Register      Login
Invertebrate Systematics Invertebrate Systematics Society
Systematics, phylogeny and biogeography
RESEARCH ARTICLE

Molecular systematics of Australian carrion-breeding blowflies (Diptera : Calliphoridae) based on mitochondrial DNA

J. F. Wallman A E , R. Leys B C and K. Hogendoorn B D
+ Author Affiliations
- Author Affiliations

A Institute for Conservation Biology, School of Biological Sciences, University of Wollongong, New South Wales 2522, Australia.

B Evolutionary Biology Unit, South Australian Museum, North Terrace, Adelaide, South Australia 5000, Australia.

C School of Earth and Environmental Sciences, The University of Adelaide, South Australia 5005, Australia.

D School of Agriculture and Wine, The University of Adelaide, South Australia 5005, Australia.

E Corresponding author. Email: jwallman@uow.edu.au

Invertebrate Systematics 19(1) 1-15 https://doi.org/10.1071/IS04023
Submitted: 13 September 2004  Accepted: 24 December 2004   Published: 6 May 2005

Abstract

Carrion-breeding blowflies have substantial ecological and forensic importance. Because morphological recognition of their immatures is difficult, sequencing of the mtDNA of these flies may assist with their identification. Molecular phylogenetic analysis based on DNA sequences can also clarify evolutionary relationships. In this study, the mitochondrial genes CO1, CO2, ND4 and ND4L were sequenced for 34 species of blowflies, among which are almost all species known or suspected to breed in carrion in Australia. The resulting sequences were analysed using parsimony and maximum-likelihood Bayesian techniques. The results showed that the combination of these four genes should identify most species reliably, although some very closely related taxa could still be misdiagnosed. The data also helped clarify the life histories of Calliphora centralis Malloch, 1927, C. fuscofemorata Malloch, 1927 and C. gilesi Norris, 1994, which have hitherto only been suspected carrion breeders, and revealed that the current subgeneric assignment of taxa within Calliphora Robineau-Desvoidy, based on morphology, requires revision. Unexpectedly, both Chrysomya rufifacies (Macquart, 1843) and Lucilia cuprina (Wiedemann, 1830) were paraphyletic; each probably comprises two distinct species. The application of a molecular-clock approach to the study of the evolutionary divergence of the carrion-breeding blowflies suggests that the speciation of at least the endemic Australian taxa may have been the result of increasing aridification in Australia during the last five million years.

Additional keywords: Calliphora, Chrysomya, evolution, forensic entomology, Hemipyrellia, Lucilia, mtDNA, Onesia.


Acknowledgments

This work was funded by grants to JFW from the Sir Mark Mitchell Research Foundation and the University of Wollongong. We thank Dr S. C. Donnellan for helpful discussion and support of the project through the provision of the facilities of the South Australian Museum’s Evolutionary Biology Unit. We are also grateful to Dr M. S. Archer for kindly providing some of the Victorian specimens for analysis.


References


Aubertin D. (1933) Revision of the genus Lucilia R.-D. (Diptera, Calliphoridae). Zoological Journal of the Linnean Society 38, 389–463. open url image1

Baumgartner D. L. (1993) Review of Chrysomya rufifacies (Diptera: Calliphoridae). Journal of Medical Entomology 30, 338–352.
PubMed | | PubMed |
open url image1

Bezzi M. (1927) Some Calliphoridae (Dipt.) from the South Pacific Islands and Australia. Bulletin of Entomological Research 17, 231–247. open url image1

Bigot J. M. F. (1877) Diptères nouveaux ou peu connus. 8e partie. X. Genre Somomyia (Rondani) Calliphora, Melinda, Mufetia, Lucilia, Chrysomya (alias Microchrysa Rond.) Robineau-Desvoidy. (Suite.) Annales de la Societe Entomologique de France, série 5 7, 243–259. open url image1

Bogdanowicz S. M., Wallner W. E., Bell T. M., 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. open url image1

