The Chewing Lice: World Checklist and Biological Overview. Illinois Natural History Survey.
Rajkumar, R., Banerjee, J., Gunturi, H. B., Trivedi, R. and Kashyap, V. K. ( 2005). Phylogeny and antiquity of M macrohaplogroup inferred from complete mt DNA sequence of Indian specific lineages. BMC Evolutionary Biology 5, 26.CrossRefGoogle Scholar
Rand, D. M., Haney, R. A. and Fry, A. J. ( 2004). Cytonuclear coevolution: the genomics of cooperation. Trends in Ecology and Evolution 19, 645–653.CrossRefGoogle Scholar
Reed, D. L., Smith, V. S., Hammond, S. L., Rogers, A. R. and Clayton, D. H. ( 2004). Genetic analysis of lice supports direct contact between modern and archaic humans. PLoS Biology 2, e340.CrossRefGoogle Scholar
Reyes, A., Gissi, C., Catzeflis, F., Nevo, E., Pesole, G. and Saccone, C. ( 2004). Congruent mammalian trees from mitochondrial and nuclear genes using Bayesian methods. Molecular Biology and Evolution 21, 397–403.Google Scholar
Rokas, A. and Holland, P. W. ( 2000). Rare genomic changes as a tool for phylogenetics. Trends in Ecology and Evolution 15, 454–459.CrossRefGoogle Scholar
Ryckman, R. R., Bentley, D. G. and Archbold, E. F. ( 1981). The Cimicidae of the Americas and Oceanic islands, a checklist and bibliography. Bulletin of the Society of Vector Ecology 6, 93–142.Google Scholar
Saito, S., Tamura, K. and Aotsuka, T. ( 2005). Replication origin of mitochondrial DNA in insects. Genetics 171, 1695–1705.CrossRefGoogle Scholar
San Mauro, D., Garcia-Paris, M. and Zardoya, R. ( 2004). Phylogenetic relationships of discoglossid frogs (Amphibia[ratio ]Anura[ratio ]Discoglossidae) based on complete mitochondrial genomes and nuclear genes. Gene 343, 357–366.Google Scholar
Scouras, A., Beckenbach, K., Arndt, A. and Smith, M. J. ( 2004). Complete mitochondrial genome DNA sequence for two ophiuroids and a holothuroid: the utility of protein gene sequence and gene maps in the analyses of deep deuterostome phylogeny. Molecular Phylogenetics and Evolution 31, 50–65.CrossRefGoogle Scholar
Shao, R. and Barker, S. C. ( 2003). The highly rearranged mitochondrial genome of the plague thrips, Thrips imaginis (Insecta: Thysanoptera): convergence of two novel gene boundaries and an extraordinary arrangement of rRNA genes. Molecular Biology and Evolution 20, 362–370.CrossRefGoogle Scholar
Shao, R., Aoki, Y., Mitani, H., Tabuchi, N., Barker, S. C. and Fukunaga, M. ( 2004). The mitochondrial genomes of soft ticks have an arrangement of genes that has remained unchanged for over 400 million years. Insect Molecular Biology 13, 219–224.CrossRefGoogle Scholar
Shao, R., Barker, S. C., Mitani, H., Aoki, Y. and Fukunaga, M. ( 2005 a). Evolution of duplicate control regions in the mitochondrial genomes of Metazoa: a case study with Australasian Ixodes ticks. Molecular Biology and Evolution 22, 620–629.Google Scholar
Shao, R., Barker, S. C., Mitani, H., Takahashi, M. and Fukunaga, M. ( 2006). Molecular mechanisms for the variation of mitochondrial gene content and gene arrangement among chigger mites of the genus Leptotrombidium (Acari: Acariformes). Journal of Molecular Evolution 63, 251–261.CrossRefGoogle Scholar
Shao, R., Campbell, N. J. H. and Barker, S. C. ( 2001). Numerous gene rearrangements in the mitochondrial genome of the wallaby louse, Heterodoxus macropus (Phthiraptera). Molecular Biology and Evolution 18, 858–865.CrossRefGoogle Scholar
Shao, R., Mitani, H., Barker, S. C., Takahashi, M. and Fukunaga, M. ( 2005 b). Novel mitochondrial gene content and gene arrangement indicate illegitimate inter-mtDNA recombination in the chigger mite, Leptotrombidium pallidum. Journal of Molecular Evolution 60, 764–773.Google Scholar
Skerratt, L. F., Campbell, N. J., Murrell, A., Walton, S., Kemp, D. and Barker, S. C. ( 2002). The mitochondrial 12S gene is a suitable marker of populations of Sarcoptes scabiei from wombats, dogs and humans in Australia. Parasitology Research 88, 376–379.CrossRefGoogle Scholar
Sprinzl, M., Hartmann, T., Weber, J., Blank, J. and Zeidler, R. ( 1989). Compilation of tRNA sequences and sequences of tRNA genes. Nucleic Acids Research 17 (Suppl.), 1–172.CrossRefGoogle Scholar
Staton, J. L., Daehler, L. L. and Brown, W. M. ( 1997). Mitochondrial gene arrangement of the horseshoe crab Limulus polyphemus L: Conservation of major features among arthropod classes. Molecular Biology and Evolution 14, 867–874.CrossRefGoogle Scholar
Taanman, J. W. ( 1999). The mitochondrial genome: structure, transcription, translation and replication. Biochimica et Biophysica Acta 1410, 103–123.CrossRefGoogle Scholar
Taylor, S. W., Fahy, E. and Ghosh, S. S. ( 2003). Global organellar proteomics. Trends in Biotechnology 21, 82–88.CrossRefGoogle Scholar
Thangaraj, K., Chaubey, G., Kivisild, T., Reddy, A. G., Singh, V. K., Rasalkar, A. A. and Singh, L. ( 2005). Reconstructing the origin of Andaman Islanders. Science 308, 996.CrossRefGoogle Scholar
Thao, M. L., Baumann, L. and Baumann, P. ( 2004). Organization of the mitochondrial genomes of whiteflies, aphids, and psyllids (Hemiptera, Sternorrhyncha). BMC Evolutionary Biology 4, 25.CrossRefGoogle Scholar
Tjensvoll, K., Hodneland, K., Nilsen, F. and Nylund, A. ( 2005). Genetic characterization of the mitochondrial DNA from Lepeophtheirus salmonis (Crustacea; Copepoda). A new gene organization revealed. Gene 353, 218–230.Google Scholar
Wallace, D. C. ( 2002). Animal models for mitochondrial disease. Methods in Molecular Biology 197, 3–54.CrossRefGoogle Scholar
Wolstenholme, D. R. ( 1992). Animal mitochondrial DNA: structure and evolution. International Review of Cytology 141, 173–216.CrossRefGoogle Scholar
Yamazaki, N., Ueshima, R., Terrett, J. A., Yokobori, S., Kaifu, M., Segawa, R., Kobayashi, T., Numachi, K., Ueda, T., Nishikawa, K., Watanabe, K. and Thomas, R. H. ( 1997). Evolution of pulmonate gastropod mitochondrial genomes: Comparisons of gene organizations of Euhadra, Cepaea and Albinaria and implications of unusual tRNA secondary structures. Genetics 145, 749–758.Google Scholar