Evolutionary dynamics of rhizopine within spatially structured rhizobium populations

Abstract

Symbiosis between legumes and nitrogen-¢xing bacteria is thought to bring mutual bene¢t to each participant. However, it is not known how rhizobia bene¢t from nodulating legume hosts because they ¢x nitrogen only after becoming bacteroids, which are terminally di¡erentiated cells that cannot reproduce. Because undi¡erentiated rhizobia in and around the nodule can reproduce, evolution of symbiotic nitrogen ¢xation may depend upon kin selection. In some hosts, these kin may persist in the nodule as viable, undi¡erentiated bacteria. In other hosts, no viable rhizobia survive to reproduce after nodule senescence. Bacteroids in these hosts may bene¢t their free-living kin by enhancing production of plant root exudates. However, unrelated non-mutualists may also bene¢t from increased plant exudates. Rhizopines, compounds produced by bacteroids in nodules and catabolized only by related free-living rhizobia, may provide a mechanism by which bacteroids can preferentially bene¢t kin. Despite this apparent advantage, rhizopine genotypes are relatively rare. We constructed a mathematical model to examine how mixing within rhizobium populations in£uences the evolution of rhizopine genotypes. Our model predicts that the success of rhizopine genotypes is strongly dependent upon the spatial genetic structure of the bacterial population; rhizopine is more likely to dominate well-mixed populations. Further, for a given level of mixing, we ¢nd that rhizopine evolves under a positive frequency-dependent process in which stochastic accumulation of rhizopine alleles is necessary for rhizopine establishment. This process leads to increased spatial structure in rhizobium populations, and suggests that rhizopine may expand the conditions under which nitrogen ¢xation can evolve via kin selection.

Sanctions and mutualism stability: why do rhizobia fix nitrogen?

“…It has been suggested that the main driving force for N 2 fixation is that it increases the root exudation of materials that can support rhizobial metabolism, and that this provides a kin-selected benefit to related rhizobia in the rhizosphere (Olivieri & Frank 1994;Simms & Bever 1998;Bever & Simms 2000;Crespi 2001). In this section we argue that this mechanism is unlikely to be generally important for several reasons.…”

Kin competition and the evolution of cooperation

“…As with the Agrobacterium system, these increased plant exudates sometimes include specialized resources (rhizopines) that can only be catabolized by other rhizobia 50 . Recently, several authors have argued that the evolution of cooperation among rhizobia is strongly hindered by kin competition at the nodule 51, 52 .…”

Controlling the reproductive fate of rhizobia: how universal are legume sanctions?

“…It has been suggested that rhizopines help promote rhizobial mutualism via kin selection by increasing the flux of root exudates to related, reproductively viable rhizobia in the rhizosphere (Olivieri & Frank, 1994; Simms & Bever, 1998). Such a mechanism relies on the assumption that the rhizobia receiving the benefits are closely related to the rhizobia in the root nodules, and that this relatedness arises through limited dispersal (Bever & Simms, 2000).…”

“…Such a mechanism relies on the assumption that the rhizobia receiving the benefits are closely related to the rhizobia in the root nodules, and that this relatedness arises through limited dispersal (Bever & Simms, 2000). However, this form of kin selection has stringent requirements for spatial genetic structures of the bacterial population outside the nodule (Simms & Bever, 1998). Given that spatial structure also undermines cooperation by making competition more local (West et al ., 2001), within‐nodule kin selection is likely to be the only form of selection strong enough to consistently promote cooperation.…”