The sharp boundaries between harsh, heavy metal-laden serpentine soils and adjacent milder soils drive striking patterns in fine-scale local adaptation in plants. However, little is known about whether these same patterns exist for mutualistic, symbiotic soil microbes, which play a critical role in plant fitness. Soil microbes may not have an evolutionary response similar to their plant hosts if they do not experience serpentine as a source of strong selection or if other constraining forces, such as higher rates of migration across serpentine boundaries, impede adaptation. This research utilized 450 native and invasive rhizobia lineages isolated from root nodules from both serpentine and adjacent non-serpentine population of legumes to investigate adaptive divergence in microbial mutualists. Rhizobia were cultured in the free-living state to examine: 1) Serpentine as a source of selection: Is the nickel present in serpentine stressful to rhizobia? 2) Adaptive divergence: Do serpentine lineages outperform non-serpentine lineages in the presence of nickel and non-serpentine lineages outperform serpentine lineages in the absence of nickel? 3) Cost of tolerance: Is there a tradeoff between high nickel tolerance and performance in the absence of nickel?
Results/Conclusions
The elevated levels of nickel present in serpentine soils imposed strong selection on rhizobia. In the native rhizobia, serpentine lineages outperformed non-serpentine lineages in the presence of nickel, and non-serpentine lineages outperformed serpentine lineages in the absence of nickel. However, this pattern was not apparent in the invasive rhizobia. On average, nickel tolerance imposed a small cost with respect to performance in the absence of nickel, however, this cost was not apparent in all populations. This study demonstrates that native rhizobia with a long evolutionary history on serpentine grasslands exhibit fine-scale adaptive divergence in response to selection differentials across serpentine soil boundaries, similar to their host legume. Newly arrived invasive rhizobia may not demonstrate similar patterns in adaptive divergence, despite the rapid evolution of local adaptation in their host legume. The small and inconsistent cost of nickel tolerance supports other recent findings suggesting that fine-scale heterogeneity in selection on natural populations may result in low- or no-cost tolerance phenotypes. These results suggest that selection on microbial symbionts may have important consequences for plant-microbe mutualisms in complex mosaics of habitat.