Microbial responses to stress cryptically alter natural selection on plants.

Microbial communities can rapidly respond to stress, meaning plants may encounter altered soil microbial communities in stressful environments. These altered microbial communities may then affect natural selection on plants. Because stress can cause lasting changes to microbial communities, microbes may also cause legacy effects on plant selection that persist even after the stress ceases. To explore how microbial responses to stress and persistent microbial legacy effects of stress affect natural selection, we grew Chamaecrista fasciculata plants in stressful (salt, herbicide, or herbivory) or nonstressful conditions with microbes that had experienced each of these environments in the previous generation. Microbial community responses to stress generally counteracted the effects of stress itself on plant selection, thereby weakening the strength of stress as a selective agent. Microbial legacy effects of stress altered plant selection in nonstressful environments, suggesting that stress-induced changes to microbes may continue to affect selection after stress is lifted. These results suggest that soil microbes may play a cryptic role in plant adaptation to stress, potentially reducing the strength of stress as a selective agent and altering the evolutionary trajectory of plant populations.

Traits of soil bacteria predict plant responses to soil moisture.

Microorganisms can help plants and animals contend with abiotic stressors, but why they provide such benefits remains unclear. Here we investigated byproduct benefits, which occur when traits that increase the fitness of one species provide incidental benefits to another species with no direct cost to the provider. In a greenhouse experiment, microbial traits predicted plant responses to soil moisture such that bacteria with self-beneficial traits in drought increased plant early growth, size at reproduction, and chlorophyll concentration under drought, while bacteria with self-beneficial traits in well-watered environments increased these same plant traits in well-watered soils. Thus, microbial traits that promote microbial success in different moisture environments also promote plant success in these same environments. Our results demonstrate that byproduct benefits, a concept developed to explain the evolution of cooperation in pairwise mutualisms, can also extend to interactions between plants and nonsymbiotic soil microbes.

Linking genetic diversity and species diversity through plant-soil feedback.

Genetic diversity and species diversity are typically studied in isolation despite theory showing they likely influence one another. Here, we used simplified communities of one or two populations of one or two species to test whether linkages between genetic and species diversity can be mediated by interactions between plants and their soil microbiota, or microbe-mediated plant-soil feedback (PSF). Interspecific PSF promotes the maintenance of species diversity when plants grow better with heterospecific soil microbes than with conspecific microbes. Similarly, intraspecific PSF promotes the maintenance of genetic diversity when plants grow better with heterogenotypic than with congenotypic microbes. In a two-phase greenhouse experiment, we conditioned the soil microbial community with pairs of plants that were either two individuals of the same species (lower species diversity) or one individual of each of two species (higher species diversity), and with pairs of plants that were either two individuals from the same population (lower genetic diversity) or one individual from each of two populations (higher genetic diversity). We then tested the effects of these microbial communities on plant growth in a second phase. We found that higher genetic diversity reduced the ability of interspecific PSF to promote plant species diversity, and for one of our two study species, higher species diversity reduced the ability of intraspecific PSF to promote plant genetic diversity. If these patterns occur in more diverse communities, then our results suggest that PSF may dampen the negative effects of diversity loss by promoting diversity at other levels of biological organization.

Mycorrhizal interactions do not influence plant-herbivore interactions in populations of Clarkia xantiana ssp. xantiana spanning from center to margin of the geographic range.

Multispecies interactions can be important to the expression of phenotypes and in determining patterns of individual fitness in nature. Many plants engage in symbiosis with arbuscular mycorrhizal fungi (AMF), but the extent to which AMF modulate other species interactions remains poorly understood. We examined multispecies interactions among plants, AMF, and insect herbivores under drought stress using a greenhouse experiment and herbivore choice assays. The experiment included six populations of Clarkia xantiana (Onagraceae), which span a complex environmental gradient in the Southern Sierra Nevada of California. Clarkia xantiana's developing fruits are commonly attacked by grasshoppers at the end of the growing season, and the frequency of attack is more common in populations from the range center than range margin. We found that AMF negatively influenced all metrics of plant growth and reproduction across all populations, presumably because plants supplied carbon to AMF but did not benefit substantially from resources potentially supplied by the AMF. The fruits of plants infected with AMF did not differ from those without AMF in their resistance to grasshoppers. There was significant variation among populations in damage from herbivores but did not reflect the center-to-margin pattern of herbivory observed in the field. In sum, our results do not support the view that AMF interactions modulate plant-herbivore interactions in this system.