Abstract
Widespread use of insecticides has led to insecticide resistance in many populations of insects. In some populations, resistance has evolved to multiple pesticides. In Drosophila melanogaster, resistance to multiple classes of insecticide is due to the overexpression of a single cytochrome P450 gene, Cyp6g1. Overexpression of Cyp6g1 appears to have evolved in parallel in Drosophila simulans, a sibling species of D. melanogaster, where it is also associated with insecticide resistance. However, it is not known whether the ability of the CYP6G1 enzyme to provide resistance to multiple insecticides evolved recently in D. melanogaster or if this function is present in all Drosophila species. Here we show that duplication of the Cyp6g1 gene occurred at least four times during the evolution of different Drosophila species, and the ability of CYP6G1 to confer resistance to multiple insecticides exists in D. melanogaster and D. simulans but not in Drosophila willistoni or Drosophila virilis. In D. virilis, which has multiple copies of Cyp6g1, one copy confers resistance to DDT and another to nitenpyram, suggesting that the divergence of protein sequence between copies subsequent to the duplication affected the activity of the enzyme. All orthologs tested conferred resistance to one or more insecticides, suggesting that CYP6G1 had the capacity to provide resistance to anthropogenic chemicals before they existed. Finally, we show that expression of Cyp6g1 in the Malpighian tubules, which contributes to DDT resistance in D. melanogaster, is specific to the D. melanogaster–D. simulans lineage. Our results suggest that a combination of gene duplication, regulatory changes and protein coding changes has taken place at the Cyp6g1 locus during evolution and this locus may play a role in providing resistance to different environmental toxins in different Drosophila species.
Highlights
Different mechanisms have evolved that allow organisms to avoid or detoxify harmful chemicals found in their environment or food source
Overexpression of Cyp6p3 in field-caught Anopheles gambiae is associated with resistance to the insecticide permethrin [6], and gain of Cyp6bq9 expression in the brain of Tribolium castaneum is responsible for deltamethrin resistance [7], while in the aphid Myzus persicae, an increase in copy number of the Cyp6cy3 gene is associated with resistance to neonicotinoid insecticides [8]
As the number of P450s varies between genomes [17,18], and the copy number of Cyp6g1 is polymorphic in D. melanogaster [12], the presence or absence and copy number of Cyp6g1 in 12 Drosophila species with complete reference genomes was investigated [19]
Summary
Different mechanisms have evolved that allow organisms to avoid or detoxify harmful chemicals found in their environment or food source. Many examples of insecticide resistance that are caused by or associated with increased transcriptional output of P450s have been documented. Overexpression of Cyp6p3 in field-caught Anopheles gambiae is associated with resistance to the insecticide permethrin [6], and gain of Cyp6bq expression in the brain of Tribolium castaneum is responsible for deltamethrin resistance [7], while in the aphid Myzus persicae, an increase in copy number of the Cyp6cy gene is associated with resistance to neonicotinoid insecticides [8]. The insertion of the long terminal repeat (LTR) of an Accord transposable element into the 59 region of Cyp6g1 is responsible for overexpression in the resistant strains, and the overexpression is specific to tissues associated with the metabolism of xenobiotics—the midgut, fat body and Malpighian tubules [11]
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