The interplay of ecology and evolution in aboveground-belowground responses to environmental change
Global changes influence the ecological outcomes of plant-microbe interactions. Because species interactions can be strong agents of natural selection, evolutionary changes are also likely and can spark eco-evolutionary feedbacks which occur when a rapid evolutionary change feedbacks to influence ecological processes. Here we illustrate the potential for eco-evolutionary feedbacks mediated by plant-soil microbe interactions using two very different, but complementary approaches: an experimental evolution approach in greenhouse mesocosms and a landscape-scale correlational analyses. In our first case study, we describe our previous research showing: 1) drought stress changes soil microbial communities in ways that influence plant fitness responses to drought and 2) plant evolutionary responses to multi-generation drought treatments feedback to influence soil microbial communities. We then present results from new analyses testing how soil microbial community responses to drought feedback to influence natural selection on plant traits. In our second case study, we describe a combined field and common garden approach to test whether the requirements of an eco-evolutionary feedback can be detected at large spatial scales. Examining intraspecific variation in plant-soil linkages across a foundation tree species’ range provided a strong test for the reciprocal effects of soil selective agents and niche construction of belowground environments by plants.
Two strengths of the experimental evolution approach are that selection can be definitively attributed to the manipulated environmental factor (simulated drought) and the evolutionary histories of both plants and associated belowground communities can be manipulated independently. We find that drought stress has caused shifts in soil microbial communities that not only protect plants from the negative fitness effects of drought stress but also alter patterns of natural selection on plant traits. In short, the changes to microbial communities resulting from both the direct effects of soil moisture and evolutionary shifts in plant traits feedback to influence evolutionary processes aboveground. A major strength of correlational landscape scale studies is ecological realism—testing for the signature of eco-evolutionary dynamics using natural plant populations and their associated microbial communities across broad environmental gradients at realistic spatial scales relevant to global change. We find that variation in soil N pools (related to belowground microbial communities) predicts genetic divergence among P. angustifolia populations, and that this evolutionary response affects a niche-constructing trait that modifies soil N and microbial diversity. Together, these results suggest that eco-evolutionary feedbacks mediated through plant-soil linkages may be a common phenomenon with important implications as global changes disrupt widespread plant-soil linkages.