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.