Climatic stress reshapes sex-specific multimodal floral phenotypes and interactions with a nursery pollinator across life stages

Abstract

Background: Nursery pollination combines mutualistic and antagonistic interactions between plants and insects: adult insects provide pollination services, while their larvae consume plant reproductive tissues. Climatic stress may alter the benefits and costs for both partners by modifying plant phenotypes and their consequences for pollinator behaviour and offspring performance. These dynamics gain an additional layer of complexity in systems where both plants and insects have separate sexes, giving rise to sex-specific interactions and potentially divergent stress responses. Yet how climatic stress affects these specialized interactions remains unexplored. Methods: We addressed this gap in a nursery pollination system comprising the dioecious plant Silene latifolia and the moth Hadena bicruris. We exposed female and male plants from five populations to water limitation, assessing visual floral traits, scent, nectar chemistry and moth behaviour alongside seed production, seed chemistry, larval consumption and performance. Results: We identified previously unexplored chemical trait spaces potentially mediating mutualistic and antagonistic components of the interaction, encompassing nectar rewards and larval seed resources. Water limitation altered floral and seed phenotypes, with pronounced reductions in nectar metabolites in male plants eroding sexual dimorphism in nectar chemistry. This was accompanied by a loss of moth preference for ovipositing on female flowers, while oviposition declined overall under water limitation and feeding behaviour remained unaffected. Meanwhile, water limitation reduced several defence-associated seed metabolites, and larvae grew faster on seeds from water-limited plants despite consuming similar amounts of seeds. Synthesis: Against the broader backdrop of specialist species loss and shifts towards more generalized interaction networks under global change, our study provides the first comprehensive assessment of climatic stress effects on a nursery pollination system. By revealing opposing effects on adult oviposition and offspring performance, our findings highlight how climatic stress may redistribute benefits and costs within specialized species interactions through changes in multidimensional plant phenotypes and interconnected mutualistic and antagonistic processes.