1. Local coevolutionary selection
Coevolutionary selection between two species within a single local community, that is local coevolutionary selection, has the potential to act as a potent evolutionary force on the traits of species by virtue of the feedbacks driven by its inherent reciprocality. The reciprocality of coevolutionary selection means that the fitnesses of two interacting species both depend not only on their own genotype (and associated traits), but also on the distribution of genotypes (and traits) in the other species. Specifically, there is a genotype by genotype (G × G) interaction effect on the fitnesses of both species. As a result of this reciprocality, adaptive changes in the traits of one species in response to selection may trigger subsequent adaptive changes in the traits of the second species, which in turn feed back to cause adaptive evolution of the first species, and so on. Put another way, the relative fitness of genotypes in one species is context-dependent and the context itself can also evolve (Wade, 2003). For example, the relative fitnesses of different genotypes of a hummingbird and a hummingbird-pollinated plant depend not only on hummingbird bill shape (which differs among hummingbird genotypes), or on flower morphology (which differs among plant genotypes), but on the match between the two, generating a G × G interaction for both hummingbird fitness and plant fitness. If hummingbird bill shape adapts in response to selection driven by the average flower morphology in the plant, reciprocal selection on flower morphology (driven by the new average hummingbird bill shape) changes as a result.
2. Heritability and genetic architecture of candidate coevolving traits
The hummingbird flower example illustrates the point that coevolution occurs not between two species, but between phenotypic traits in two species (Kiester et al., 1984; Wade, 2003; Ridenhour, 2005). Thus, the first step in investigating the potential consequences of ongoing coevolution for mycorrhizal interactions must be to identify phenotypic traits of plants and mycorrhizal fungi that are potentially the targets of ongoing coevolutionary selection, and to assess the degree to which they are genetically variable among individuals and thus subject to natural selection (see Supporting Information Notes S1 for a discussion of related key concepts from quantitative genetics, and their application in analyzing mycorrhizal interactions).
3. The hierarchy of candidate coevolving traits in mycorrhizal interactions
Although most analyses of adaptive evolution have focused on single traits or small numbers of traits, it is now widely recognized in evolutionary biology that environments impose natural selection not on single traits, but simultaneously on complex suites of species traits (Lande & Arnold, 1983; Phillips & Arnold, 1989; Kingsolver et al., 2001; Blows, 2007). Furthermore, we now recognize that traits can be discerned at multiple levels of a hierarchy, ranging from the proteins produced directly by genes to higher level traits that result from integration of multiple components of an organism’s physiology (Whitham et al., 2006). Thus, consideration of potential traits under coevolutionary selection in mycorrhizal interactions may begin with lower level traits that are probably not far removed from the controlling genes in plants and fungi, but must also consider higher level traits, including those controlling the community structure of mycorrhizal interactions. For all of these candidate traits, we need studies of their phenotypic and genetic variability within and among populations, heritability, and genetic architecture (including correlations with other traits), so that that we can assess their potential to evolve in response to ongoing selection.
A priori, the most obvious candidate traits that may have at one time undergone coevolutionary selection in mycorrhizal interactions are the lower level traits controlling the formation of the mycorrhizal interface, for example the ability to form an arbuscule in AM symbioses or a Hartig net in ectomycorrhizal (EM) symbioses. However, I know of no studies estimating the heritability of these lower level traits, and it has been suggested that they are fixed within species of plants and mycorrhizal fungi (Morton, 1999), although screening of whole soil fungal communities for allelic variants of key functional genes (e.g. Artz et al., 2009) may increase our power to detect variation in such traits. Lower level traits governing specificity in signaling and recognition between interacting partners in mycorrhizal interactions deserve special attention as candidate coevolving traits because a high degree of specificity in such traits could allow coevolutionary cycling to drive fluctuating polymorphisms at corresponding recognition loci in plants and fungi, as has been found for the major histocompatibility complex (MHC) loci in vertebrates (Hughes & Nei, 1988) and self incompatibility loci in fungi (May & Matzke, 1995). For example, if plants are capable of some degree of specificity in recognition of fungi, then selection should strongly favor recognition by plants of beneficial vs nonbeneficial (pathogenic or mycorrhizal) taxa of fungi, and subsequent exclusion or rejection of nonbeneficial fungi (Kiers & van der Heijden, 2006; Bever et al., 2009). In turn, pathogenic or nonbeneficial mycorrhizal fungi would be under selection to avoid recognition, which would drive further reciprocal evolution in the recognition genes of the plant.
Some evidence points to the existence of some specificity in mycorrhizal signaling: AM plants can apparently distinguish between broad groups of soil fungi (AM vs ericoid vs pathogenic; Genre et al., 2009) and can under some circumstances allocate preferentially to more beneficial AM fungal partners (Bever et al., 2009), not all plant and AM or EM mycorrhizal fungal taxa exhibit identical preferences for each other (e.g. Molina et al., 1992; Halling, 2001; Vandenkoornhuyse et al., 2003), and molecules contained in root exudates have been shown to serve as signaling molecules for both the EM symbiosis (Lagrange et al., 2001) and the AM symbiosis (Reinhardt, 2007). However, we still have much to learn about specificity in mycorrhizal signaling as it relates to coevolution. In particular, the degree of specificity in recognition of signaling molecules by different members of the rhizosphere community is still poorly understood, and we have a pressing need for studies that quantify phenotypic variation and heritability of signaling and recognition traits within species of both plants and mycorrhizal fungi, including characterization of the range of specificity in those traits.
