Sequential evolution of resistance by western corn rootworm to multiple Bacillus thuringiensis traits in transgenic maize

Transgenic crops that produce insecticidal toxins derived from the bacterium Bacillus thuringiensis (Bt) are grown worldwide to manage insect pests. Western corn rootworm is a serious pest of maize in the United States and is managed with Bt maize. In the United States, the commercial cultivation of a Bt crop requires an accompanying resistance-management strategy to delay the evolution of Bt resistance. One of the primary resistance-management strategies consists of non-Bt refuges along with a Bt crop that produces two Bt toxins (i.e., a pyramid) that kill the same pest species. This approach delays resistance because individuals with resistance to one toxin are killed by the second. However, if a pest species is resistant to one toxin in a pyramid, the effectiveness of a pyramid to delay resistance is compromised, potentially leading to the evolution of resistance to both toxins. Here, we apply a meta-analysis to demonstrate the sequential evolution of resistance by western corn rootworm to Bt maize producing Cry3Bb1 followed by resistance to Gpp34/Tpp35Ab1 maize, with resistance to each Bt toxin increasing in a linear manner over time. Additionally, we show that Bt-resistant western corn rootworm imposed substantial feeding injury, in the field, to maize containing a pyramid of Gpp34/Tpp35Ab1 and Cry3Bb1. To minimize the risk of sequential evolution of resistance to multiple transgenic traits, an emphasis should be placed on developing transgenic pyramids not compromised by prior resistance, and in cases where resistance is already present, larger non-Bt refuges and more diversified pest-management approaches should be applied.