Bohart G. E., Gressitt J. L. (1951) Filth-inhabiting flies of Guam. Bulletin of the Bernice P. Bishop Museum 204, 1–152. open url image1

Brower A. V. Z. (1994) Rapid morphological radiation and convergence among races of the butterfly Heliconius erato inferred from patterns of mitochondrial DNA evolution. Proceedings of the National Academy of Sciences of the United States of America 91, 6491–6495.
PubMed | | PubMed |
open url image1

Catts E. P., Goff M. L. (1992) Forensic entomology in criminal investigations. Annual Review of Entomology 37, 253–272.
Crossref | GoogleScholarGoogle Scholar | PubMed | PubMed | open url image1

Chen W.-Y., Hung T.-H., Shiao S.-F. (2004) Molecular identification of forensically important blow fly species (Diptera: Calliphoridae) in Taiwan. Journal of Medical Entomology 41, 47–57.
PubMed | | PubMed |
open url image1

Chomczynski P., Mackey K., Drews R., Wilfinger W. (1997) DNAzol®: a reagent for the rapid isolation of genomic DNA. BioTechniques 22, 550–553.
PubMed | | PubMed |
open url image1

Crozier R. H., Crozier Y. C. (1993) The mitochondrial genome of the honeybee Apis mellifera: complete sequence and genome organisation. Genetics 133, 97–117.
PubMed | | PubMed |
open url image1

Cutler D. J. (2000) Estimating divergence times in the presence of an overdispersed molecular clock. Molecular Biology and Evolution 17, 1647–1660.
PubMed | | PubMed |
open url image1

Dear J. P. (1986). ‘Fauna of New Zealand, Vol. 8. Calliphoridae (Insecta: Diptera).’ (Ed. T. Crosby.) (Manaaki Whenua Press: Canterbury, New Zealand.)

Erzinçlioğlu Y. Z. (1984). Studies on the morphology and taxonomy of the immature stages of Calliphoridae, with analysis of phylogenetic relationships within the family, and between it and other groups in the Cyclorrhapha (Diptera). Ph.D. Thesis, University of Durham, UK.

Erzinçlioğlu Y. Z. (1989) The origin of parasitism in blowflies. British Journal of Entomology and Natural History 2, 125–127. open url image1

Fabricius J. C. (1775). ‘Systema entomologiae, sistens insectorvm classes, ordines, genera, species adiectis synonymis, locis, descriptionibvs, observationibvs.’ (Kortii: Flensburg, Germany.)

Fabricius J. C. (1782). ‘Species insectorvm exhibentes eorvm differentias specificas, synonyma, avctorvm loca natalia, metamorphosin adiectis observationibvs, descriptionibvs. Tome II.’ (C. E. Bohnii: Hamburg, Germany.)

Fabricius J. C. (1794). ‘Entomologia systematica emendata et aucta. Secundum classes, ordines, genera, species, adjectis synonimis, locis observationibus, descriptionibus. Tome 4.’ (Copenhagen, Denmark.)

Felsenstein J. (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution; International Journal of Organic Evolution 39, 783–791. open url image1

Greenberg B., and Kunich J. C. (2002). ‘Entomology and the Law: Flies as Forensic Indicators.’ (Cambridge University Press: Cambridge, UK.)

Hardy G. H. (1930) The Queensland species of Calliphora subgenus Neopollenia. Bulletin of Entomological Research 21, 441–448. open url image1

Hardy G. H. (1937) Notes on the genus Calliphora (Diptera). Classification, synonymy, distribution and phylogeny. Proceedings of the Linnean Society of New South Wales 62, 17–26. open url image1

Harvey M. L., Dadour I. R., Gaudieri S. (2003) Mitochondrial DNA cytochrome oxidase I gene: potential for distinction between immature stages of some forensically important fly species (Diptera) in western Australia. Forensic Science International 131, 134–139.
Crossref | GoogleScholarGoogle Scholar | PubMed | PubMed | open url image1

