Significance: 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 pestHelicoverpa zeaover a 15-y period concurrent with commercialization of transgenicBacillus 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.

Background: Within theCulex pipiensmosquito complex, there are six contemporarily recognized taxa:Cx.quinquefasciatus,Cx.pipiensf.pipiens,Cx.pipiensf.molestus,Cx.pipiens pallens,Cx.australicusandCx.globocoxitus. Many phylogenetic aspects within this complex have eluded resolution, such as the relationship of the two Australian endemic taxa to the other four members, as well as the evolutionary origins and taxonomic status ofCx.pipiens pallensandCx.pipiensf.molestus. Ultimately, insights into lineage relationships within the complex will facilitate a better understanding of differential disease transmission by these mosquitoes. To this end, we have combined publicly available data with our own sequencing efforts to examine these questions.Results: We found that the two Australian endemic complex members,Cx.australicusandCx.globocoxitus, comprise a monophyletic group, are genetically distinct, and are most closely related to the cosmopolitanCx.quinquefasciatus. Our results also show thatCx.pipiens pallensis genetically distinct, but may have arisen from past hybridization. Lastly, we observed complicated patterns of genetic differentiation within and betweenCx.pipiensf.pipiensandCx.pipiensf.molestus.Conclusions: Two Australian endemicCulextaxa,Cx.australicusandCx.globocoxitus, belong within theCx. pipienscomplex, but have a relatively older evolutionary origin. They likely diverged fromCx.quinquefasciatusafter its colonization of Australia. The taxonCx.pipiens pallensis a distinct evolutionary entity that likely arose from past hybridization betweenCx.quinquefasciatusandCx.pipiensf.pipiens/Cx. pipiensf.molestus. Our results do not suggest it derives from ongoing hybridization. Finally, genetic differentiation within theCx.pipiensf.pipiensandCx.pipiensf.molestussamples suggests that they collectively form two separate geographic clades, one in North America and one in Europe and the Mediterranean. This may indicate that theCx.pipiensf.molestusform has two distinct origins, arising fromCx.pipiensf.pipiensin each region. However, ongoing genetic exchange within and between these taxa have obscured their evolutionary histories, and could also explain the absence of monophyly among our samples. Overall, this work suggests many avenues that warrant further investigation.

Daily blood feeding rhythms of laboratory-reared North American Culex pipiens

Adaptation to human‐induced environmental change has the potential to profoundly influence the genomic architecture of affected species. This is particularly true in agricultural ecosystems, where anthropogenic selection pressure is strong. Heliothis virescens primarily feeds on cotton in its larval stages, and US populations have been declining since the widespread planting of transgenic cotton, which endogenously expresses proteins derived from Bacillus thuringiensis (Bt). No physiological adaptation to Bt toxin has been found in the field, so adaptation in this altered environment could involve (i) shifts in host plant selection mechanisms to avoid cotton, (ii) changes in detoxification mechanisms required for cotton‐feeding vs. feeding on other hosts or (iii) loss of resistance to previously used management practices including insecticides. Here, we begin to address whether such changes occurred in H. virescens populations between 1997 and 2012, as Bt‐cotton cultivation spread through the agricultural landscape. For our study, we produced an H. virescens genome assembly and used this in concert with a ddRAD‐seq‐enabled genome scan to identify loci with significant allele frequency changes over the 15‐year period. Genetic changes at a previously described H. virescens insecticide target of selection were detectable in our genome scan and increased our confidence in this methodology. Additional loci were also detected as being under selection, and we quantified the selection strength required to elicit observed allele frequency changes at each locus. Potential contributions of genes near loci under selection to adaptive phenotypes in the H. virescens cotton system are discussed.

The evolution of pest resistance to management tools reduces productivity and results in economic losses in agricultural systems. To slow its emergence and spread, monitoring and prevention practices are implemented in resistance management programs. Recent work suggests that genomic approaches can identify signs of emerging resistance to aid in resistance management. Here, we empirically examined the sensitivity of genomic monitoring for resistance management in transgenic Bt crops, a globally important agricultural innovation. Whole genome resequencing of wild North American Helicoverpa zea collected from non-expressing refuge and plants expressing Cry1Ab confirmed that resistance-associated signatures of selection were detectable after a single generation of exposure. Upon demonstrating its sensitivity, we applied genomic monitoring to wild H. zea that survived Vip3A exposure resulting from cross-pollination of refuge plants in seed-blended plots. Refuge seed interplanted with transgenic seed exposed H. zea to sublethal doses of Vip3A protein in corn ears and was associated with allele frequency divergence across the genome. Some of the greatest allele frequency divergence occurred in genomic regions adjacent to a previously described candidate gene for Vip3A resistance. Our work highlights the power of genomic monitoring to sensitively detect heritable changes associated with field exposure to Bt toxins and suggests that seed-blended refuge will likely hasten the evolution of resistance to Vip3A in lepidopteran pests.