Hostname: page-component-586b7cd67f-g8jcs Total loading time: 0 Render date: 2024-11-24T09:01:23.611Z Has data issue: false hasContentIssue false
  • English
  • Français

The molecular systematics of blowflies and screwworm flies (Diptera: Calliphoridae) using 28S rRNA, COX1 and EF-1α: insights into the evolution of dipteran parasitism

Published online by Cambridge University Press:  26 August 2011

LAURA M. McDONAGH  and
JAMIE R. STEVENS
LAURA M. McDONAGH
Affiliation:
Biosciences, College of Life and Environmental Sciences, University of Exeter, Stocker Road, Exeter EX4 4QD, UK
JAMIE R. STEVENS*
Affiliation:
Biosciences, College of Life and Environmental Sciences, University of Exeter, Stocker Road, Exeter EX4 4QD, UK
*
*Corresponding author: Dr J. R. Stevens, Biosciences, College of Life and Environmental Sciences, Geoffrey Pope Building, University of Exeter, Stocker Road, Exeter EX4 4QD. Tel: 01392 263775, Fax: 01392 263700; Email: j.r.stevens@exeter.ac.uk
Get access Rights & Permissions [Opens in a new window]

Summary

The Calliphoridae include some of the most economically significant myiasis-causing flies in the world – blowflies and screwworm flies – with many being notorious for their parasitism of livestock. However, despite more than 50 years of research, key taxonomic relationships within the family remain unresolved. This study utilizes nucleotide sequence data from the protein-coding genes COX1 (mitochondrial) and EF1α (nuclear), and the 28S rRNA (nuclear) gene, from 57 blowfly taxa to improve resolution of key evolutionary relationships within the family Calliphoridae. Bayesian phylogenetic inference was carried out for each single-gene data set, demonstrating significant topological difference between the three gene trees. Nevertheless, all gene trees supported a Calliphorinae-Luciliinae subfamily sister-lineage, with respect to Chrysomyinae. In addition, this study also elucidates the taxonomic and evolutionary status of several less well-studied groups, including the genus Bengalia (either within Calliphoridae or as a separate sister-family), genus Onesia (as a sister-genera to, or sub-genera within, Calliphora), genus Dyscritomyia and Lucilia bufonivora, a specialised parasite of frogs and toads. The occurrence of cross-species hybridisation within Calliphoridae is also further explored, focusing on the two economically significant species Lucilia cuprina and Lucilia sericata. In summary, this study represents the most comprehensive molecular phylogenetic analysis of family Calliphoridae undertaken to date.

Keywords

Calliphoridaeblow-flyscrew-wormdipteran parasitismmyiasishybridizationphylogenetics
Type
Research Article
Information
Parasitology , Volume 138 , Special Issue 13: Systematics as a cornerstone of parasitology , November 2011 , pp. 1760 - 1777
Copyright
Copyright © Cambridge University Press 2011