Holdaway F. G. (1933) The synonymy and distribution of Chrysomyia rufifacies (Macq.), an Australian sheep blowfly. Bulletin of Entomological Research 24, 549–560. open url image1

Huang Y.-C., Li W.-F., Lu W., Chen Y.-J., Zhang Y.-P. (2001) Mitochondrial DNA ND4 sequence variation and phylogeny of five species of Bostrychidae (Coleoptera). Acta Entomologica Sinica 44, 494–500. open url image1

Huelsenbeck J. P., Ronquist F. (2001) MrBayes: Bayesian inference of phylogenetic trees. Bioinformatics (Oxford, England) 17, 754–755.
Crossref | GoogleScholarGoogle Scholar | PubMed | PubMed | open url image1

Knowles L. L. (2000) Test of Pleistocene speciation in montane grasshoppers (genus Melanoplus) from the sky islands of western North America. Evolution; International Journal of Organic Evolution 54, 1337–1348.
PubMed | | PubMed |
open url image1

Kurahashi H. (1971) The tribe Calliphorini from Australian and Oriental regions, II. Calliphora-group (Diptera: Calliphoridae). Pacific Insects 13, 141–204. open url image1

Kurahashi H. (1982). Probable origin of a synanthropic fly Chrysomya megacephala, in New Guinea (Diptera: Calliphoridae). In ‘Biogeography and Ecology of New Guinea. Monographiae Biologicae, Vol. 42’. (Ed. J. L. Gressit.) pp. 689–698. (Springer: Heidelberg, Germany.)

Kurahashi H. (1989). Family Calliphoridae. In ‘Catalog of the Diptera of the Australasian and Oceanian Region’. (Ed. N. L. Evenhuis.) pp. 702–718. (Bishop Museum Press: Honolulu, HI, USA.)

Lessinger A. C., Martins Junqueira A. C., Lemos T. A., Kemper E. L., da Silva F. R., Ettore A. L., Arrunda P., Azeredo-Espin A. M. L. (2000) The mitochondrial genome of the primary screwworm fly Cochliomyia hominivorax (Diptera: Calliphoridae). Insect Molecular Biology 9, 521–529.
Crossref | GoogleScholarGoogle Scholar | PubMed | PubMed | open url image1

Leys R., Cooper S. J. B., Schwarz M. P. (2000) Molecular phylogeny of the large carpenter bees, genus Xylocopa (Hymenoptera: Apidae) based on mitochondrial DNA sequences. Molecular Phylogenetics and Evolution 17, 407–418.
Crossref | GoogleScholarGoogle Scholar | PubMed | PubMed | open url image1

Leys R., Cooper S. J. B., Schwarz M. P. (2002) Molecular phylogeny and historical biogeography of the large carpenter bees, genus Xylocopa (Hymenoptera: Apidae). Biological Journal of the Linnean Society 77, 249–266.
Crossref | GoogleScholarGoogle Scholar | open url image1

Leys R., Watts C. H. S., Cooper S. J. B., Humpreys W. S. (2003) Evolution of the subterranean diving beetles (Coleoptera: Dystiscidae: Hydroporini, Bidessini) in the arid zone of Australia. Evolution; International Journal of Organic Evolution 57, 2819–2834.
PubMed | | PubMed |
open url image1

Lunt D. H., Zhang D.-X., Szymura J. M., Hewitt G. M. (1996) The insect cytochrome oxidase I gene: evolutionary patterns and conserved primers for phylogenetic study. Insect Molecular Biology 5, 153–165.
PubMed | | PubMed |
open url image1

Macquart J. (1843) Diptères exotiques nouveaux ou peu connus. Tome deuxième.–3e partie. Mémoires de la Société Royale des Sciences, de l’Agriculture et des Arts de Lille 1842, 162–460. open url image1

Macquart J. (1846) Diptères exotiques nouveaux ou peu connus. Supplément. Mémoires de la Société Royale des Sciences, de l’Agriculture et des Arts de Lille 1844, 133–364. open url image1

