Preferential allocation to beneficial symbiont with spatial structure maintains mycorrhizal mutualism

Abstract

Mutualisms, beneficial interactions between species, are expected to be unstable because delivery of benefit likely involves fitness costs and selection should favour partners that deliver less benefit. Yet, mutualisms are common and persistent, even in the largely promiscuous associations between plants and soil microorganisms such as arbuscular mycorrhizal fungi. In two different systems, we demonstrate preferential allocation of photosynthate by host plants to the more beneficial of two AM fungal symbionts. This preferential allocation could allow the persistence of the mutualism if it confers sufficient advantage to the beneficial symbiont that it overcomes the cost of mutualism. We find that the beneficial fungus does increase in biomass when the fungi are spatially separated within the root system. However, in well-mixed fungal communities, non-beneficial fungi proliferate as expected from their reduced cost of mutualism. Our findings suggest that preferential allocation within spatially structured microbial communities can stabilize mutualisms between plants and root symbionts.

The Coexistence of Hosts with Different Abilities to Discriminate against Cheater Partners: An Evolutionary Game-Theory Approach

“…While Foster and Kokko (2006) have demonstrated the importance of variability in partner cooperation to maintain host discrimination, our model proposes that cheaters can facilitate host species coexistence. The existence of host species with different capacities to discriminate against cheater partners has recently been demonstrated to occur in a wide variety of mutualisms (Pellmyr 1994;Keirs et al 2007;Bever et al 2009;Heil et al 2009;Jandér and Herre 2010;Kiers et al 2011;Grman 2012), suggesting these population dynamics may be a general feature of mutualisms. In this context, giving and discriminating hosts act as reservoirs of the cheater and mutualist partners each requires to coexist.…”

“…Arbuscular mycorrhizal fungi have a large incentive to cheat (high cost of mutualism), with a steep trade-off between providing host benefits via nutrient acquisition and enhancing their own competitive ability within a host root (Bennett and Bever 2009;Bever et al 2009). Consistent with this finding, several generalist mycorrhizal species have evolved to exploit plant C without providing any benefits (Graham and Abbott 2000;Burleigh et al 2002;Smith et al 2003Smith et al , 2004Koch et al 2006;Violi et al 2007).…”

Stochastic distribution of small soil eukaryotes resulting from high dispersal and drift in a local environment

“…The importance of aboveground interactions on these groups was also supported by the scale of the observed spatial autocorrelation range in EcM fungi, which nearly corresponded to that in the spatial distribution of trees in our study sites. Spatial distance has an important role in maintaining symbiotic (Bever et al, 2009) and pathogenic relationships (Kerr et al, 2006) through positive and negative soil feedbacks, respectively. At very fine scales (o2 m), spatial autocorrelation resulting from aggregate growth of individuals affects community turnover in certain eukaryotic microbes.…”

Evolution of microbial markets

“…For instance, if more food-providing vervet monkeys are introduced in a population, the grooming services received as payment decrease (31). species preferentially supporting rhizobial symbionts that provide more fixed N 2 for hosts (39)(40)(41) and in the arbuscular mycorrhizal mutualism in which host plants allocate more carbon resources to fungal strains providing more nutrient resources (42,43).…”