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

Alfaro, M. E., Zoller, S. and Lutzoni, F. (2003). Bayes or bootstrap? A simulation study comparing the performance of Bayesian Markov chain Monte Carlo sampling and bootstrapping in assessing phylogenetic confidence. Molecular Biology and Evolution 20, 255–266.CrossRefGoogle ScholarPubMed
Aljanabi, S. M. and Martinez, I. (1997). Universal and rapid salt-extraction of high quality genomic DNA for PCR-based techniques. Nucleic Acids Research 25, 4692–4693.CrossRefGoogle ScholarPubMed
Aubertin, D. (1933). Revision of the genus Lucilia R.-D. (Diptera, Calliphoridae). Journal of the Linnean Society of London, Zoology 38, 389–463.CrossRefGoogle Scholar
Avise, J. C., Giblin-Davidson, C., Laerm, J., Patton, J. C. and Lansman, R. A. (1979). The use of restriction endonucleases to measure mitochondrial DNA sequence relatedness in natural populations II: Mitochondrial DNA clones and matriarchal phylogeny within and among geographic populations of the pocket gopher, Geomys pinetis. Proceedings of the National Academy of Sciences, USA 76, 6694–6698.CrossRefGoogle Scholar
Baker, R. H., Wilkinson, G. S. and DeSalle, R. (2001). Phylogenetic utility of different types of data used to infer evolutionary relationships among stalk-eyed flies (Diopsidae). Systematic Biology 50, 87–105.CrossRefGoogle ScholarPubMed
Bishop, F. (1913). The stable fly (Stomoxys calcitrans L.): An important live stock pest. Journal of Economic Entomology 6, 112–126.CrossRefGoogle Scholar
Boakye, D. A. and Meredith, S. E. O. (1993). Introgression between members of the Simulium damnosum complex: Larvicidal implications. Medical and Veterinary Entomology 7, 393–397.CrossRefGoogle ScholarPubMed
Bogdanowicz, S. M., Wallner, W. E., Bell, J., Odell, T. M. and Harrison, R. G. (1993). Asian gypsy moths (Lepidoptera: Lymantriidae) in North America: Evidence from molecular data. Annals of the Entomological Society of America 86, 710–715.CrossRefGoogle Scholar
Brooks, D. R., Bilewitch, J., Condy, C., Evans, D. E., Folinsbee, K. E., Fröbisch, J., Halas, D., Hill, S., McLennan, D. A., Mattern, M., Tsuji, L. A., Ward, J. L., Wahlberg, N., Zamparo, D. and Zanatta, D. (2007). Quantitative phylogenetic analysis in the 21st Century. Revista Mexicana de Biodiversidad 78, 225–252.Google Scholar
Brower, A. V. Z. and DeSalle, R. (1994). Practical and theoretical considerations for choice of a DNA sequence region in insect molecular systematics, with a short review of published studies using nuclear gene regions. Annals of the Entomological Society of America 87, 702–716.CrossRefGoogle Scholar
Brumpt, E. (1934). Recherches experimentales sur la biologie de la Lucilia bufonivora. Annals of Parasitology 12, 81–97.Google Scholar
Chen, W. Y., Hung, T. H. and Shiao, S. F. (2004). Molecular identification of forensically important blow fly species (Diptera: Calliphoridae) in Taiwan. Journal of Medical Entomology 41, 47–57.CrossRefGoogle ScholarPubMed
Collins, K. P. and Wiegmann, B. M. (2002). Phylogenetic relationships of the lower Cyclorrhapha (Diptera: Brachycera) based on 28S rDNA sequences. Insect Systematics and Evolution 33, 445–456.CrossRefGoogle Scholar
D'Assis Fonseca, E. C. M. (1968). Diptera Cyclorrhapha Calyptrata: Muscidae. Handbooks for the Identification of British Insects, No. 10. Royal Entomological Society of London, London, England.Google Scholar
Danforth, B. N. and Ji, S. Q. (1998). Elongation factor-1 alpha occurs as two copies in bees: Implications for phylogenetic analysis of EF-1 alpha sequences in insects. Molecular Biology and Evolution 15, 225–235.CrossRefGoogle ScholarPubMed
Dear, J. P. (1985 a). Calliphoridae (Insecta: Diptera). Fauna of New Zealand, No. 8. Department of Scientific and Industrial Research, Wellington, New Zealand.Google Scholar