Macquart J. (1851) Diptères exotiques nouveaux ou peu connus. Suite du 4.e supplément publié dans les mémoires de 1849. Mémoires de la Société Royale des Sciences, de l’Agriculture et des Arts de Lille 1850, 134–294. open url image1

Macquart J. (1855) Diptères exotiques nouveaux ou peu connus. 5.e supplément. Mémoires de la Société des Sciences, de l’ Agriculture de Lille 1, 25–156. open url image1

Malloch J. R. (1927) Notes on Australian Diptera. XI. Proceedings of the Linnean Society of New South Wales 52, 299–335. open url image1

Malloch J. R. (1932) Notes on Australian Diptera. XXX. Proceedings of the Linnean Society of New South Wales 57, 64–68. open url image1

Markgraf V., McGlone M., Hope G. (1995) Neogene paleoenvironmental and paleoclimatic change in southern temperate ecosystems – a southern perspective. Trends in Ecology & Evolution 10, 143–147.
Crossref | GoogleScholarGoogle Scholar | open url image1

Martin H. A. (1998) Tertiary climatic evolution and the development of aridity in Australia. Proceedings of the Linnean Society of New South Wales 119, 115–136. open url image1

McAlpine J. F. (1970) First record of calyptrate flies in the Mesozoic Era (Diptera, Calliphoridae). Canadian Entomologist 102, 342–346. open url image1

McAlpine J. F. (1989). Phylogeny and classification of the Muscomorpha. In ‘Manual of Nearctic Diptera. Vol. 3’. (Ed. J. F. McAlpine.) pp. 1397–1518. (Research Branch, Agriculture Canada: Canada.)

Meigen J. W. (1826). ‘Systematische Beschreibung der bekannten europäischen zweiflügeligen Insekten. Fünfter Theil.’ (Schulz: Hamm.)

Monzu N. (1977). Coexistence of carrion-breeding Calliphoridae (Diptera) in Western Australia. Ph.D. Thesis, University of Western Australia, Perth, Australia.

Muse S. V., Weir B. S. (1992) Testing equality of evolutionary rates. Genetics 132, 269–276.
PubMed | | PubMed |
open url image1

Norris K. R. (1959). The ecology of sheep blowflies in Australia. In ‘Biogeography and Ecology in Australia’. (Eds A. Keast, R. L. Crocker and C. S. Christian.) Monographiae Biologicae 8, 514–544.

Norris K. R. (1990) Evidence for the multiple exotic origin of Australian populations of the sheep blowfly, Lucilia cuprina (Wiedemann) (Diptera: Calliphoridae). Australian Journal of Zoology 38, 635–648. open url image1

Norris K. R. (1991). General biology. In ‘The Insects of Australia’. (Eds I. D. Naumann, P. B. Carne, J. F. Lawrence, E. S. Nielsen, J. P. Spradbery, R. W. Taylor, M. J. Whitten and M. J. Littlejohn.) pp. 68–108. (Melbourne University Press: Melbourne, Australia.)

Norris K. R. (1994) Three new species of Australian ‘golden blowflies’ (Diptera: Calliphoridae: Calliphora), with a key to described species. Invertebrate Taxonomy 8, 1343–1366.
Crossref | Crossref |
open url image1

O’Flynn M. A., Moorhouse D. E. (1979) Species of Chrysomya as primary flies in carrion. Journal of the Australian Entomological Society 18, 31–32. open url image1

Paramonov S. J. (1959). Zoogeographical aspects of the Australian dipterofauna. In ‘Biogeography and Ecology in Australia’. (Eds A. Keast, R. L. Crocker and C. S. Christian.) Monographiae Biologicae 8, 164–191.

