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Genome evolution in an agricultural pest following adoption of transgenic crops
Friday, 2022/01/07 | 06:29:33

Katherine L. Taylor, Kelly A. Hamby, Alexandra M. DeYonke, Fred Gould, and Megan L. Fritz

PNAS December 28, 2021 118 (52) e2020853118


Evolution of resistance to management approaches in agricultural landscapes is common and results in economic losses. Early detection of pest resistance prior to significant crop damage would benefit the agricultural community. It has been hypothesized that new genomic approaches could track molecular signals of emerging resistance and trigger efforts to preempt widespread damage. We tested this hypothesis by quantifying genomic changes in the pest Helicoverpa zea over a 15-y period concurrent with commercialization of transgenic Bacillus thuringiensis–expressing crops and their subsequent loss of efficacy. Our results demonstrate the complex nature of evolution in agricultural ecosystems and provide insight into the potential and pitfalls of using genomic approaches for resistance monitoring.


Replacing synthetic insecticides with transgenic crops for pest management has been economically and environmentally beneficial, but these benefits erode as pests evolve resistance. It has been proposed that novel genomic approaches could track molecular signals of emerging resistance to aid in resistance management. To test this, we quantified patterns of genomic change in Helicoverpa zea, a major lepidopteran pest and target of transgenic Bacillus thuringiensis (Bt) crops, between 2002 and 2017 as both Bt crop adoption and resistance increased in North America. Genomic scans of wild H. zea were paired with quantitative trait locus (QTL) analyses and showed the genomic architecture of field-evolved Cry1Ab resistance was polygenic, likely arising from standing genetic variation. Resistance to pyramided Cry1A.105 and Cry2Ab2 toxins was controlled by fewer loci. Of the 11 previously described Bt resistance genes, 9 showed no significant change over time or major effects on resistance. We were unable to rule out a contribution of aminopeptidases (apns), as a cluster of apn genes were found within a Cry-associated QTL. Molecular signals of emerging Bt resistance were detectable as early as 2012 in our samples, and we discuss the potential and pitfalls of whole-genome analysis for resistance monitoring based on our findings. This first study of Bt resistance evolution using whole-genome analysis of field-collected specimens demonstrates the need for a more holistic approach to examining rapid adaptation to novel selection pressures in agricultural ecosystems.


See: https://www.pnas.org/content/118/52/e2020853118


Figure 2: Genomic divergence in Cry-associated regions of the H. zea genome. SNP additive effect sizes, β (LMM), of the resistant parent allele are plotted for Cry1Ab (A) and Cry1A.105+Cry2Ab2 (B). All SNPs in significant QTL windows are in color. Genome-wide divergence in field-collected H. zea from Louisiana (2002-2017) are in C. Alternating light and dark gray points represent pairwise FST values for 10-kb windows with a 1-kb step. Points above the red line underwent significant temporal genomic divergence. Points in color were also associated with increased growth on Cry1Ab (red), Cry1A.105+Cry2Ab2 (blue), or both (purple) in our QTL analysis.

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