Insecticide resistance is one of the most widespread genetic changes caused by human activity, but we still understand little about the origins and spread of resistant alleles in global populations of insects. Here, via microarray analysis of all P450s in Drosophila melanogaster , we show that DDT-R , a gene conferring resistance to DDT, is associated with overtranscription of a single cytochrome P450 gene, Cyp6g1 . Transgenic analysis of Cyp6g1 shows that overtranscription of this gene alone is both necessary and sufficient for resistance. Resistance and up-regulation in Drosophila populations are associated with a single Cyp6g1 allele that has spread globally. This allele is characterized by the insertion of an Accord transposable element into the 5′ end of the Cyp6g1 gene.

Significance: This research uncovers the mechanisms of an ancient arms race between butterflies and plants, seen today in countless gardens as caterpillars of cabbage butterflies that devour cabbage crop varieties. Nearly 90 million years ago, the ancestors of Brassica (mustards, cabbage) and related plants developed a chemical defense called glucosinolates. While very toxic to most insects, humans experience glucosinolates as the sharp taste in wasabi, horseradish and mustard. Here we report that this triggered a chemical arms race that escalated in complexity over time. By investigating the evolutionary histories of these plants and insects, we found that major increases in chemical defense complexity were followed by butterflies evolving countertactics to allow them to continue to attack and feed on the plants.

Transgenic crops producing insecticidal toxins from Bacillus thuringiensis (Bt) are widely used for pest control. Bt-resistant insect strains have been studied, but the molecular basis of resistance has remained elusive. Here, we show that disruption of a cadherin-superfamily gene by retrotransposon-mediated insertion was linked to high levels of resistance to the Bt toxin Cry1Ac in the cotton pest Heliothis virescens . Monitoring the early phases of Bt resistance evolution in the field has been viewed as crucial but extremely difficult, especially when resistance is recessive. Our findings enable efficient DNA-based screening for resistant heterozygotes by directly detecting the recessive allele.

Bypassing a plant's defense for pest defense: Colorado potato beetles can skeletonize the leaves on a potato plant, devastating crop yields. Insecticides are increasingly useless as the beetle evolves resistance. Zhang et al. used RNA interference to take down this beetle (see the Perspective by Whyard). Success required shifting production of the double-stranded RNA to the plastids to evade the plant's own RNA management mechanisms. The insect's own RNA interference mechanisms then inactivated two everyday genes that the beetle can't do without. Science , this issue p. 991 ; see also p. 950

Evolution of resistance by pests is the main threat to long-term insect control by transgenic crops that produce Bacillus thuringiensis (Bt) toxins. Because inheritance of resistance to the Bt toxins in transgenic crops is typically recessive, DNA-based screening for resistance alleles in heterozygotes is potentially much more efficient than detection of resistant homozygotes with bioassays. Such screening, however, requires knowledge of the resistance alleles in field populations of pests that are associated with survival on Bt crops. Here we report that field populations of pink bollworm ( Pectinophora gossypiella ), a major cotton pest, harbored three mutant alleles of a cadherin-encoding gene linked with resistance to Bt toxin Cry1Ac and survival on transgenic Bt cotton. Each of the three resistance alleles has a deletion expected to eliminate at least eight amino acids upstream of the putative toxin-binding region of the cadherin protein. Larvae with two resistance alleles in any combination were resistant, whereas those with one or none were susceptible to Cry1Ac. Together with previous evidence, the results reported here identify the cadherin gene as a leading target for DNA-based screening of resistance to Bt crops in lepidopteran pests.