Patton W. S. (1925) Diptera of medical and veterinary importance, II. The more important blowflies, Calliphorinae. Philippine Journal of Science 27, 397–411. open url image1

Patton W. S. (1935) Studies on the higher Diptera of medical and veterinary importance. A revision of the genera of the subfamily Calliphorinae based on a comparative study of the male and female terminalia. The genus Calliphora Robineau-Desvoidy (sens. lat.): a practical guide to the Australian species. Annals of Tropical Medicine and Parasitology 29, 19–32. open url image1

Posada D., Crandall K. A. (1998) MODELTEST: testing the model of DNA substitution. Bioinformatics (Oxford, England) 14, 817–818.
Crossref | GoogleScholarGoogle Scholar | PubMed | PubMed | open url image1

Putman R. J. (1983). ‘Carrion and Dung: Decomposition of Animal Wastes.’ (Edward Arnold (Publishers) Limited: London, UK.)

Robineau-Desvoidy J. B. (1830) Essai sur les myodaires. Mémoires présentés par divers Savans à l’Académie Royale des Sciences de l’Institut de France 2, 1–813. open url image1

Rodríguez F. J., Oliver J. L., Marín A., Medina J. R. (1990) The general stochastic model of nucleotide substitution. Journal of Theoretical Biology 142, 485–501.
PubMed | | PubMed |
open url image1

Rognes K. (1997) The Calliphoridae (blowflies) (Diptera: Oestroidea) are not a monophyletic group. Cladistics 13, 27–66.
Crossref | GoogleScholarGoogle Scholar | open url image1

Sanderson M. J. (1997) A nonparametric approach to estimating divergence times in the absence of rate constancy. Molecular Biology and Evolution 14, 1218–1231. open url image1

Sanderson M. J. (2002a) Estimating absolute times of molecular evolution and divergence times: a penalized likelihood approach. Molecular Biology and Evolution 19, 101–109.
PubMed | | PubMed |
open url image1

Sanderson M. J. (2002b). ‘R8s, Version 1.05 (beta) User’s Manual.’ (University of California: Davis, CA, USA.)

Schiner I. R. (1868). Diptera. In ‘Reise der österreichischen Fregatte Novara um die Erde in den Jahren 1857, 1858, 1859 unter den Befehlen des Commodore B. von Whllerstorf-Urbair. Zoologischer Theil. Zweiter Band. 1. Abtheilung’. (B. K. Gerold’s Sohn: Vienna, Austria.)

Simon C., Frati F., Beckenbach A., Crespi B., Liu H., 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. open url image1

Sorhannus U., Van Bell C. (1999) Testing for equality of molecular evolutionary rates: a comparison between a relative rate test and a likelihood rate test. Molecular Biology and Evolution 16, 849–855. open url image1

Stevens J. R. (2003) The evolution of myiasis in blowflies (Calliphoridae). International Journal for Parasitology 33, 1105–1113.
Crossref | GoogleScholarGoogle Scholar | PubMed | PubMed | open url image1

Stevens J. R., Wall R., Wells J. D. (2002) Paraphyly in Hawaiian hybrid blowfly populations and the evolutionary history of anthrophilic species. Insect Molecular Biology 11, 141–148.
Crossref | GoogleScholarGoogle Scholar | PubMed | PubMed | open url image1

Swederus N. S. (1787) Et nytt genus och femtio nya species af insecter [concl.]. Kungliga Svenska Vetenskapsakademien Handlingar 8, 276–290. open url image1

Swofford D. L. (2001). ‘PAUP: Phylogenetic Analysis Using Parsimony, Version 4.0b8’. (Sinauer Associates: Sunderland, MA, USA.)

Szalanski A. L., Powers T. O. (1996) Molecular diagnostics of three Diabrotica (Coleoptera: Chrysomelidae) pest species. Journal of the Kansas Entomological Society 69, 260–266. open url image1

Tang J., Toe L., Back C., Zimmerman P. A., Oruess K., Unnasch T. R. (1995) The Simulium damnosum species complex: phylogenetic analysis and molecular identification based upon mitochondrially encoded gene sequences. Insect Molecular Biology 4, 79–88. open url image1

Tantawi T. I., Greenberg B. (1993) Chrysomya albiceps and C. rufifacies (Diptera: Calliphoridae): contribution to an ongoing taxonomic problem. Journal of Medical Entomology 30, 646–648.
PubMed |
open url image1

Trewick S. A., Wallis G. P. (2001) Bridging the ‘Beech-gap’: New Zealand invertebrate phylogeography implicates Pleistocene glaciation and Pliocene isolation. Evolution; International Journal of Organic Evolution 55, 2170–2180.
PubMed |
open url image1

Walker F. (1849). ‘List of the Specimens of Dipterous Insects in the Collection of the British Museum. Parts II–IV.’ (British Museum: London, UK.)

