The evolutionary implications of exploitation in mycorrhizas

Abstract

Some views of mutualism, where the fitness of two symbiotic partners is higher in association than when apart, assume that they necessarily evolve towards greater benefit for the partners. Most mutualisms, however, seem prone to conflicts of interest that destabilize the partnership. These conflicts arise in part because mutualistic outcomes are conditional, depending upon complex interactions between environmental, developmental, and genotypic factors. Mutualisms are also subject to exploitation or cheating. Although various compensating mechanisms have been proposed to explain how mutualism can be maintained in the presence of exploiters, none of these mechanisms can eliminate exploitation. In this paper we explore various compensating mechanisms in mycorrhizas, examine the evidence for exploitation in mycorrhizas, and conclude that mycorrhizal mutualisms exhibit characteristics that are more consistent with a concept of reciprocal parasitism. We propose that researchers should not assume mycorrhizas are mutualistic based upon structural characteristics or limited functional studies showing bilateral exchange and should view mycorrhizas as occupying a wider range on the symbiotic continuum, including commensalism and antagonism. We recommend that comparative studies of mycorrhizas incorporate other types of root associations that have traditionally been considered antagonistic.Key words: mycorrhizas, mutualism, exploiters, compensating mechanisms, symbiotic continuum.

Variation in ectomycorrhizal fungal communities associated with Oreomunnea mexicana (Juglandaceae) in a Neotropical montane forest

“…Several authors have also noted that EM fungi associated with N-rich habitats may form less beneficial or parasitic relationships with their hosts (Johnson et al 1997;Egger and Hibbett 2004;Avis 2012). It is possible that less beneficial EM fungi reduce the competitive advantage of Oreomunnea relative to co-occurring tree species in the more fertile sites studied here (Table 1).…”

Plant species differ in their ability to reduce allocation to non‐beneficial arbuscular mycorrhizal fungi

“…The plant-arbuscular mycorrhizal symbiosis is vulnerable to conditional cheaters (Egger and Hibbett 2004). In this symbiosis, plant response ranges along the mutualism-parasitism continuum (Johnson et al 1997).…”

Testing the ecological stability of ectomycorrhizal symbiosis: effects of heat, ash and mycorrhizal colonization on Pinus muricata seedling performance

“…A number of recent studies have highlighted the need for investigation of the effects of spatial and temporal variation in the environment on the outcome of mutualistic interactions (Bronstein 1994(Bronstein , 2001Egger and Hibbett 2004;Herre et al 1999;Jones and Smith 2004). Much of the interest in this topic was generated by Bronstein's (1994) conclusion that conditional exploitation-the change of a normally '+' '+' to a '+' '−' interaction-should be fairly common in mutualisms that are affected by ecological context.…”

“…Johnson et al 1997). Ectomycorrhizal interactions occur in a wide range of environments and exhibit few of the characteristics thought to stabilize mutualisms, such as vertical transmission, genotypic uniformity and limited number of symbionts (Egger and Hibbett 2004;Herre et al 1999), making conditional exploitation seem a likely outcome. While there are a number of good examples of host plant exploitation by arbuscular mycorrhizal fungi (Jones and Smith 2004;Klironomos 2002), the evidence for exploitation by ectomycorrhizal fungi is limited.…”