Rapid evolution of pesticide resistance via adaptation and interspecific introgression in a major North American crop pest

Abstract

AbstractInsect crop pests threaten global food security. This threat is amplified through the spread of non-native species and the evolution of pesticide resistance, which can be introduced to a population thoughde novomutation or gene flow. We investigate these processes in an economically important noctuid crop pest,Helicoverpa zea, which has rapidly evolved resistance to several pesticides. Its sister speciesHelicoverpa armigera, first detected as an invasive species in Brazil in 2013, introduced the pyrethroid resistance geneCYP337B3to South AmericanH. zeavia introgression. To understand whether this contributes to pesticide resistance in North America, we sequenced 237H. zeagenomes across 10 sample sites in the US. First, we reportH. armigeraintrogression into the North AmericanH. zeapopulation. Two individuals sampled in Texas in 2019 carryH. armigerahaplotypes in a 4Mbp region containingCYP337B3. Second, we show that the remarkable dispersal ability ofH. zearesults in a panmictic North American population. Third, we detect signatures of selection in non-admixedH. zea, identifying a selective sweep at a second pesticide resistance locus with a similar name:CYP333B3. We estimate that its derived allele conferred a ∼4.9% fitness advantage and show that this estimate explains independently observed rare nonsynonymousCYP333B3mutations approaching fixation over a ∼20-year period. We also detect putative signatures of selection at a kinesin gene associated with Bt resistance. Our results show that pesticide resistance inH. zeaevolved rapidly and recently via two independent mechanisms: interspecific introgression and rapid intraspecific adaptation.