Microbe-mediated adaptive plasticity
Phenotypic plasticity is when the environment affects the expression of an organism’s traits (Richards et al. 2006), and adaptive plasticity occurs when these environmentally-induced changes in phenotype increase fitness in that environment (Dudley & Schmitt 1996). Microbe-mediated adaptive plasticity is when local plant phenotypes have higher fitness than foreign phenotypes as a result of interactions with locally important microbes and could occur in two ways. First, plants might have higher fitness because they demonstrate plasticity in traits that attract, retain, and regulate important microbes (microbe facing traits), and associating with these important microbes subsequently affects plant functional traits (environment facing traits) in ways that enhance fitness. The commonly observed autoregulation response of legumes (Wang et al. 2018) may exemplify this process; in low nitrogen environments plants form many rhizobium-housing nodules and are rewarded with fixed nitrogen, while in high nitrogen environments where biologically-fixed nitrogen is less useful, plants plastically reduce nodulation, therefore reducing the costs of supporting bacterial symbionts. Plastic shifts in investment in key microbes likely maintain fitness across a range of nutrient conditions.
Second, local environmental conditions can affect the abundance and composition of microbial communities, and this variation in microbial communities can induce plastic changes in plant phenotypes. A number of studies have now demonstrated that foliar and root endophytes, diverse soil microbial communities, and individual bacterial or fungal taxa affect expression of plant functional traits (e.g., Wagner et al.2014; Giauque et al. 2019). For example, Giauque and Hawkes (2019) measured trait plasticity in Panicum virgatum exposed to low or high water conditions (3% or 15% gravimetric soil moisture), and inoculated with one of 35 different fungal isolates. Plasticity was calculated for six traits (whole plant water loss, relative growth rate, tiller number, and number of wilt free days, and root biomass). Average plasticity (mean plasticity of all six traits) was almost double in plants infected with endophytes compared to uninfected plants, presumably because endophytes influence the expression of plant traits that influence subsequent physiological and growth responses to soil moisture. Authors also demonstrated that endophytes isolated from hotter drier environments increase plant survival under dry conditions, likely because endophyte communities from different environments differ in their effects on the expression of plant traits associated with drought tolerance. However, the relationship between traits and fitness was not empirically tested.
Work by Lau and Lennon (2012) also is consistent with microbe-mediated adaptive plasticity. They manipulated soil moisture for replicated plant populations and their associated microbial communities over the course of multiple plant generations. There was minimal plant evolutionary response to soil moisture across multiple generations, but microbial communities that had experienced ~16 months of drought buffered plants against contemporary exposure to drought. Plants experienced a 58% reduction in fitness during drought when grown in association with wet-adapted microbes, but only a 20% reduction in fitness when grown in association with drought-adapted microbes. Likewise, plants grown with wet-adapted microbes had higher fitness under higher soil moisture conditions. The authors postulate that microbial community effects on flowering phenology, a trait that commonly exhibits plasticity to drought, may underlie the observed fitness effects (Lau & Lennon 2012), although the link between flowering time and fitness responses to drought also was not explicitly demonstrated.
The two pathways through which microbes can elicit adaptive plasticity are not independent and are likely to feedback to affect the evolution of each pathway. For example, plant plastic responses to abiotic environmental variation can affect the abundance and diversity of microbes attracted to the rhizosphere (Jones et al. 2019), and this variation in microbial community composition can in turn cause plastic shifts in plant traits that increase fitness. Ultimately, the same forces that favor the evolution of adaptive plasticity, like temporal or spatial environmental heterogeneity, are also expected to select for microbe-mediated adaptive plasticity. Additionally, plasticity in microbe-facing traits might be expected to evolve when different microbes promote plant fitness in different environments, and microbe-induced plasticity in environment-facing traits might be expected to evolve when microbes are better predictors of environmental conditions than other environmental cues (Metcalf et al. 2019) or when microbes elicit larger changes in plant phenotypes than genetic changes within the plant itself (Hawkes et al. 2020).
The most convincing studies of adaptive plasticity explicitly link phenotypes (traits) to fitness (Schmitt et al. 2003). In the case of microbe-mediated adaptive plasticity, the traits underlying these adaptive responses are often unknown, hard to measure, and/or cryptic, particularly for microbe-facing traits. Although there is substantial evidence that microbes mediate plant phenotype, few studies explicitly link plasticity with fitness to definitively demonstrate microbe-mediated adaptive plasticity (vs. microbe-mediated plasticity, Goh et al. 2013).