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

Abstract

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 × 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.

Release from natural enemies mitigates inbreeding depression in native and invasive Silene latifolia populations

“…Overall invasive plants received more infestation damage, but exhibited similar or even higher values for fitness-related traits as native plants (Table 1). This observation has also been made in previous studies on S. latifolia (Blair & Wolfe, 2004;Schrieber et al, 2018Wolfe et al, 2004) and suggests that invasive populations evolved increased tolerance of enemy infestation. The evolution of increased tolerance during range expansion has been observed in several other plant species (Abhilasha & Joshi, 2009;Zou, Rogers, & Siemann, 2007) and is assumed to arise from shifts in the natural enemy community, that is, reduced attack by specialists and increased attack by generalist (Fornoni, 2011).…”

“…. latifolia populations investigated in the present study,Schrieber et al (2018) demonstrated that inbreeding significantly compromises the plants' metabolic responses to insect herbivory. This study also indicated that higher infestation damage on inbred S. latifolia individuals can result from compensatory feeding triggered by poor host plant quality.…”

“…Plants often exhibit increased susceptibility to enemies following inbreeding (Bello‐Bedoy & Núñez‐Farfán, ; Muola, Mutikainen, Laukkanen, Lilley, & Leimu, ; Stephenson, Leyshon, Travers, Hayes, & Winsor, ), since dominance and overdominance can either reduce the expression of genes that contribute directly to plant resistance against enemies (Kariyat, Mena‐Alí et al, ; Portman et al, ) or induce general stress responses that trade‐off against responses to environmental stressors such as natural enemies (Kristensen et al, ). Using the same inbred and outbred families of native and invasive S. latifolia populations investigated in the present study, Schrieber et al () demonstrated that inbreeding significantly compromises the plants’ metabolic responses to insect herbivory. This study also indicated that higher infestation damage on inbred S. latifolia individuals can result from compensatory feeding triggered by poor host plant quality.…”

“…Moreover, Schrieber, Schweiger, Kröner, and Müller (2018) demonstrated that inbreeding diminishes metabolic responses to herbivory in populations from both distribution ranges. Finally, invasive populations evolved differences in enemy susceptibility and performance (Blair & Wolfe, 2004;Keller, Sowell, Neiman, Wolfe, & Taylor, 2009;Wolfe, Elzinga, & Biere, 2004), making S. latifolia ideally suited for examining the impact of genetic differentiation on the outcomes of I × E interactions.…”

Interactions of Bunias orientalis plant chemotypes and fungal pathogens with different host specificity in vivo and in vitro

“…In addition, individual extracts of leaf material in the same composition as used in the bioassays, i.e., leaf material pooled from all plants per chemotype, and fractions of extracts from leaf material pooled from all plants including both chemotypes, were prepared. Samples were extracted in 90% methanol and chemical analysis was performed according to Schrieber et al (2019) 57 , but in negative electrospray ionisation mode and with further modifications of instrument settings and in processing raw data from chromatograms (see Supplementary Information Methods S3). UV absorption was recorded at 360 nm.…”