Dear, J. P. (1985 b). A revision of the New World Chrysomyini (Diptera: Calliphoridae). Revista Brasileira de Zoologia 3, 109–169.CrossRefGoogle Scholar
Dogra, S. S. and Mahajan, V. K. (2010). Oral myiasis caused by Musca domestica larvae in a child. International Journal of Pediatric Otorhinolaryngology Extra 5, 105–107.CrossRefGoogle Scholar
Dowton, M. (2004). Assessing the relative rate of (mitochondrial) genomic change. Genetics 167, 1027–1030.CrossRefGoogle ScholarPubMed
Eaton, B. R., Moenting, A. E., Paszkowski, C. A. and Shpeley, D. (2008). Myiasis by Lucilia silvarum (Calliphoridae) in amphibian species in boreal Alberta, Canada. Journal of Parasitology 94, 949–952.CrossRefGoogle ScholarPubMed
Edgar, R. C. (2004). MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research 32, 1792–1797.CrossRefGoogle ScholarPubMed
Foster, G. G. (1989). The sheep blowfly genetic control program in Australia. FAO/IAEA Insect and Pest Control Newsletter 43, 23–26.Google Scholar
Foster, G. G. (1991). Simulation of genetic control: homozygous-viable pericentric inversions in field-female killing systems. Theoretical and Applied Genetics 82, 368–378.CrossRefGoogle ScholarPubMed
Foster, G. G., Vogt, W. G. and Woodburn, T. L. (1985). Genetic analysis of field trials of sex-linked translocation strains for genetic control of the Australian sheep blowfly Lucilia cuprina (Wiedemann). Australian Journal of Biological Sciences 38, 275–293.CrossRefGoogle ScholarPubMed
Foster, G. G., Vogt, W. G., Woodburn, T. L. and Smith, P. H. (1988). Computer simulation of genetic control: Comparison of sterile males and field-female killing systems. Theoretical and Applied Genetics 76, 870–879.CrossRefGoogle ScholarPubMed
Friedlander, T. P., Regier, J. C. and Mitter, C. (1992). Nuclear gene sequences for higher level phylogenetic analysis: 14 promising candidates. Systematic Biology 41, 483–490.CrossRefGoogle Scholar
Friedlander, T. P., Regier, J. C. and Mitter, C. (1994). Phylogenetic information content of five nuclear gene sequences in animals: Initial assessment of character sets from concordance and divergence studies. Systematic Biology 43, 511–525.CrossRefGoogle Scholar
Friedrich, M. and Tautz, D. (1997 a). An episodic change of rDNA nucleotide substitution rate has occurred during the emergence of the insect order Diptera. Molecular Biology and Evolution 14, 644–653.CrossRefGoogle ScholarPubMed
Friedrich, M. and Tautz, D. (1997 b). Evolution and phylogeny of the diptera: A molecular phylogenetic analysis using 28S rDNA sequences. Systematic Biology 46, 674–698.CrossRefGoogle ScholarPubMed
Fuller, M. E. (1934) The insect inhabitants of carrion: a study in animal ecology. Bulletin of the Council for Scientific and Industrial Research (Australia) 82, 1–63.Google Scholar
Funk, D. J. and Omland, K. E. (2003). Species-level paraphyly and polyphyly: frequency, causes, and consequences, with insights from animal mitochondrial DNA. Annual Review of Ecology Evolution and Systematics 34, 397–423.CrossRefGoogle Scholar
Galtier, N., Gouy, M. and Gautier, C. (1996). SEAVIEW and PHYLO_WIN: Two graphic tools for sequence alignment and molecular phylogeny. Computer Applications in the Biosciences 12, 543–548.Google ScholarPubMed
Gleeson, D. M. and Sarre, S. (1997). Mitochondrial DNA variability and geographic origin of the sheep blowfly, Lucilia cuprina (Diptera: Calliphoridae), in New Zealand. Bulletin of Entomological Research 87, 265–272.CrossRefGoogle Scholar
Hall, D. G. (1948) The Blowflies of North America. The Thomas Say Foundation, Lafayette, Indiana, USA.CrossRefGoogle Scholar
Hardy, G. H. (1937). Notes on the genus Calliphora (Diptera). Proceedings of the Linnean Society of New South Wales 62, 17–26.Google Scholar
Harvey, M. L., Gaudieri, S., Villet, M. H. and Dadour, I. R. (2008). A global study of forensically significant calliphorids: Implications for identification. Forensic Science International 177, 66–76.CrossRefGoogle ScholarPubMed
