Aphid infestation induces plant-sex-specific changes in floral chemistry and pollinator behaviour in Silene latifolia

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Abstract

Pollinators consistently share the complex information and resource landscape of their host plants with herbivores. Yet, how sap feeders affect floral attractiveness to pollinators remains poorly understood, despite the critical role of this tripartite interaction in natural and agricultural ecosystems. These intricate interactions may be further enriched by pronounced sexual dimorphisms in dioecious species. In this study, we examined how infestation by the oligophagous aphid Brachycaudus lychnidis affects sex-specific interactions among the dioecious plant Silene latifolia and its specialist moth pollinator Hadena bicruris . We exposed male and female plants to aphid herbivory and evaluated its effects on floral traits (visual cues, floral scent, and nectar chemistry) and pollinator behaviour. Contrary to sexual selection theory, female plants were not less attractive than males under control conditions. Instead, our results suggest that females exhibit plasticity in floral trait expression depending on pollination success. Moreover, both sexes produced a diverse array of potentially bioactive nectar metabolites, with females showing higher abundances of many compounds that may influence female pollinator behaviour. Aphid infestation altered floral traits differently between sexes, with stronger declines in female floral attractiveness, suggesting sex-specific defence strategies and possible involvement of indirect defences in stabilizing this specialized plant–pollinator– herbivore system.

Highlight

Aphid infestation alters multiple visual and chemical floral traits in a plant sex-specific manner, leading to reduced attractiveness to moth pollinators in female plants, but not in males.

Graphical Abstract

Plant-sex specific effect of aphid infestation on floral traits (number, size, colour, scent composition, nectar quantity and composition) and pollinator behaviour.

Abbreviations used in the main text

  • ANOVA: analysis of variance

  • FC, FA, MC, MA: female control, female aphid infested, male control, male aphid infested

  • GC-MS: gas chromatography-mass spectrometry

  • (G)L(M)M: (generalized) linear (mixed effects) model

  • NMDS: nonmetric multi-dimensional scaling

  • UHPLC-ESI-qTof-MS/MS: quadrupole time of flight – electro spray ionization – tandem mass spectrometry

  • PERMANOVA: permutational analysis of variance

  • VOCs: Volatile organic compounds

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