Contemporary evolution of a Lepidopteran species, Heliothis virescens, in response to modern agricultural practices

Abstract

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. K E Y W O R D SBacillus thuringiensis, cotton, Heliothis virescens, selective sweep, tobacco budworm

Genome evolution in an agricultural pest following adoption of transgenic crops

“…We also examined whether any of the 11 previously identified candidate Cry resistance genes showed evidence of strong shifts in allele frequency over time. Surprisingly, none of these genes implicated in Cry-toxin resistance underwent significant temporal changes, nor did genes associated with detoxification of synthetic insecticides or plant defensive compounds, as was observed in another species where Bt crops replaced insecticidal control (Fritz et al 2018). Instead, we found multiple novel candidate genes within regions of greater than expected allele frequency change, and quantified the effect size of the region showing the greatest temporal change on Cry resistance.…”

The role of population and quantitative genetics and modern sequencing technologies to understand evolved herbicide resistance and weed fitness

“…Biologists who study invasive species have started to recognize the importance of paying more attention to the evolutionary characteristics that drive invasiveness 40 . Weed scientists and pest specialists can and should use these tools to better describe resistance evolution as well as pest fitness and pest behavior 6,27,41 . This could generate a more comprehensive and better informed understanding of how pests adapt to human disturbance.…”

Patterns of genetic differentiation in Colorado potato beetle correlate with contemporary, not historic, potato land cover

“…Legacies of the effects of historic landscape structure on genetic differentiation might be especially important in agricultural pest systems, where the configuration and composition of agricultural land cover can change rapidly, and the geographic ranges of many insect pests have only recently expanded to encompass agroecosystems (Kirk, Dorn, & Mazzi, 2013). Changes in the structure of agricultural landscapes have been shown to influence genetic diversity in local populations (Crawford, Peterman, Kuhns, & Eggert, 2016;Dixo, Metzger, Morgante, & Zamudio, 2009;Favre-Bac, Mony, Ernoult, Burel, & Arnaud, 2016) and drive local adaptation to pesticides over short time scales (Crossley, Chen, Groves, & Schoville, 2017;Fritz et al, 2018), but effects on contemporary genetic differentiation among insect populations are limited in taxonomic scope (to bees and grasshoppers; Keller et al, 2013;Jaffé et al, 2016;Suni, 2017) and remain unexamined in insect pest systems. Ignoring the historical landscape context of agricultural pest systems could result in misleading inferences about factors that modulate pest invasions, adaptive evolution, and ultimately give rise to the geographic variation observed in pest traits (Pélissié, Crossley, Cohen, & Schoville, 2018).…”