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.