Evidence of within-species specialization by soil microbes and the implications for plant community diversity.

Microbes are thought to maintain diversity in plant communities by specializing on particular species, but it is not known whether microbes that specialize within species (i.e., on genotypes) affect diversity or dynamics in plant communities. Here we show that soil microbes can specialize at the within-population level in a wild plant species, and that such specialization could promote species diversity and seed dispersal in plant communities. In a shadehouse experiment in Panama, we found that seedlings of the native tree species, Virola surinamensis (Myristicaceae), had reduced performance in the soil microbial community of their maternal tree compared with in the soil microbial community of a nonmaternal tree from the same population. Performance differences were unrelated to soil nutrients or to colonization by mycorrhizal fungi, suggesting that highly specialized pathogens were the mechanism reducing seedling performance in maternal soils. We then constructed a simulation model to explore the ecological and evolutionary consequences of genotype-specific pathogens in multispecies plant communities. Model results indicated that genotype-specific pathogens promote plant species coexistence-albeit less strongly than species-specific pathogens-and are most effective at maintaining species richness when genetic diversity is relatively low. Simulations also revealed that genotype-specific pathogens select for increased seed dispersal relative to species-specific pathogens, potentially helping to create seed dispersal landscapes that allow pathogens to more effectively promote diversity. Combined, our results reveal that soil microbes can specialize within wild plant populations, affecting seedling performance near conspecific adults and influencing plant community dynamics on ecological and evolutionary time scales.

Microbial cross-feeding promotes multiple stable states and species coexistence, but also susceptibility to cheaters.

Mutualism, interspecific cooperation that yields reciprocal benefits, can promote species coexistence, enhancing biodiversity. As a specific form of mutualism, cross-feeding, where each of two mutualists produces a resource the other one needs, has been broadly studied. However, few theoretical studies have examined competition between cross-feeding mutualists and cheaters, who do not synthesize resources themselves. In this paper we study a model with two mutualists, a cheater, two micronutrients that are synthesized and exchanged by the mutualists, and one macronutrient that is only from external supply. We investigate the coexistence of the species in the framework of resource competition theory. In particular, we examine the effect of the mutualists' synthesis rates on their coexistence. In the absence of cheaters, multiple stable states occur if the synthesis rates are high, and higher synthesis rates increase the possibility that mutualists coexist. However, when the cheater is present, higher synthesis rates promote invasion by the cheater: If the cheater is superior on all three resources, it will either persist with at most one mutualist or even trigger extinction of all three species; if the cheater is only superior on the macronutrient, both mutualists may still coexist with the cheater. Our results provide a framework for further study on more complex mutualistic networks and real microbial communities.

Soilborne fungi have host affinity and host-specific effects on seed germination and survival in a lowland tropical forest.

The Janzen-Connell (JC) hypothesis provides a conceptual framework for explaining the maintenance of tree diversity in tropical forests. Its central tenet-that recruits experience high mortality near conspecifics and at high densities-assumes a degree of host specialization in interactions between plants and natural enemies. Studies confirming JC effects have focused primarily on spatial distributions of seedlings and saplings, leaving major knowledge gaps regarding the fate of seeds in soil and the specificity of the soilborne fungi that are their most important antagonists. Here we use a common garden experiment in a lowland tropical forest in Panama to show that communities of seed-infecting fungi are structured predominantly by plant species, with only minor influences of factors such as local soil type, forest characteristics, or time in soil (1-12 months). Inoculation experiments confirmed that fungi affected seed viability and germination in a host-specific manner and that effects on seed viability preceded seedling emergence. Seeds are critical components of reproduction for tropical trees, and the factors influencing their persistence, survival, and germination shape the populations of seedlings and saplings on which current perspectives regarding forest dynamics are based. Together these findings bring seed dynamics to light in the context of the JC hypothesis, implicating them directly in the processes that have emerged as critical for diversity maintenance in species-rich tropical forests.

Competition and coexistence between a syntrophic consortium and a metabolic generalist, and its effect on productivity.

Syntrophic interactions, where species consume metabolites excreted by others, are common in microbial communities, and have uses in synthetic biology. Syntrophy is likely to arise when trade-offs favor an organism that specializes on particular metabolites, rather than all possible metabolites. Several trade-offs have been suggested; however, few models consider different trade-offs to test which are most consistent with observed patterns. Here, we develop a differential equation model to study competition between a syntrophic processing chain, where each microbe can perform one step in metabolizing an initial resource to a final state, and a metabolic generalist that can perform all metabolic functions. We also examine how competition affects the production of the final metabolic compound. We find that competitive outcomes can be predicted by a generalization of the R(⁎)-rule and relative nonlinearity. Therefore, the species that can persist at the lowest resource level is the competitive dominant in a constant environment, and species can coexist by partitioning variation in resources. We derive a simple rule for predicting production rates of the final metabolite, and show that competition may not maximize final metabolite production. We show that processing chains are inherently less efficient, because resources are lost during each step of the process. Our results also suggest which trade-offs are capable of explaining certain empirical observations. For example, processing chains appear to be more common in nutrient-rich environments; our model suggests that a specificity trade-off and an affinity-yield trade-off would not predict this, but a yield-maximum growth trade-off might.