Harvey, M. L., Mansell, M. W., Villet, M. H. and Dadour, I. R. (2003). Molecular identification of some forensically important blowflies of southern Africa and Australia. Medical and Veterinary Entomology 17, 363–369.CrossRefGoogle ScholarPubMed
Hillis, D. M. and Bull, J. J. (1993). An empirical test of bootstrapping as a method for assessing confidence in phylogenetic analysis. Systematic Biology 42, 182–192.CrossRefGoogle Scholar
Hoelzel, A. R. and Green, A. (1992). Analysis of population-level variation by sequencing PCR-amplified DNA. In Molecular Genetic Analysis of Populations: A Practical Approach (Ed. Hoelzel, A. R.), pp. 159–187. Oxford University Press, Oxford, UK.Google Scholar
Holloway, B. A. (1991 a). Identification of third-instar larvae of flystrike and carrion-associated blowflies in New Zealand (Diptera: Calliphoridae). New Zealand Entomologist 14, 24–28.CrossRefGoogle Scholar
Holloway, B. A. (1991 b). Morphological characters to identify adult Lucilia sericata (Meigen, 1826) and Lucilia cuprina (Wiedemann, 1830) (Diptera: Calliphoridae). New Zealand Journal of Zoology 18, 415–420.CrossRefGoogle Scholar
Hovemann, B., Richter, S., Walldorf, U. and Cziepluch, C. (1988). Two genes encode related cytoplasmic elongation factors 1 alpha (EF-1 alpha) in Drosophila melanogaster with continuous and stage specific expression. Nucleic Acids Research 16, 3175–3194.CrossRefGoogle ScholarPubMed
Huelsenbeck, J. P. and Ronquist, F. (2001). MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17, 754–755.CrossRefGoogle ScholarPubMed
Iwasa, M. and Ishiguro, N. (2010). Genetic and morphological differences of Haematobia irritans and H. exigua, and molecular phylogeny of Japanese Stomoxyini flies (Diptera, Muscidae). Medical Entomology and Zoology 61, 335–344.CrossRefGoogle Scholar
James, M. T. (1947). The Flies that Cause Myiasis in Man. US Department of Agriculture, Miscellaneous Publication 631, Washington D.C.CrossRefGoogle Scholar
James, M. T. (1955). The blowflies of California (Diptera: Calliphoridae). Bulletin of the California Insect Survey Vol. 4, No. 1.Google Scholar
James, M. T. (1981) Genus DYSCRITOMYIA Grimshaw. In A Manual of the Insects of the Hawaiian Islands, including an Enumeration of the Species and Notes on their Origin, Distribution, Hosts, Parasites, etc. (Hardy, D. E.) Vol. 14, 294–349. The University Press of Hawaii, Honolulu, Hawaii, USA.Google Scholar
Karpa, A., Petrova, V. and Čudare, Z. (2007). Study of Diptera fauna (Nematocera, Brachycera) from the strawberry plantings. Acta Biologica Universitatis Daugavpilensis 7, 175–180.Google Scholar
Kutty, S. N., Pape, T., Pont, A., Wiegmann, B. M. and Meier, R. (2008). The Muscoidea (Diptera: Calyptratae) are paraphyletic: Evidence from four mitochondrial and four nuclear genes. Molecular Phylogenetics and Evolution 49, 639–652.CrossRefGoogle ScholarPubMed
Lehrer, A. Z. (2003). Bengaliidae n. fam. Une nouvelle famille de Diptera Cyclorrhpha. Entomologia Croatica 7, 5–14.Google Scholar
Leonard, S. A. (2003). IUPAC/IUB single-letter codes within nucleic acid and amino acid sequences. Current Protocols in Bioinformatics, Appendix 1A.CrossRefGoogle Scholar
Lin, C. P. and Danforth, B. N. (2004). How do insect nuclear and mitochondrial gene substitution patterns differ? Insights from Bayesian analyses of combined datasets. Molecular Phylogenetics and Evolution 30, 686–702.CrossRefGoogle ScholarPubMed
Lunt, D. H., Zhang, D.-X., Szymura, J. M. and Hewitt, G. M. (1996). The insect cytochrome oxidase I gene: Evolutionary patterns and conserved primers for phylogenetic studies. Insect Molecular Biology 5, 153–165.CrossRefGoogle ScholarPubMed
Mallet, J. (2005). Hybridization as an invasion of the genome. Trends in Ecology and Evolution 20, 229–237.CrossRefGoogle ScholarPubMed
