Context dependence shapes the evolution of glyphosate and herbivory resistance in Ipomoea purpurea
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Abstract
Plant defense evolution has often been examined under single-stressor scenarios, overlooking the complex, interacting stressors of natural environments. Recent research incorporating multiple stressors has largely emphasized physiological and molecular responses rather than evolutionary dynamics, leaving such dynamics less explored. To address this gap, we examined the potential for fitness costs and benefits to the herbicide glyphosate and insect herbivory in Ipomoea purpurea (common morning glory). Through a factorial field experiment, we manipulated glyphosate and the insecticide spinosad to estimate selection on glyphosate and herbivory resistance. We found that glyphosate resistance was under positive selection with no detectable fitness costs, whereas herbivory resistance showed neither costs nor benefits. Notably, positive correlational selection favored higher glyphosate and herbivory resistance in the combined-stressor environment, suggesting these traits may be genetically linked. Further, the strength of positive selection on glyphosate resistance depended on the environmental context of herbivory. Together, these results indicate that selection for glyphosate resistance predominantly drives evolution in this system and may promote increased herbivory resistance. By applying a fitness cost-benefit framework to multiple interacting stressors, our study underscores the context-dependent nature of selection on plant defense traits and highlights how combined stressors can shape their evolutionary trajectories.
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We also identified a fitness peak for high levels of both glyphosate and herbivory resistance (i.e., correlational selection: γ = 0.06, F1 = 5.10, p = 0.030; Figure 4; Table S6),
It is exciting to see a non-linear relationship (epistasis) between these two environmental stressors. To help with interpreting this figure, I suggest that the figure 4 legend include the analysis being done a bit further: explaining what it means for a number to be more or less negative, naming the type of analysis in the first sentence, as done for figure 5, and explaining the meaning of the axis values.
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There was evidence for potential positive selection for glyphosate resistance
I noticed that for some scatter plots there is a clear correlation shown with a solid line (a), and for others there is no clear correlation and no linear regression shown in the figure (all herbivory resistance scatters, as well as (b). I think it would make sense to follow suit with (c) and (d) and not show dashed 'potential' selection when the p-values do not support a correlation, and the scatter plots don't have a visible correlation.
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Figure 2.
Do shriveled and yellow leaves get counted when randomly sampling leaves for herbivory damage? I'm assuming these leaves are not counted, and this is what is meant by in the methods 'excluded ambiguous damage'.
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We found that spinosad application significantly reduced herbivory (untreated: 0.53%, treated: 0.15%; F1 = 174.06, p < 0.001; Figure 2a, Table S1).
I am struggling with the Y-axis '% herbivory per leaf'. Firstly, I am confused about the range. It seems to go from around -2% to 3% damage. However, in the methods, damage values are explained as being the percentage of the leaf surface damaged by herbivory, averaged across four leaves). How can there be negative herbivory damage? Also, perhaps the Y axis title should be something like '% leaf area damaged'
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In line with our previous work, we elected to be conservative with our herbivory damage estimates and excluded ambiguous damage that could be attributed to glyphosate from our estimates (Zhang & Baucom, 2024).
I'm curious what leaf damage due to glyphosate versus leaf damage do to herbivores looks like. It would be nice to see what each of these looks like in a figure, maybe as a supplement. For both, leaf damage is used as an important measure of the effects of stressors on the health/fitness of the plant. This section would benefit from a citation to point to the previous work referenced here that shows this software can exclude one damage from the other.
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