An empirical test of partner choice mechanisms in a wild legume–rhizobium interaction

Abstract

Mutualisms can be viewed as biological markets in which partners of different species exchange goods and services to their mutual benefit. Trade between partners with conflicting interests requires mechanisms to prevent exploitation. Partner choice theory proposes that individuals might foil exploiters by preferentially directing benefits to cooperative partners. Here, we test this theory in a wild legumerhizobium symbiosis.Rhizobial bacteria inhabit legume root nodules and convert atmospheric dinitrogen (N 2 ) to a plant available form in exchange for photosynthates. Biological market theory suits this interaction because individual plants exchange resources with multiple rhizobia. Several authors have argued that microbial cooperation could be maintained if plants preferentially allocated resources to nodules harbouring cooperative rhizobial strains. It is well known that crop legumes nodulate non-fixing rhizobia, but allocate few resources to those nodules. However, this hypothesis has not been tested in wild legumes which encounter partners exhibiting natural, continuous variation in symbiotic benefit.Our greenhouse experiment with a wild legume, Lupinus arboreus, showed that although plants frequently hosted less cooperative strains, the nodules occupied by these strains were smaller. Our survey of wild-grown plants showed that larger nodules house more Bradyrhizobia, indicating that plants may prevent the spread of exploitation by favouring better cooperators.

An experimental and modelling exploration of the host-sanction hypothesis in legume–rhizobia mutualism

“…Another proposed evidence of plant host sanctions, an inverse relationship between nodule size and strain fixation effectiveness in a field experiment using Lupinus arboreus plants and associated Bradyrhizobium spp. was reported (Simms et al, 2006). However, nodule rhizobial population sizes were measured and related only to nodule size and not to strain efficiency in independently field collected nodules (Simms et al, 2006), thus not really testing the main host sanction assumption.…”

“…was reported (Simms et al, 2006). However, nodule rhizobial population sizes were measured and related only to nodule size and not to strain efficiency in independently field collected nodules (Simms et al, 2006), thus not really testing the main host sanction assumption.…”

“…Under a restrictive scenario, that the only source of nitrogen is from symbiosis, experimental plants survive in good conditions and simulated plants are able of maintaining viable populations despite being cheated by non-fixing rhizobia when they can at least get some amount of fixed N 2 from the effectively mutualistic rhizobia occupying some nodules, which is a common situation in field (Amarger, 1981;Singleton and Tavares, 1986;Simms et al, 2006). Taken together, the experimental results and the simulation outcomes provide evidence against functioning plant host sanctions.…”

Human selection and the relaxation of legume defences against ineffective rhizobia

“…Legumes that preferentially allocate resources to nodule rhizobia on the basis of their actual symbiotic performance are likely to promote the evolution of higher levels of N 2 fixation while directly increasing their own fitness ( West et al 2002a,b). Sanctions can result in nodule growth differences, which have been documented in soya bean (Singleton & Stockinger 1983;Kiers et al 2003Kiers et al , 2006 and recently in wild lupines (Simms et al 2006). These sanctions tend to increase the N return on a plant's C investment.…”

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

“…By avoiding the costs, cheaters could outcompete reciprocating members and might drive the mutualism to an antagonism (Bronstein 2001). Cheaters exist in many mutualisms, such as ant-plant protection mutualisms (Edwards et al 2010), the legume-rhizobia symbiosis (Simms et al 2006), and the plant-mycorrhizal symbiosis (Bever et al 2009). Bronstein (2001) noted that some cheaters are conditional, behaving mutualistically in some contexts but parasitically in others.…”