McDonagh, L., García, R. and Stevens, J. R. (2009). Phylogenetic analysis of New World screwworm fly, Cochliomyia hominivorax, suggests genetic isolation of some Caribbean island populations following colonization from South America. Medical and Veterinary Entomology 23 (Suppl. 1), 14–22.CrossRefGoogle ScholarPubMed
Meier, R., Kotrba, M. and Ferrar, P. (1999). Ovoviviparity and viviparity in the Diptera. Biological Reviews of the Cambridge Philosophical Society 74, 199–258.CrossRefGoogle Scholar
Monteiro, A. and Pierce, N. E. (2001). Phylogeny of Bicyclus (Lepidoptera: Nymphalidae) inferred from COI, COII, and EF-1 alpha gene sequences. Molecular Phylogenetics and Evolution 18, 264–281.CrossRefGoogle Scholar
Moulton, J. K. (2000). Molecular sequence data resolves basal divergences within Simuliidae (Diptera). Systematic Entomology 25, 95–113.CrossRefGoogle Scholar
Nelder, M. P., McCreadie, J. W. and Major, C. S. (2009). Blow flies visiting decaying alligators: is succession synchronous or asynchronous? Psyche: A Journal of Entomology. Article ID 575362, 7 pages, 2009. doi:10.1155/2009/575362.CrossRefGoogle Scholar
Nelson, L. A., Wallman, J. F. and Dowton, M. (2007). Using COI barcodes to identify forensically and medically important blowflies. Medical and Veterinary Entomology 21, 44–52.CrossRefGoogle ScholarPubMed
Neumann, V. and Meyer, F. (2008). Lucilia bufonivora Moniez, 1876 – an euryxene parasite of amphibians (Insecta: Diptera: Calliphoridae). Mitteilungen aus dem Museum für Naturkunde in Berlin. Zoologisches Museum und Institut für Spezielle Zoologie (Berlin) 70, 331–341.CrossRefGoogle Scholar
Norris, K. R. (1991). General biology. In The Insects of Australia. (Eds. Naumann, I. D., Carne, P. B., Lawrence, J. F., Nielsen, E. S., Spradberry, J. P., Taylor, R. W., Whitten, M. J. and Littlejohn, M. J.). Melbourne University Press, Melbourne, Australia.Google Scholar
Otranto, D. and Stevens, J. R. (2002). Molecular approaches to the study of myiasis-causing larvae. International Journal for Parasitology 32, 1345–1360.CrossRefGoogle Scholar
Otranto, D., Traversa, D., Milillo, P., De Luca, F. and Stevens, J. (2005). Utility of mitochondrial and ribosomal genes for differentiation and phylogenesis of species of gastrointestinal bot flies. Journal of Economic Entomology 98, 2235–2245.CrossRefGoogle ScholarPubMed
Park, S. H., Zhang, Y., Piao, H., Yu, D. H., Jeong, H. J., Yoo, G. Y., Chung, U., Jo, T.-H. and Hwang, J.-J. (2009). Use of cytochrome c oxidase subunit I (COI) nucleotide sequences for identification of the Korean Luciliinae fly species (Diptera: Calliphoridae) in forensic investigations. Journal of Korean Medical Science 24, 1058–1063.CrossRefGoogle Scholar
Parr, H. C. M. (1962). Studies on Stomoxys calcitrans (L.) in Uganda, East Africa. II. – Notes on life-history and behaviour. Bulletin of Entomological Research 53, 437–443.CrossRefGoogle Scholar
Petersen, F. T., Meier, R., Kutty, S. N. and Wiegmann, B. M. (2007). The phylogeny and evolution of host choice in the Hippoboscoidea (Diptera) as reconstructed using four molecular markers. Molecular Phylogenetics and Evolution 45, 111–122.CrossRefGoogle ScholarPubMed
Pollock, J. N. (1974). Comparative notes on adaptations for viviparity shown by Dyscritomyia (Calliphoridae, Diptera) of Hawaii, and Glossina (Glossinidae, Diptera). Proceedings of the Hawaiian Entomological Society 21, 447–455.Google Scholar
Posada, D. and Crandall, K. A. (1998). Modeltest: Testing the model of DNA substitution. Bioinformatics 14, 817–818.CrossRefGoogle ScholarPubMed
Rognes, K. (1991). Blowflies (Diptera, Calliphoridae) of Fennoscandia and Denmark. Fauna Entomologica Scandinavica, Volume 24. E. J. Brill/Scandinavian Science Press Ltd., Leiden, The Netherlands.CrossRefGoogle Scholar
Rognes, K. (1997). The Calliphoridae (Blowflies) (Diptera: Oestroidea) are not a monophyletic group. Cladistics 13, 27–66.CrossRefGoogle Scholar
