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Published online on May 24, 2006, 10.1073/pnas.0509590103
PNAS | June 6, 2006 | vol. 103 | no. 23 | 8757-8762


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BIOLOGICAL SCIENCES / EVOLUTION
Amplification of DNA from preserved specimens shows blowflies were preadapted for the rapid evolution of insecticide resistance

C. J. Hartley*,{dagger}, R. D. Newcomb{ddagger}, R. J. Russell*, C. G. Yong{ddagger}, J. R. Stevens§, D. K. Yeates*, J. La Salle*, and J. G. Oakeshott*

*Division of Entomology, Commonwealth Scientific and Industrial Research Organization (CSIRO), P.O. Box 1700, Canberra, ACT 2601, Australia; {ddagger}Horticulture and Food Research Institute of New Zealand, Private Bag 92169, Auckland, New Zealand; and §School of Biosciences, University of Exeter, Prince of Wales Road, Exeter EX4 4PS, United Kingdom

Edited by May R. Berenbaum, University of Illinois at Urbana–Champaign, Urbana, IL, and approved March 31, 2006 (received for review November 6, 2005)

Mutations of esterase 3 confer two forms of organophosphate resistance on contemporary Australasian Lucilia cuprina. One form, called diazinon resistance, is slightly more effective against commonly used insecticides and is now more prevalent than the other form, called malathion resistance. We report here that the single amino acid replacement associated with diazinon resistance and two replacements associated with malathion resistance also occur in esterase 3 in the sibling species Lucilia sericata, suggesting convergent evolution around a finite set of resistance options. We also find parallels between the species in the geographic distributions of the polymorphisms: In both cases, the diazinon-resistance change is absent or rare outside Australasia where insecticide pressure is lower, whereas the changes associated with malathion resistance are widespread. Furthermore, PCR analysis of pinned specimens of Australasian L. cuprina collected before the release of organophosphate insecticides reveals no cases of the diazinon-resistance change but several cases of those associated with malathion resistance. Thus, the early outbreak of resistance in this species can be explained by the preexistence of mutant alleles encoding malathion resistance. The pinned specimen analysis also shows much higher genetic diversity at the locus before organophosphate use, suggesting that the subsequent sweep of diazinon resistance in Australasia has compromised the scope for the locus to respond further to the ongoing challenge of the insecticides.

Lucilia cuprina | Lucilia sericata | mutation | convergent evolution | organophosphates

Author contributions: R.J.R., C.J.H., and J.G.O. designed research; C.J.H., C.G.Y., and J.R.S. performed research; D.K.Y. and J.L.S. contributed new reagents/analytic tools; C.J.H. and R.D.N. analyzed data; and C.J.H., R.D.N., and J.G.O. wrote the paper.

Conflict of interest statement: No conflicts declared.

This paper was submitted directly (Track II) to the PNAS office.

Data deposition: The sequences reported in this paper are variants of esterase 3, as detailed in Figs. 2–4, and have been deposited in the GenBank database (accession no. U56636).

{dagger}To whom correspondence should be addressed. E-mail: carol.hartley{at}csiro.au

© 2006 by The National Academy of Sciences of the USA


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