Microbe-mediated local adaptation
Microbe-mediated local adaptation results when natural selection operates on plant traits that attract, retain, and regulate locally important microbes (hereafter ”microbe facing traits”). The outcome is microbe-mediated changes to plant functional traits (hereafter ”environment facing traits”) that lead to higher fitness of local plant genotypes compared with foreign plant genotypes that do not associate as well with local microbes (Box 1). Microbe-mediated local adaptation can occur when plant genotype and microbial genotypes/phenotypesinteract to determine plant fitness in response to environmental conditions, or when plant genotype affects microbial community composition and/or function in ways that determine plant fitness in response to environmental conditions. These possibilities are not easily differentiated and also result in similar plant fitness responses so here we have included these processes together, but in Box 2 we further discuss the complications of identifying microbes driving host fitness effects.
The studies that have provided evidence for microbe-mediated local adaptation generally involve classic, widespread resource mutualisms and adaptation to soil nutrient availability, likely because plant ecologists focusing on these mutualisms are well aware of the importance of such mutualisms to population (Bennett et al. 2017), community (van der Heijden et al. 1998), and ecosystem processes (Vitousek & Walker 1989), and because extensive mutualism theory predicts how nutrient availability should influence the evolution of these associations (West et al. 2002; Akçay & Simms 2011). Given the prevalence of these interactions (80% of plant families are mycorrhizal and a number of others engage in tight symbiotic relationships with N-fixing bacteria like rhizobia), the following examples may represent common phenomena rather than rare exceptions.
In one of the most complete tests of microbe-mediated local adaptation, Johnson and co-authors (2010) used a fully factorial greenhouse experiment manipulating seed source, soil source, microbial source, and the presence/absence of microbes, to show that genotypes ofAndropogon gerardii were coadapted/coevolved with local arbuscular mycorrhizal communities to access the most limiting nutrient at each site. They found accessing limiting nutrients was predicated not only on plant genotype but also on being paired with coevolved/coadapted microbes and growing in home soils. However, this enhanced nutrient uptake only translated to increased fitness and patterns of local adaptation for two out of three plant populations, indicating context dependency in microbe-mediated effects (Johnson et al. 2010).
In another example, microbial symbionts acted as a heritable component of the plant phenotype, a necessary condition for evolution by natural selection (Box 1), and these heritable microbial communities affected plant phenotypes in ways that led to adaptive responses. Ectomycorrhizal fungal (EcM) communities of drought-adapted pinyon pine were nearly entirely determined by plant genotype (drought tolerant vs. drought intolerant), and microbes associated with drought-tolerant trees reduced mortality and enhanced plant growth of drought tolerant plant genotypes by 25% under drought conditions (Gehring et al. 2017). Authors identified an Ascomycete fungus in the genus, Geopora , that was associated predominantly with drought tolerant trees, and whose abundance was correlated with plant drought tolerance even in the drought intolerant tree genotypes. In this case, a combination of greenhouse, field, and molecular data support the case that microbial communities, which are determined by plant genotype, underlie plant adaptation to drought (i.e., microbe-mediated local adaptation).
Despite the examples highlighted above, there are few empirical examples of microbe-mediated local adaptation; however, we suspect that this reflects the fact that microbially-mediated effects are often cryptic. The gold standard in testing for local adaptation is the reciprocal transplant experiment where seeds are transplanted into their natal (home) habitat and also moved to a novel (foreign) habitat. In these designs it is unusual for researchers to manipulate the biotic environment (including mutualists and pathogens; Cheplick 2015) even though adaptation to biotic effects may be important (Benning & Moeller 2019). In a review of the literature, we found that the potential for microbe-mediated local adaptation is very high; in 94% of studies where local adaptation was detected authors transplanted plants into soil in the presence of natural microbial communities and measured traits that could be microbially-mediated (Petipas 2018). In contrast, although sample size is small (6 studies), half of studies that failed to detect local adaptation transplanted plants in the absence of natural microbial communities (e.g. autoclaved soils). These results suggest that microbe-mediated local adaptation may be common, but the vast majority of classic plant local adaptation studies cannot differentiate between microbe-mediated effects and non-microbe-mediated effects. For example, Roy Turkington’s classic work suggested patterns of local adaptation were the result of fine-scale interactions between plant competitors (Turkington & Harper 1979; Aarssen & Turkington 1985). Authors demonstrated that clover, Trifolium repens , was adapted to neighboring pasture plants (Turkington and Harper 1979), and this effect was primarily driven by the presence of a grass neighbor, Lolium perenne . Clover genotypes had greater biomass when grown in association with grass genotypes that they had previously coexisted with (Aarssen & Turkington 1985). However, in experiments designed to explicitly consider soil microbes, authors found biotic specialization between the plant species was only evident when Rhizobium isolated from parental Trifolium was included (Chanway et al. 1989), demonstrating the pattern of local adaptation was microbe-mediated.