Rognes, K. (1998). Family Calliphoridae, Ch. 3.51. In Contributions to a Manual of Palaearctic Diptera (Eds. Papp, L. and Darvas, B.) Vol. 3, 617–648. Science Herald, Budapest, Hungary.Google Scholar
Rognes, K. (2005). Bengalomania – A review of Andy Z. Lehrer's book on Bengalia Robineau-Desvoidy, 1830 and related works (Diptera, Calliphoridae). Studia Dipterologica 12, 443–471.Google Scholar
Rognes, K. and Paterson, H. E. H. (2005). Chrysomya chloropyga (Wiedemann, 1818) and C. putoria (Wiedemann, 1830) (Diptera: Calliphoridae) are two different species. African Entomology 13, 49–70.Google Scholar
Ronquist, F., Huelsenbeck, J. P. and van der Mark, P. (2005). MrBayes 3.1, Manual (http://mrbayes.scs.fsu.edu/manual.php).Google Scholar
Sabrosky, C. W., Bennett, G. F. and Whitworth, T. L. (1989). Bird blow flies (Protocalliphora) in North America (Diptera: Calliphoridae), with notes on Palearctic species. Smithsonian Institution Press, Washington D.C.CrossRefGoogle Scholar
Scott, M. J., Heinrich, J. C. and Li, X. L. (2004). Progress towards the development of a transgenic strain of the Australian sheep blowfly (Lucilia cuprina) suitable for a male-only sterile release program. Insect Biochemistry and Molecular Biology 34, 185–192.CrossRefGoogle ScholarPubMed
Shah, Z. A. and Sakhawat, T. (2004). The effect of flesh age, trap colour, decomposition stage, temperature and relative humidity on the visitation pattern of blow and flesh flies. International Journal of Agriculture and Biology 6, 370–374.Google Scholar
Shao, R. and Barker, S. C. (2007). Mitochondrial genomes of parasitic arthropods: implications for studies of population genetics and evolution. Parasitology 134, 153–167.CrossRefGoogle ScholarPubMed
Shewell, G. E. (1987). Calliphoridae. In Manual of Nearctic Diptera. (Eds. McAlpine, J. F., Peterson, B. V., Shewell, G. E., Teskey, H. J., Vockeroth, J. R., Wood, D. M.) Chapter 106, 2, 1133–1145. Research Branch, Agriculture Canada, Ottawa, Canada.Google Scholar
Simon, C., Frati, F., Beckenbach, A., Crespi, B., Liu, H. and Flook, P. (1994). Evolution, weighting, and phylogenetic utility of mitochondrial gene-sequences and a compilation of conserved polymerase chain-reaction primers. Annals of the Entomological Society of America 87, 651–701.CrossRefGoogle Scholar
So, P. and Dudgeon, D. (1989). Larval growth dynamics of Hemipyrellia ligurriens (Calliphoridae) and Boettcherisca formosensis (Sarcophagidae) in crowded and uncrowded cultures. Researches on Population Ecology 31, 113–122.CrossRefGoogle Scholar
Sperling, F. A. H., Anderson, G. S. and Hickey, D. A. (1994). A DNA-based approach to the identification of insect species for postmortem interval estimation. Journal of Forensic Sciences 39, 418–427.CrossRefGoogle Scholar
Sperling, F. A. H. and Hickey, D. A. (1994). Mitochondrial sequence variation in the spruce budworm species complex (Choristoneura: Lepidoptera). Molecular Biology and Evolution 11, 656–665.Google ScholarPubMed
Sperling, F. A. H., Landry, J.-F. and Hickey, D. A. (1995). DNA-based identification of introduced ermine moth species in North America (Lepidoptera: Yponomeutidae). Annals of the Entomological Society of America 88, 155–162.CrossRefGoogle Scholar
Spradbery, J. P. (1991) A Manual for the Diagnosis of Screw-Worm Fly. CSIRO, Australian Government Publishing Service, Canberra, Australia.Google Scholar
Stevens, J. R. (2003). The evolution of myiasis in blowflies (Calliphoridae). International Journal for Parasitology 33, 1105–1113.CrossRefGoogle ScholarPubMed
Stevens, J. and Wall, R. (1996 a). Classification of the genus Lucilia (Diptera: Calliphoridae): a preliminary parsimony analysis. Journal of Natural History 30, 1087–1094.CrossRefGoogle Scholar
Stevens, J. and Wall, R. (1996 b). Species, sub-species and hybrid populations of the blowflies Lucilia cuprina and Lucilia sericata (Diptera: Calliphoridae). Proceedings of the Royal Society of London Series B 263, 1335–1341.Google ScholarPubMed
