For some polyphagous insects, adaptation to phytochemically novel plants can enhance resistance to certain pesticides, but whether pesticide resistance expands tolerance to phytochemicals has not been examined. Amyelois transitella Walker (navel orangeworm) is an important polyphagous pest of nut and fruit tree crops in California. Bifenthrin resistance, partially attributable to enhanced cytochrome P450 (P450)-mediated detoxification, has been reported in an almond-infesting population exposed to intense pesticide selection. We compared the toxicity of bifenthrin and three phytochemicals–chlorogenic acid, and the furanocoumarins xanthotoxin and bergapten–to three strains of A. transitella: pyrethroid-resistant R347 (maintained in the laboratory for ∼10 generations), fig-derived FIG (in the laboratory for ∼25 generations), and CPQ–a laboratory strain derived from almonds ∼40 years ago). Whereas both Ficus carica (fig) and Prunus dulcis (almond) contain chlorogenic acid, furanocoumarins occur only in figs. Both R347 and FIG exhibited 2-fold greater resistance to the three phytochemicals compared with CPQ; surprisingly, bifenthrin resistance was highest in FIG. Piperonyl butoxide, a P450 synergist, increased toxicity of all three phytochemicals only in CPQ, implicating alternate tolerance mechanisms in R347 and FIG. To test the ability of the strains to utilize novel hostplants directly, we compared survival on diets containing seeds of Wisteria sinensis and Prosopis pallida, two non-host Fabaceae species; survival of FIG was highest and survival of R347 was lowest. Our results suggest that, while P450-mediated pesticide resistance enhances tolerance of certain phytochemicals in this species, it is only one of multiple biochemical adaptations associated with acquiring novel hostplants.
Among the most familiar forms of human-driven evolution on ecological time scales is the rapid acquisition of resistance to pesticides by insects. Since the widespread adoption of synthetic organic insecticides in the mid-twentieth century, over 500 arthropod species have evolved resistance to at least one insecticide. Efforts to determine the genetic bases of insecticide resistance have historically focused on individual loci, but the availability of genomic tools has facilitated the screening of genome-wide characteristics. We re-sequenced three contemporary populations of the navel orangeworm (Amyelois transitella), the principal pest of almond orchards in California, differing in bifenthrin resistance status to examine insecticide-induced changes in the population genomic landscape of this species. We detected an exceptionally large region with virtually no polymorphisms, extending to up to 1.3 Mb in the resistant population. This selective sweep includes genes associated with pyrethroid and DDT resistance, including a cytochrome P450 gene cluster and the gene encoding the voltage-gated sodium channel para. Moreover, the sequence along the sweep is nearly identical in the genome assembled from a population founded in 1966, suggesting that the foundation for insecticide resistance may date back a half-century, when California’s Central Valley experienced massive area-wide applications of DDT for pest control.
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