Ecological context and the influence of interactions on the evolution of resistance
Pesticide use can have impacts far beyond their intended target organism by influencing the ecology and evolution of organisms with which the target species interact. Contributions in this issue explore the ecological context of resistance evolution by assessing how pesticide application may affect interactions between target and non-target organisms, which may influence downstream eco-evolutionary feedback dynamics.
Iriart et al. (2020) set the stage for our understanding of the ecological context of resistance evolution by reviewing the role of herbicides in driving the ecology and evolution of plants and plant-associates (e.g. pollinators, soil microbes, herbivores, and parasitoids) living in communities at the agro-ecological interface. They synthesize what is known about how herbicides can alter plant phenotypes from plastic or genetic changes and how plant-associates may be directly or indirectly (via interactions) affected by herbicides. Building off this knowledge, they demonstrate that herbicides can induce sufficiently rapid change in plants and plant-associates to alter both evolution and ecological dynamics over the same timescales, thus producing eco-evolutionary feedbacks. From these insights, they provide suggestions for future research into herbicide catalyzed eco-evolutionary dynamics, with the goal of deciphering the effects of herbicides on plant and plant-associates’ traits, on species interactions, and on the composition of the broader ecological community.
Herbicide application may alter eco-evolutionary dynamics by selecting for traits that are correlated to resistance, such as earlier flowering time or altered mating patterns (among other changes) thereby potentially modifying mutualistic interactions between plants and their associates. For example, glyphosate resistant populations of the common morning glory (Ipomoea purpurea ) exhibit higher selfing rates compared to susceptible populations (Kuester et al 2017), perhaps due to reproductive assurance associated with being both highly selfing and herbicide resistant. However, an association between the mating system and resistance would not be expected to be maintained over time if the resistant, selfing types exhibited inbreeding depression. In this issue, Van Etten et al. (2021) combined growth chamber and field studies with transcriptome surveys to ask whether genetic lines of Ipomoea purpurea selected for increased glyphosate resistance exhibited signs of inbreeding depression (i.e. poorer performance of inbred versus outcross progeny) compared to both non-selected control lines and lines selected for increased susceptibility. Interestingly, they found that while plants from non-selected control lines and susceptible lines exhibited evidence of inbreeding depression, plants from resistant lines provided no evidence for inbreeding depression in most characters. Rather, in the presence of herbicide, resistant lines tended to showoutbreeding depression : seeds from resistant lines that were produced via selfing germinated more and grew to be larger plants than those from resistant lines that were produced from outcrossing. Additionally, the authors showed that the expression of genes within the transcriptome mirrored the phenotypic patterns—resistant, inbred plants showed higher expression of genes involved in translation and DNA replication compared to resistant, outcrossed progeny in the presence of glyphosate. Thus, in this case study, continued resistance evolution would support higher self-fertilization and decreased outcrossing. In this way, the maintenance of plant-pollinator interactions could be negatively altered over time in herbicide-exposed populations ofI. purpurea .
As with herbicides, the evolution of resistance to insecticides has the potential to alter ecological interactions in crop ecosystems, as shown by Paddock et al. (2021). Their study investigated whether the microbial communities differed between herbivorous western corn rootworms (a widespread agricultural pest) that were susceptible or had evolved resistance to the insecticide Bacillus thuringiensis (Bt) produced by genetically-modified maize. Their results supported different enteric microbiomes between resistant and susceptible western corn rootworm in that resistant individuals had less rich and diverse bacterial communities. Additionally, western corn rootworm digesting the insecticide caused a severe shift towards more simplified bacterial communities in susceptible WCR, but not resistant western corn rootworm, suggesting an effect of host-microbial interactions in the evolution of resistance to Bt. Together, these results contribute to our budding understanding of the role that ecology can play in resistance evolution to modern stressors, further perpetuating eco-evolutionary feedbacks and dynamics in natural communities.