Soil microbiota explain differences in herbivore resistance between native and invasive populations of a perennial herb

Soil microbiota can either slow down or facilitate plant invasions through their effects on plant performance. Associations with soil microbiota can also modify other plant traits such as herbivore resistance, which can indirectly affect the outcome of plant introductions. We studied the effects of soil microbiota on the perennial herbaceous legume Lupinus polyphyllus that hosts nitrogen-fixing mutualistic bacteria. We compared the plant performance, herbivore resistance and volatile organic compounds (VOCs) of plants from native (North American) and invasive (Finnish) populations of the species that were inoculated with intact or autoclaved soil from an invasive population. We found that plants of both origins greatly benefited from the intact soil inoculum with respect to all performance measures considered, suggesting that beneficial nitrogen-fixing rhizobia in the soil play a major role in shaping plant phenotypes. For three traits, effects of the intact soil inoculum were stronger in plants of native origin than in plants of invasive origin (number of leaves, herbivore resistance and total biomass). With the intact soil inoculum, plants of invasive origin were more resistant to snails than plants of native origin. Strikingly, differences in resistance to snails between plants of different origins disappeared entirely when soil microbes were reduced. Soil inoculum treatment altered the composition of the leaf VOC bouquet similarly regardless of plant origin. Synthesis. These results demonstrate the ability of Lupinus polyphyllus to associate with and benefit from putatively novel soil microbiota including rhizobia, which has likely contributed to its invasion success. Furthermore, it appears that the invasive populations have adapted to be less reliant on their symbionts, which further facilitates species spread. To our knowledge, this is the first study to demonstrate that differences in herbivore resistance between native and invasive plant populations of the same species can depend entirely on soil microbiota.

Automated summary

This study demonstrates the significance of soil microbiota on the plant performance, herbivore resistance, and volatile organic compounds production in Lupinus polyphyllus. The intact soil inoculum has a greater impact on plants of native origin, while plants of invasive origin exhibit higher resistance to snails. However, this resistance difference disappears when soil microbes are reduced.