Introduction
Major evolutionary innovations and events that span the tree of life are
the result of host interactions with microorganisms. Perhaps the most
dramatic example of microbe-mediated evolutionary events occurred when
symbioses with the bacterial predecessors of chloroplasts and
mitochondria were incorporated as part of the host cell (Sagan 1967). In
more recent evolutionary history, the gut microbiome has been implicated
in the rapid diversification of herbivorous mammals (Price et al.2012) and wasps (Brucker & Bordenstein 2013). In these cases,
interactions with microbiota transformed the macroevolutionary
trajectory of their hosts. There is accumulating evidence that
microorganisms are also affecting patterns of host adaptation on
microevolutionary timescales.
The human microbiome project as well as work with other vertebrates,
insects, and plants has illuminated a complex feedback loop of host
affecting microbial form and function and microbial form and function
feeding back to affect host phenotype (Fig. 1A; Kohl et al. 2014;
Mueller & Sachs 2015; Sanders et al. 2015; Weese et al.2015; Gehring et al. 2017; Moeller et al. 2019; Petipaset al. 2020a). Host genotypes enrich for specific microbiome
components. For example, the mycorrhizal communities associated with
Pinyon pines are almost entirely determined by pine morphotype (Gehringet al. 2017), soil microbiomes differ across Arabidopsis
thaliana genotypes (Bulgarelli et al. 2012; Lundberg et
al. 2012), and both mouse (Benson et al. 2010) and human
(Goodrich et al. 2014) genotype shape their respective
microbiomes. Reciprocally, this variation in microbiome composition can
affect host phenotypes and performance. Across host organisms, the
microbiome can affect nutrient acquisition (Krajmalnik-Brown et
al. 2012; Newell & Douglas 2014), for example, access to phosphorus is
often mediated by the unique enzymatic capabilities of arbuscular
mycorrhizal fungi (Smith & Read 2008). Microbes also affect stress
tolerance (Bang et al. 2018), immune phenotype (Foster et
al. 2017), and pathogen susceptibility (King et al. 2016). For
example, microbial symbionts of aphids provide their insect hosts with
enhanced heat tolerance (Russell & Moran 2006), and Clostridiumin the human gut produces butyrate, a compound essential to host immune
homeostasis (Velasquez-Manoff 2015). Often these changes are assumed to
be adaptive (i.e. increasing host fitness, Kohl & Carey 2016) but this
assumption is rarely tested. If these microbial effects increase host
fitness then they can lead to microbe-mediated
adaptation , defined as enhanced host fitness in a particular
environment that is partially or entirely the result of interacting with
microorganisms.
Adaptive responses can occur through local adaptation or adaptive
plasticity, two non-mutually-exclusive responses to the heterogeneous
selection pressures species experience in nature. Local adaptation is
the result of genetic differentiation in response to local conditions
and is manifest when local genotypes have higher fitness in their home
habitat compared with foreign genotypes (Kawecki & Ebert 2004).
Adaptive plasticity is a form of phenotypic plasticity and is manifest
when the environment affects organismal traits in ways that increase
fitness in that particular environment (i.e., local phenotypeshave higher fitness in their home habitat compared with foreignphenotypes ; Dudley & Schmitt 1996). Both local adaptation and
phenotypic plasticity might be influenced by microbes, where in the
absence of microbes you might observe low fitness and no pattern of
local adaptation (Fig. 1B). We propose that microbe-mediated adaptive
responses are the result of microbe-mediated local adaptationwhen local host genotypes have higher fitness than foreign genotypes
because of a genotype-specific affiliation with locally important
microbes (Fig. 1C), or microbe-mediated adaptive plasticitywhen local host phenotypes have higher fitness than foreign phenotypes
as a result of interactions with locally important microbes (Fig. 1D).
Although microbe-mediated adaptation (including both microbe-mediated
local adaptation and microbe-mediated phenotypic plasticity) may occur
for many taxa (Alberdi et al. 2016; Sharpton 2018; Trevellineet al. 2019; Moeller & Sanders 2020), here we focus primarily on
plants for three reasons: 1) The foundation for investigations into
microbe-mediated adaptation have been laid through decades of avid
interest in plant-microbe interactions. 2) Plants are tractable
experimental systems amenable to classic experimental designs for
testing local adaptation and adaptive plasticity, and 3) as sessile
organisms, plants cannot move to escape stress and therefore may be even
more dependent on microbes for adaptive responses. Additionally, while
many interactions with microorganisms may be antagonistic (reducing
plant fitness), here we focus on local adaptation to beneficial
microorganisms as they have the potential to affect host adaptive
responses, thus providing a unique avenue to adaptation. The population
level consequences of antagonistic interactions have been extensively
discussed elsewhere (e.g. Thompson 2005).
There are a growing number of examples showing that microbes canaffect adaptive plant responses (Chanway et al. 1989; Schultzet al. 2001; Johnson et al. 2010, 2013; Smith et
al. 2012; Lau & Lennon 2012; Lankau & Nodurft 2013; Wagner et
al. 2014; Pickles et al. 2015; Barrett et al. 2016; RĂșaet al. 2016; Van Nuland et al. 2016; Revillini et
al. 2016; Gehring et al. 2017; Porter et al. 2020). Here
we provide a framework that first identifies and defines the potential
patterns and processes underlying microbe-mediated effects on adaptation
(i.e., microbe-mediated local adaptation and microbe-mediated adaptive
plasticity) and then propose empirical approaches to identify and
differentiate between these two modes of microbe-mediated adaptation.
Finally, we discuss implications and propose future research directions
in the study of microbe-mediated adaptation.