Abstract
Transgenic crops expressing Bacillus thuringiensis (Bt) toxins have been widely and successfully deployed for the control of target pests, while allowing a substantial reduction in insecticide use. The evolution of resistance (a heritable decrease in susceptibility to Bt toxins) can pose a threat to sustained control of target pests, but a high‐dose refuge (HDR) management strategy has been key to delaying countervailing evolution of Bt resistance. The HDR strategy relies on the mating frequency between susceptible and resistant individuals, so either partial dominance of resistant alleles or nonrandom mating in the pest population itself could elevate the pace of resistance evolution. Using classic Wright‐Fisher genetic models, we investigated the impact of deviations from standard refuge model assumptions on resistance evolution in the pest populations. We show that when Bt selection is strong, even deviations from random mating and/or strictly recessive resistance that are below the threshold of detection can yield dramatic increases in the pace of resistance evolution. Resistance evolution is hastened whenever the order of magnitude of model violations exceeds the initial frequency of resistant alleles. We also show that the existence of a fitness cost for resistant individuals on the refuge crop cannot easily overcome the effect of violated HDR assumptions. We propose a parametrically explicit framework that enables both comparison of various field situations and model inference. Using this model, we propose novel empiric estimators of the pace of resistance evolution (and time to loss of control), whose simple calculation relies on the observed change in resistance allele frequency.
Highlights
Modified crops, expressing insecticidal toxins of Bacillus thuringiensis (Bt), were first introduced in 1995, and have been adopted worldwide; by 2010, they had been planted on ~ 66 Mha of agricultural crop land (James 2011)
While Bt-expressing crops have met with considerable success, resistance can arise whenever a pest population develops a genetically-based decrease in susceptibility to the toxin (Tabashnik et al 2009), which may lead in turn to drastic loss of Bt crop efficacy under field conditions
This study is aimed at: (i) testing the robustness of the model when F and/or h might be slightly higher than 0; (ii) assessing the extent to which non-recessiveness and non-random mating may balance the effects of fitness cost (USS – URR > 0 and g > 0) and incomplete resistance (USS – VRR > 0); (iii) evaluating whether violations of model assumptions impact the expected time elapsed before buildup of resistance in the pest threatens the efficacy of the Bt-crop itself
Summary
Modified crops, expressing insecticidal toxins of Bacillus thuringiensis (Bt), were first introduced in 1995, and have been adopted worldwide; by 2010, they had been planted on ~ 66 Mha of agricultural crop land (James 2011). The high-dose / refuge (HDR) strategy, resulting in a lowered selection pressure on susceptible individuals (Carrière et al 2010), has generally been effective (Huang et al 2011), in the USA, where its proper implementation has seldom led to loss of control (Tabashnik et al; 2013). This strategy amounts to planting non-resistant cultivars within or surrounding Bt-crop plantings, allowing the survival of some susceptible individuals in a Btdominated environment. If susceptible alleles (S) in the pest are dominant and rare resistant mutants (R) are completely recessive, rare resistant individuals (RR) emerging from Bt plants will mate preferentially with susceptible individuals (SS) emerging from refuge plants
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