Inbreeding diminishes herbivore-induced metabolic responses in native and invasive plant populations

Inbreeding and herbivory can interactively reduce the performance of flowering plants. Here, we investigated whether the magnitude of plant inbreeding depression increases under herbivory as a result of diminished leaf metabolic responses to herbivory in inbreds, which entails increased herbivore growth and feeding damage. We additionally explored whether genetic differentiation among native and invasive plant populations impacts the magnitude and direction of these inbreeding x herbivory interactions. Inbred and outbred plants from eight European (native) and eight North American (invasive) populations of Silene latifolia were exposed to two consecutive control or herbivory treatments (infestation with larvae of Mamestra brassicae). After the first treatment, leaf metabolic responses to herbivory were assessed with untargeted metabolic fingerprinting using UHPLC-ESI+-QTOF-MS/MS. After the second herbivory treatment, herbivore growth and plant feeding damage were assessed. Moreover, plant performance traits were recorded 4 weeks after the second herbivory treatment. Metabolic fingerprinting revealed that changes in the pool sizes of various metabolic features in response to herbivory were less intense in inbred than outbred plants from native and invasive populations. While herbivore growth and feeding damage were largely unaffected by plant breeding status in invasive populations, herbivores consumed more biomass from, but showed reduced growth on, inbred than outbred native plants. The magnitude of inbreeding depression in plant performance traits was not affected by herbivory. Synthesis. Our findings suggest that inbreeding compromises herbivory-induced metabolic defences in S. latifolia, and simultaneously reduces the nutritional quality of plants. The magnitude and direction of these inbreeding effects were shaped by genetic differentiation among native and invasive plants. These range-specific responses provide novel insights into the role of inbreeding x herbivory interactions in invasion success.