Pest control and resistance management through release of insects carrying a male-selecting transgene

Abstract

BackgroundDevelopment and evaluation of new insect pest management tools is critical for overcoming over-reliance upon, and growing resistance to, synthetic, biological and plant-expressed insecticides. For transgenic crops expressing insecticidal proteins from the bacterium Bacillus thuringiensis (‘Bt crops’) emergence of resistance is slowed by maintaining a proportion of the crop as non-Bt varieties, which produce pest insects unselected for resistance. While this strategy has been largely successful, multiple cases of Bt resistance have now been reported.One new approach to pest management is the use of genetically engineered insects to suppress populations of their own species. Models suggest that released insects carrying male-selecting (MS) transgenes would be effective agents of direct, species-specific pest management by preventing survival of female progeny, and simultaneously provide an alternative insecticide resistance management strategy by introgression of susceptibility alleles into target populations. We developed a MS strain of the diamondback moth, Plutella xylostella, a serious global pest of crucifers. MS-strain larvae are reared as normal with dietary tetracycline, but, when reared without tetracycline or on host plants, only males will survive to adulthood. We used this strain in glasshouse-cages to study the effect of MS male P. xylostella releases on target pest population size and spread of Bt resistance in these populations.ResultsIntroductions of MS-engineered P. xylostella males into wild-type populations led to rapid pest population decline, and then elimination. In separate experiments on broccoli plants, relatively low-level releases of MS males in combination with broccoli expressing Cry1Ac (Bt broccoli) suppressed population growth and delayed the spread of Bt resistance. Higher rates of MS male releases in the absence of Bt broccoli were also able to suppress P. xylostella populations, whereas either low-level MS male releases or Bt broccoli alone did not.ConclusionsThese results support theoretical modeling, indicating that MS-engineered insects can provide a powerful pest population suppressing effect, and could effectively augment current Bt resistance management strategies. We conclude that, subject to field confirmation, MS insects offer an effective and versatile control option against P. xylostella and potentially other pests, and may reduce reliance on and protect insecticide-based approaches, including Bt crops.

Type of fitness cost influences the rate of evolution of resistance to transgenic Bt crops

“…2010; Harvey‐Samuel et al . 2015), may be beneficial in prolonging susceptibility, suppressing pests and protecting yields (Alphey, Bonsall & Alphey 2009), potentially making smaller refuges optimal. Furthermore, we have assumed transgenic crops express a single toxin but pyramided crops expressing multiple toxins are now available (Tabashnik, Brévault & Carrière 2013) and may present an additional barrier to resistance by necessitating the occurrence of two distinct mutations.…”

Genetics‐based methods for agricultural insect pest management

“…Various insect species, crop pests and human disease vectors are undergoing trials ranging from laboratory experiments to large‐scale open releases (Gong et al ., 2005; Ant et al ., 2012; Harris et al ., 2012; Harvey‐Samuel et al ., 2015). Insects have been engineered with a self‐limiting construct conferring a dominant lethal phenotype.…”

“…Building on this theoretical work, genetic strains of diamondback moth with the female‐lethal trait have been developed (Jin et al ., 2013) and tested for fitness costs with population‐level effects (Harvey‐Samuel et al ., 2014). Proof of principle of population suppression combined with resistance dilution has now been demonstrated in field‐cage experiments with experimental Bt broccoli (Harvey‐Samuel et al ., 2015) and work is progressing towards open field trials to evaluate performance in an agricultural habitat (Cornell University, 2016; Oxitec Ltd, 2016). …”

Sustainable Agriculture and Climate Change

“…Similarly, genetic engineering, through the release of insects carrying a male-selecting transgene, has equally managed to suppress DBM populations through the prevention of female progeny survival [106]. The same technique has been used successfully to control the fruit flies, B. oleae [107] and Ceratitis capitata (Wiedemann) [108], and the mosquito, Aedes aegypti (L.) [109].…”