Eco-Evolutionary Dynamics of Plant-Soil Feedbacks Explain the Spread Potential of a Plant Invader Under Climate Warming and Biocontrol Herbivory

Plant-soil feedbacks (PSFs) can contribute to the success of invasive plants. Despite strong evidence that plant genetic traits influence soil microbial communities and vice versa, empirical evidence exploring these feedbacks over evolutionary timescales, especially under climate change, remains limited. We conducted a 5-year field study of the annual invasive plant, Ambrosia artemisiifolia L., to examine how selection under climate warming and biocontrol insect herbivory shapes plant population genetics, soil properties, and microbial communities. After four generations under warming and herbivory, we collected seeds of the F4 plant populations together with their conditioned soil for a common garden PSF experiment to explore how resulting PSFs patterns are influencing the performance and spread potential of Ambrosia under changing environmental conditions. This is especially relevant because our recent predictions point to a northward spread of Ambrosia in Europe and Asia under climate change, outpacing the spread of its insect biocontrol agent. We discovered that warming and herbivory significantly but differentially altered plant genetic composition and its soil microbial communities, with less pronounced effects on soil physicochemical properties. Our results indicate that both herbivory and warming generated negative PSFs. These negative PSFs favored plant growth of the seeds from the persistent soil seed bank growing in the conditioned soil under insect herbivory, and by this maintaining the Ambrosia population genetic diversity. They also enhanced the spread potential of warming-selected plant offspring, especially from warmer (southern) to colder (northern) climates. This can be explained by the observed decrease in soil pathogens occurrence under insect herbivory and by the especially strong genetic changes in plant populations under climate warming. Our findings provide insights into how climate warming and biocontrol management affect eco-evolutionary interactions between invasive plant populations and their soil environments, which are critical for predicting invasion dynamics in the context of global change.