Multiple Origins of Cyclodiene Insecticide Resistance in Tribolium castaneum (Coleoptera: Tenebrionidae) |
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Authors: | Dmitri Andreev Martin Kreitman Thomas W Phillips Richard W Beeman Richard H ffrench-Constant |
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Institution: | (1) Department of Entomology, 237 Russell Laboratories, 1630 Linden Drive, University of Wisconsin, Madison, WI 53706, USA, US;(2) Department of Ecology and Evolution, University of Chicago, Chicago, IL 60637, USA, US;(3) USDA Tropical Fruit and Vegetable Research Laboratory, P.O. Box 4459, Hilo, HI 96720, USA, US;(4) Grain Marketing and Production Research Center, USDA, ARS, 1515 College Avenue, Manhattan, KS 66502, USA, US |
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Abstract: | The number of origins of pesticide resistance-associated mutations is important not only to our understanding of the evolution
of resistance but also in modeling its spread. Previous studies of amplified esterase genes in a highly dispersive Culex mosquito have suggested that insecticide resistance-associated mutations (specifically a single-gene duplication event) can
occur a single time and then spread throughout global populations. In order to provide data for resistance-associated point
mutations, which are more typical of pesticide mechanisms as a whole, we studied the number of independent origins of cyclodiene
insecticide resistance in the red flour beetle Tribolium castaneum. Target-site insensitivity to cyclodienes is conferred by single point mutations in the gene Resistance to dieldrin (Rdl), which codes for a subunit of a γ-aminobutyric acid (GABA) receptor. These point mutations are associated with replacements
of alanine 302 which render the receptor insensitive to block by the insecticide. We collected 141 strains of Tribolium worldwide and screened them for resistance. Twenty-four strains contained resistant individuals. After homozygosing 23 of
these resistance alleles we derived a nucleotide sequence phylogeny of the resistant strains from a 694-bp section of Rdl, encompassing exon 7 (which contains the resistance-associated mutation) and part of a flanking intron. The phylogeny also
included six susceptible alleles chosen at random from a range of geographical locations. Resistance alleles fell into six
clades and three clades contained both resistant and susceptible alleles. Although statistical analysis provided support at
only the 5–6% level, the pattern of variation in resistance alleles is more readily explained by multiple independent origins
of resistance than by spread of a single resistance-associated mutation. For example, two resistance alleles differed from
two susceptible alleles only by the resistance-associated mutation itself, suggesting that they form the susceptible ancestors
and that resistance arose independently in several susceptible backgrounds. This suggests that in Tribolium Rdl, de novo mutations for resistance have arisen independently in several populations. Identical alleles were found in geographically distant regions as well, also
implying that some Rdl alleles have been exported in stored grain. These differences from the Culex study may stem both from differences in the population genetics of Tribolium versus that of mosquitoes and differences in mutation rates associated with point mutations versus gene duplication events.
The Tribolium data therefore suggest that multiple origins of insecticide resistance (associated with specific point mutations) may be
more common than the spread of single events. These findings have implications for the way in which we model the evolution
and spread of insecticide resistance genes and also suggest that parallel adaptive substitutions may not be uncommon in phyletic
evolution.
Received: 14 October 1998 / Accepted: 4 January 1999 |
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Keywords: | : Mutation rate — Migration — Point mutation — Pesticide resistance — γ -Aminobutyric acid receptor |
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