Walker F. (1856) Catalogue of the dipterous insects collected in Singapore and Malacca by Mr. A. R. Wallace, with descriptions of new species. Journal of the Proceedings of the Linnean Society of London, Zoology 1, 4–39. open url image1

Wallman J. F. (2001) Third-instar larvae of common carrion-breeding blowflies of the genus Calliphora in South Australia. Invertebrate Taxonomy 15, 37–51.
Crossref | GoogleScholarGoogle Scholar | open url image1

Wallman J. F., Adams M. (1997) Molecular systematics of carrion-breeding blowflies of the genus Calliphora (Diptera: Calliphoridae). Australian Journal of Zoology 45, 337–356.
Crossref | GoogleScholarGoogle Scholar | open url image1

Wallman J. F., Adams M. (2001) The forensic application of allozyme electrophoresis to the identification of blowfly larvae (Diptera: Calliphoridae) in southern Australia. Journal of Forensic Sciences 46, 681–684.
PubMed |
open url image1

Wallman J. F., Donnellan S. C. (2001) The utility of mitochondrial DNA sequences for the identification of forensically important blowflies (Diptera: Calliphoridae) in south-eastern Australia. Forensic Science International 120, 60–67.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Walton C., Sharpe R. G., Pritchard S. J., Thelwell N. J., Butlin R. K. (1999) Molecular identification of mosquito species. Biological Journal of the Linnean Society 68, 241–256.
Crossref | GoogleScholarGoogle Scholar | open url image1

Waterhouse D. F., Paramonov S. J. (1950) The status of the two species of Lucilia (Diptera, Calliphoridae) attacking sheep in Australia. Australian Journal of Scientific Research B 3, 310–336.
Crossref | Crossref |
open url image1

Wells J. D., Sperling F. A. H. (1999) Molecular phylogeny of Chrysomya albiceps and C. rufifacies (Diptera: Calliphoridae). Journal of Medical Entomology 36, 222–226.
Crossref | Crossref | PubMed | PubMed |
open url image1

Wells J. D., Sperling F. A. H. (2001) DNA-based identification of forensically important Chrysomyinae (Diptera: Calliphoridae). Forensic Science International 120, 110–115.
Crossref | GoogleScholarGoogle Scholar | PubMed | PubMed | open url image1

Wiedemann C. R. W. (1819) Beschreibung neuer Zweiflügler aus Ostindien und Afrika. Zoologisches Magazine 1, 1–39. open url image1

Wiedemann C. R. W. (1830). ‘Ausseuropäische zweiflügelige Insekten. Als Fortsetzung des Meigenschen Werkes.’ Erster Theil. (Schulz: Hamm.)

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 | | PubMed |
open url image1

Yu H., Wang W., Zhang Y.-P., Lin F.-J., Geng Z.-C. (1999) Phylogeny and evolution of the Drosophila nasuta subgroup based on mitochondrial ND4 and ND4L gene sequences. Molecular Phylogenetics and Evolution 13, 556–565.
Crossref | GoogleScholarGoogle Scholar | PubMed | PubMed | open url image1

Zherikhin V. V. (2002). Ecological history of the terrestrial insects. In ‘History of Insects’. (Eds A. P. Rasnitsyn and D. L. J. Quicke.) pp. 331–388. (Kluwer: Dordrecht, The Netherlands.)

Zumpt F. (1965). ‘Myiasis in Man and Animals in the Old World.’ (Butterworths: London, UK.)