Polygenic response to selection by transgenic Bt-expressing crops in wild Helicoverpa zea and characterization of a major effect locus

Strong and shifting selective pressures of the Anthropocene are rapidly shaping phenomes and genomes of organisms worldwide. Crops expressing pesticidal proteins from Bacillus thuringiensis (Bt) represent one major selective force on insect genomes. 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 amplification event, 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. Multiple genes were annotated in this genomic region, and all appeared to be significantly upregulated in Bt resistant H. zea. We functionally characterized genes within the copy number variant (CNV), providing insight into their potential roles in resistance evolution. Our findings reveal the nature of rapid genome evolution in a major crop pest following anthropogenic selection and highlight the role that CNVs can have in rapid evolutionary responses.