Stevens, J. and Wall, R. (1997 a). The evolution of ectoparasitism in the genus Lucilia (Diptera: Calliphoridae). International Journal for Parasitology 27, 51–59.CrossRefGoogle ScholarPubMed
Stevens, J. and Wall, R. (1997 b). Genetic variation in populations of the blowflies Lucilia cuprina and Lucilia sericata (Diptera: Calliphoridae). Random amplified polymorphic DNA analysis and mitochondrial DNA sequences. Biochemical Systematics and Ecology 25, 81–97.CrossRefGoogle Scholar
Stevens, J. and Wall, R. (2001). Genetic relationships between blowflies (Calliphoridae) of forensic importance. Forensic Science International 120, 116–123.CrossRefGoogle ScholarPubMed
Stevens, J. R., Wall, R., Wells, J. D. (2002). Paraphyly in Hawaiian hybrid blowfly populations and the evolutionary history of anthropophilic species. Insect Molecular Biology 11, 141–148.CrossRefGoogle ScholarPubMed
Stevens, J. R. and Wallman, J. F. (2006). The evolution of myiasis in humans and other animals in the Old and New Worlds (part I): phylogenetic analyses. Trends in Parasitology 22, 129–136.CrossRefGoogle ScholarPubMed
Stevens, J. R., Wallman, J. F., Otranto, D., Wall, R. and Pape, T. (2006). The evolution of myiasis in humans and other animals in the Old and New Worlds (part II): biological and life-history studies. Trends in Parasitology 22, 181–188.CrossRefGoogle ScholarPubMed
Stevens, J. R., West, H. and Wall, R. (2008). Mitochondrial genomes of the sheep blowfly, Lucilia sericata, and the secondary blowfly, Chrysomya megacephala. Medical and Veterinary Entomology 22, 89–91.CrossRefGoogle ScholarPubMed
Stireman, J. R. (2002). Phylogenetic relationships of tachinid flies in subfamily Exoristinae (Tachinidae: Diptera) based on 28S rDNA and elongation factor-1alpha. Systematic Biology 27, 409–435.Google Scholar
Strijbosch, H. (1980). Mortality in a population of Bufo bufo resulting from the fly Lucilia bufonivora. Ocecologia 45, 285–286.CrossRefGoogle Scholar
Sukontason, K. L., Sribanditmongkol, P., Chaiwong, T., Vogtsberger, R. C., Piangjai, S. and Sukontason, K. (2008). Morphology of immature stages of Hemipyrellia ligurriens (Wiedemann) (Diptera: Calliphoridae) for use in forensic entomology applications. Parasitology Research 103, 877–887.CrossRefGoogle ScholarPubMed
Swofford, D. L. (1998). PAUP*. Phylogenetic Analysis Using Parsimony (* and Other Methods), Version 4. Sunderland, M.A., Sinauer Associates.Google Scholar
Tourle, R., Downie, D. A. and Villet, M. H. (2009). Flies in the ointment: a morphological and molecular comparison of Lucilia cuprina and Lucilia sericata (Diptera: Calliphoridae) in South Africa. Medical and Veterinary Entomology 23, 6–14.CrossRefGoogle ScholarPubMed
Townsend, C. H. T. (1935). Muscoid classification and habits. In Manual of Myiology, Part II. (Eds. Townsend, C. H. T. and Filhos, I.), pp. 164–172. Itaquaquecetuba, Sao Paulo, Brazil.Google Scholar
Ullyett, G. C. (1945). Species of Lucilia attacking sheep in South Africa. Nature 155, 636–637.CrossRefGoogle Scholar
van Emden, F. I. (1954). Diptera: Cyclorrhapha Calyptrata (I) Sect (a) Tachinidae and Calliphoridae. Vol X. Part 4(a). The Royal Entomological Society of London (RES).Google Scholar
Wallman, J. F. (2001). A key to the adults of species of blowflies in southern Australia known or suspected to breed in carrion. Medical and Veterinary Entomology 15, 433–437.CrossRefGoogle ScholarPubMed
Wallman, J. F. and Adams, M. (1997). Molecular systematics of Australian carrion-breeding blowflies of the genus Calliphora (Diptera: Calliphoridae). Australian Journal of Zoology 45, 337–356.CrossRefGoogle Scholar
Wallman, J. F. and Donnellan, S. C. (2001). The utility of mitochondrial DNA sequences for the identification of forensically important blowflies (Diptera: Calliphoridae) in southeastern Australia. Forensic Science International 120, 60–67.CrossRefGoogle ScholarPubMed
