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

Abstract

Inbreeding and enemy infestation are common in plants and can synergistically reduce their performance. This inbreeding ×environment (I × E) interaction may be of particular importance for the success of plant invasions if introduced populations experience a release from attack by natural enemies relative to their native conspecifics. Here, we investigate whether inbreeding affects plant infestation damage, whether inbreeding depression in growth and reproduction is mitigated by enemy release, and whether this effect is more pronounced in invasive than native plant populations. We used the invader Silene latifolia and its natural enemies as a study system. We performed two generations of experimental out‐ and inbreeding within eight native (European) and eight invasive (North American) populations under controlled conditions using field‐collected seeds. Subsequently, we exposed the offspring to an enemy exclusion and inclusion treatment in a common garden in the species’ native range to assess the interactive effects of population origin (range), breeding treatment, and enemy treatment on infestation damage, growth, and reproduction. Inbreeding increased flower and leaf infestation damage in plants from both ranges, but had opposing effects on fruit damage in native versus invasive plants. Inbreeding significantly reduced plant fitness; whereby, inbreeding depression in fruit number was higher in enemy inclusions than exclusions. This effect was equally pronounced in populations from both distribution ranges. Moreover, the magnitude of inbreeding depression in fruit number was lower in invasive than native populations. These results support that inbreeding has the potential to reduce plant defenses in S. latifolia, which magnifies inbreeding depression in the presence of enemies. However, future studies are necessary to further explore whether enemy release in the invaded habitat has actually decreased inbreeding depression and thus facilitated the persistence of inbred founder populations and invasion success.

Inbreeding in a dioecious plant has sex- and population origin-specific effects on its interactions with pollinators

“…The assumption that sex-specific viability selection plays a role in the expression of inbreeding depression seems likely for S. latifolia. Previous research elaborated that females of this species experience resource depletion stress more often than males in the late growing season during fruit maturation (Gehring and Monson, 1994) and that inbreeding reduces resistance to environmental stress (Schrieber et al, 2018(Schrieber et al, , 2019. Another non-exclusive explanation for the different inbreeding effects on female versus male S. latifolia may be found in sexual selection.…”

Sex and origin-specific inbreeding effects on flower attractiveness to specialised pollinators

“…The field sampling, rearing conditions and experimental crossing are described in detail in (Schrieber et al, 2018(Schrieber et al, , 2019. Seeds were dried and stored at room temperature until use.…”

“…As colonization events are associated with successive demographic bottlenecks, purging is expected to be one determinant for the successful establishment and proliferation of plant populations in novel habitats (Facon et al, 2011;Schrieber and Lachmuth, 2017). However, only few empirical studies verified the role of purging in plant colonization success by revealing significantly lower inbreeding depression following experimental crossings in invasive than native plant populations (Rosche et al, 2016;Schrieber et al, 2019). Again, the focus of these studies was on fitness components rather than floral attractiveness traits.…”

“…Natural S. latifolia populations partly suffer from biparental inbreeding due to limited seed and pollen dispersal (McCauley, 1997). As inbreeding reduces not only fitness (Teixeira et al, 2009), but also impairs interactions with herbivorous insects in S. latifolia (Schrieber et al, 2018(Schrieber et al, , 2019, a disruption of plant-pollinator interactions can be expected for this species. Moreover, the dioecious reproductive system of S. latifolia provides the opportunity to quantify variation in the magnitude of inbreeding effects in these traits among females and males.…”

Genetic and epigenetic regulation of phenotypic variation in invasive plants – linking research trends towards a unified framework

“…(Campbell et al 2013;Kariyat et al 2012;Kristensen et al 2010). Recent empirical studies support that inbreeding x environment interactions can prevent or foster successful invasion (Hufbauer et al 2013;Rosche et al 2017;Schrieber et al 2019), while molecular studies suggest that epigenetic modifications play a decisive role in stress responses (Chinnusamy and Zhu 2009) and the expression of inbreeding depression. For example, a study on Scabiosa columbaria (a self-compatible but predominantly outcrossing species) revealed that inbreeding caused inbreeding depression for fitness-related traits and increased methylation levels (Vergeer et al 2012).…”