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).