Mycorrhizal colonization intensity, measured as the proportional or absolute amount of root length or fine root tips colonized, is a higher level trait that potentially integrates all of the lower level traits discussed so far and may be controlled in part by genes in both plants and mycorrhizal fungi. Numerous studies have now demonstrated significant genetically based variation for these traits within plant species (e.g. Dixon et al., 1987; Graham & Eissenstat, 1994) and within fungal species (e.g. Lamhamedi et al., 1990; Burgess et al., 1994). Although only a handful of such studies have been designed to allow the estimation of the heritability of those traits (e.g. Rosado et al., 1994a,b; Kropp, 1997), the few examples suggest that, for some pairs of plant and fungal species in natural populations, sufficient additive genetic variation exists for coevolutionary selection to potentially act on these traits in both plants and mycorrhizal fungi (but see Gahoonia & Nielsen, 2004).
Some of the studies of variation in colonization intensity provide insight into the genetic architecture governing those traits in plants and fungi. Specifically, the distributions of such traits observed among progeny from controlled crosses (Lamhamedi et al., 1990; Kropp, 1997; Tagu et al., 2005) suggest that EM colonization intensity of tree hosts is under polygenic control, rather than under control by a small number of genes of major effect. Moreover, several studies (e.g. Toth et al., 1990; Zhu et al., 2001) have demonstrated reduced mycorrhizal colonization intensity in highly selected modern cultivars of crop plants compared with older cultivars, suggesting that artificial selection for crop traits (such as disease resistance) may have resulted in correlated selection against mycorrhizal colonization intensity. These results parallel those of a recent study showing how artificial selection has reduced the ability of modern cultivars of soybean (Glycine max) to benefit from root symbiosis with rhizobia bacteria (Kiers et al., 2007). Intriguingly, one study found that putative quantitative trait loci (QTLs) in the genome of the tree Populus trichocarpa controlling mycorrhizal colonization intensity by the EM fungus Laccaria bicolor mapped onto the P. trichocarpa genome very near a previously discovered QTL that contributes to mediation of poplar resistance to fungal rust pathogens (Tagu et al., 2005). If such findings are confirmed for poplar or other plants, they raise the possibility that one or more closely linked loci may have simultaneous (pleiotropic) effects on both mycorrhizal colonization and disease resistance traits of plants. This type of pleiotropy could potentially constrain coevolution of plants with mycorrhizal and/or pathogenic fungi, because the two types of partners may impose conflicting selection pressures on the same genes (Griswold & Whitlock, 2003).
A second class of higher level traits that potentially integrates the lower level traits discussed so far is the set of ecological interaction strengths for a particular interaction between an individual plant and a fungal genet. Relevant plant traits, for example, include the response of the plant to the presence of the fungus, in terms of absolute or relative performance. Many studies have now found significant genetic variation within plant or mycorrhizal fungal species (e.g. Boerner, 1990; Hetrick et al., 1995; Eason et al., 2001; Schultz et al., 2001; Koch et al., 2006; Piculell et al., 2008; Hoeksema et al., 2009; Karst et al., 2009; Seifert et al., 2009) for their ecological effect on or response to each other. For example, Koch et al. (2006) found significant variation in host-plant growth promotion among isolates from a natural population of the AM fungus Glomus intraradices. Schultz et al. (2001) found substantial differences between two ecotypes of the grass Andropogon gerardii for responsiveness to infection with AM fungi. These examples demonstrate the presence of genetic variability within or between natural populations for ecological effect and response traits of mycorrhizal interactions, allowing for the possibility that such traits could be subject to ongoing natural selection. As discussed for colonization intensity above, however, we understand very little about the specificity of these traits, and are in need of studies that test whether they vary depending on the identity of the partner species.
At the highest levels of the trait hierarchy we find traits that are referred to as ‘community phenotypes’ whereby the genotype of one species determines the composition of other species with which it interacts (Whitham et al., 2006). Some of the best examples of community phenotypes are emerging from studies of poplar trees (Populus species), where it has been shown that different plant genotypes host different communities of arthropods, bacteria, fungi, and vertebrates (Whitham et al., 2006). Some of these community phenotypes of poplar have high heritabilities, suggesting that these higher level traits have a genetic basis and that poplar populations could respond to natural selection by changing the communities of other species with which they interact. Whether such adaptations result from selection pressure by those same communities, and whether such adaptation would result in reciprocal selection pressure on those same communities, has not been determined. Several studies report significant genetic variation within plant species for mycorrhizal fungal community structure (e.g. Taylor et al., 2004; Korkama et al., 2006). Such studies provide intriguing evidence of a genetic basis in plants for mycorrhizal fungal community structure, raising the possibility that a plant population could adapt to changing environments via a shift in the species composition of the mycorrhizal fungal guild with which they are interacting. Fungal guild composition would only be considered a coevolving trait, however, if both plant and fungal fitnesses depend on fungal guild composition, and also on the traits of one or more members of the fungal guild.