Symbiotic specialization and the potential for genotypic coexistence in a plant-bacterial mutualism.

Abstract

Genotypes of the annual legume Amphicarpaea bracteata vary in their degree of specialization toward different nitrogen-fixing bacteria. Plants of lineages "Ib" and "II" are specialized for mutualism with a limited group of bacterial genotypes. Lineage "Ia" plants are symbiotic generalists, interacting with all bacteria associated with specialist (Ib and II) plants, and also with a distinct class of bacteria that only fix nitrogen with lineage Ia plants. The relative performance of generalist and specialist plant lineages was measured in four symbiotic environments: (1) in the absence of nitrogen-fixing bacteria, (2) with bacteria with broad host ranges, (3) with bacteria specialized on lineage Ia hosts, and (4) with a mixture of the bacteria with broad and narrow host ranges. In the presence of bacteria with broad host ranges, the relative performance of different plant lineages was inconsistent among experimental replicates. However, lineage Ia plants had nearly 3 times higher total biomass and 6 times higher seed biomass than lineage Ib or II plants when grown with bacteria specialized on Ia hosts. When exposed to a mixture of bacteria with broad and narrow host ranges, generalist plants had 72% higher total biomass and >100% higher seed biomass than specialist plants. These results imply that in diverse natural populations, where all plants have a choice of symbiotic partners, mutualistic interactions are likely to foster competitive exclusion rather than stable coexistence of different plant lineages.