Polygenic basis of Bt Cry resistance evolution in wild Helicoverpa zea

Strong and shifting selective pressures of the anthropocene are rapidly shaping phenomes and genomes of organisms worldwide. One major selective force on insect genomes is crops expressing pesticidal proteins from Bacillus thuringiensis (Bt). Here we characterize a rapid response to selection by Bt crops in a major crop pest, Helicoverpa zea. We reveal the polygenic architecture of Bt resistance evolution in H. zea and identify multiple genomic regions underlying this trait. In the genomic region of largest effect, we identified a gene cluster amplification, where resistant individuals showed variation in copy number for multiple genes. Signals of this amplification increased over time, consistent with the history of field-evolved Bt resistance evolution. Modern wild populations from disparate geographical regions are positive for this variant at high, but not fixed, allele frequencies. We also detected selection against single copy variants at this locus in wild H. zea collected from Bt expressing plants, further supporting its role in resistance. Seven trypsin genes were present in this genomic region and all appeared to be significantly upregulated in Bt resistant H. zea. Biochemically inhibiting trypsin activity decreased H. zeas tolerance to Bt. These findings characterize rapid genome evolution in a major crop pest following anthropogenic selection and highlight the role that gene copy number variants can have in rapid evolutionary responses.