Wallman, J. F., Leys, R. and Hogendoorn, K. (2005). Molecular systematics of Australian carrion-breeding blowflies (Diptera: Calliphoridae) based on mitochondrial DNA. Invertebrate Systematics 19, 1–15.CrossRefGoogle Scholar
Weddeling, K. and Kordges, T. (2008). Lucilia bufonivora-Befall (Myiasis) bei Amphibien in Nordrhein-Westfalen – Verbreitung, Wirtsarten, Ökologie und Phänologie [Lucilia bufonivora infestation (myiasis) of amphibians in NorthRhine-Westphalia – distribution, host species, ecology and phenology]. Zeitschrift für Feldherpetologie 15, 183–202.Google Scholar
Wells, J. D., Goff, M. L., Tomberlin, J. K. and Kurahashi, H. (2002). Molecular systematics of the endemic Hawaiian blowfly genus Dyscritomyia Grimshaw, (Diptera: Calliphoridae). Medical Entomology and Zoology 53, 231–238.CrossRefGoogle Scholar
Wells, J. D., Introna, F. Jr, Di Vella, G., Campobasso, C. P., Hayes, J. and Sperling, F. A. (2001). Human and insect mitochondrial DNA analysis from maggots. Journal of Forensic Science 46, 685–687.CrossRefGoogle ScholarPubMed
Wells, J. D., Lunt, N. and Villet, M. H. (2004). Recent African derivation of Chrysomya putoria from C. chloropyga and mitochondrial DNA paraphyly of cytochrome oxidase subunit one in blowflies of forensic importance. Medical and Veterinary Entomology 18, 445–448.CrossRefGoogle Scholar
Wells, J. D. and Sperling, F. A. H. (1999). Molecular phylogeny of Chrysomya albiceps and C. rufifacies (Diptera: Calliphoridae). Journal of Medical Entomology 36, 222–226.CrossRefGoogle Scholar
Wells, J. D. and Sperling, F. A. (2001). DNA-based identification of forensically important Chrysomyinae (Diptera: Calliphoridae). Forensic Science International 120, 110–115.CrossRefGoogle ScholarPubMed
Wells, J. D., Wall, R. and Stevens, J. R. (2007). Phylogenetic analysis of forensically important Lucilia flies based on cytochrome oxidase I sequence: a cautionary tale for forensic species determination. International Journal of Legal Medicine 121, 229–233.CrossRefGoogle ScholarPubMed
Whitten, M. J. (1979). The use of genetically selected strains for pest replacement or suppression. In Genetics in Relation to Insect Management (Eds. Hoy, M. A. and McKelvey, J. J.), pp. 31–40. The Rockefeller Foundation, New York.Google Scholar
Whitten, M. J., Foster, G. G., Vogt, W. G., Kitching, R. L., Woodburn, T. L. and Konovalov, C. (1977). Current status of genetic control of the Australian sheep blowfly, Lucilia cuprina Wiedemann (Diptera: Calliphoridae). Proceedings XV International Congress of Entomology, Washington, D.C. 129–139.Google Scholar
Wiegmann, B. M. et al. (2011). Episodic radiations in the fly tree of life. Proceedings of the National Academy of Sciences, USA 108, 5690–5695.CrossRefGoogle ScholarPubMed
Wilcox, T. P., Zwickl, D. J., Heath, T. A. and Hillis, D. M. (2002). Phylogenetic relationships of the dwarf boas and a comparison of Bayesian and bootstrap measures of phylogenetic support. Molecular Phylogenetics and Evolution 25, 361–371.CrossRefGoogle Scholar
Zumpt, F. (1956). Calliphoridae (Diptera Cyclorrhapha) Part 1: Calliphorini and Chrysomyiini. Exploration du Parc National Albert, Mission G. F. de Witte (1933–1935). Bruxelles.Google Scholar
Zumpt, F. (1965). Myiasis in Man and Animals in the Old World. Butterworths, London.Google Scholar
Supplementary material: File

McDonagh Supplementary Data 1

Supplementary Data File 1. EF1-alpha data

Download McDonagh Supplementary Data 1(File)
File 130 KB
Supplementary material: File

McDonagh Supplementary Data 2

Supplementary Data File 2. COX1 data

Download McDonagh Supplementary Data 2(File)
File 167.9 KB
Supplementary material: File

McDonagh Supplementary Data 3

Supplementary Data File 3. 28S rRNA data

Download McDonagh Supplementary Data 3(File)
File 220.7 KB