Genome evolution in an agricultural pest following adoption of transgenic crops
AbstractReplacement of synthetic insecticides with transgenic crops for pest management has been both economically and environmentally beneficial. These benefits have often eroded as pests evolved resistance to the transgenic crops, but a broad understanding of the timing and complexity of the adaptive changes which lead to field-evolved resistance in pest species is lacking. Wild populations of Helicoverpa zea, a major lepidopteran crop pest and the target of transgenic Cry toxin-expressing cotton and corn, have recently evolved widespread, damaging levels of resistance. Here, we quantified patterns of genomic change in wild H. zea collected between 2002 and 2017 when adoption rates of Cry-expressing crops expanded in North America. Using a combination of genomic and genotypic approaches, we identified significant temporal changes in allele frequency throughout the genomes of field-collected H. zea. Many of these changes occurred concurrently with increasingly damaging levels of resistance to Cry toxins between 2012 and 2016, in a pattern consistent with polygenic selection. Surprisingly, none of the eleven previously described Cry resistance genes showed signatures of selection in wild H. zea. Furthermore, we observed evidence of a very strong selective sweep in one region of the H. zea genome, yet this strongest change was not additively associated with Cry resistance. This first, whole genome analysis of field-collected specimens to study evolution of Cry resistance demonstrates the potential and need for a more holistic approach to examining pest adaptation to changing agricultural practices.