Tripartite mutualism: Facilitation or trade-offs between rhizobial and mycorrhizal symbionts of legume hosts

PREMISE OF THE STUDY: Multiple mutualist effects (MMEs) are common in nature, yet we lack a predictive understanding of how two mutualists on the same host will influence each other and whether these effects will be positive or negative. Leguminous plants maintain root symbioses with two nutritional mutualists: rhizobia that fix atmospheric nitrogen and arbuscular mycorrhizal fungi (AMF) that increase phosphorus uptake. Both symbionts receive plant carbon, and host genetic networks that regulate colonization are partially shared by both symbioses; whether these factors generate trade-offs or facilitation between rhizobial and AMF symbionts of legumes is not well known. METHODS: We evaluated host allocation to each symbiont in three settings. First, in situ in a remnant prairie, then in a greenhouse experiment with multiple plant populations, and finally under manipulated rhizobium densities in the greenhouse. KEY RESULTS: In the remnant prairie, rhizobium nodule number and colonization of AMF were positively correlated, and plants with increased nodule number had higher fitness in the field, generating indirect selection on the colonization of AMF. In the greenhouse experiment, allocation to each symbiont was genetically variable among populations, with some suggestion that rhizobium and AMF colonization are positively genetically correlated. Finally, increasing the number of rhizobia in the soil decreased AMF colonization. CONCLUSIONS: Our results suggest that trade-offs between plant colonization by rhizobia and AMF are context dependent and might not be common under field conditions, but that physiological and/or genetic drivers couple these two symbioses in nature.