Aerial litter mimicry: a novel form of floral deception mediated by a monoterpene synthase

Floral mimics deceive their pollinators by developing visual and olfactory resemblance to their models. Our knowledge on the diversity of models is expanding rapidly. We report a system in which the flowers exhibit phenotypes similar to aerial litter and deceives an aerial litter specialist beetle to achieve pollination. We assessed the floral phenology and the effective pollinators of an Australian understorey treelet, Meiogyne heteropetala (Annonaceae). The similarities of morphology, colour and odour between the flowers and co-occurring aerial litter were investigated. The terpene synthase involved in floral scent emission was identified by expression patterns and product profile. The behavioural responses of the pollinator to various odours were assessed using bioassays. The erotylid beetle Loberus sharpi is the most likely effective pollinator of M. heteropetala , and its eggs were found on the petals of M. heteropetala . Loberus sharpi was exclusively found in aerial litter and M. heteropetala flowers. The morphology and spectral reflectance of the flowers overlap with aerial litter. The floral scent was dominated by monoterpenes, especially 1,8-cineole. The cineole synthase MhCINS was the only highly expressed floral terpene synthase and possessed a highly similar product profile to the floral scent composition. NMDS showed that the volatile composition of M. heteropetala flowers is distinct from other congeners and highly similar to aerial litter, indicating advergence to aerial litter. Visual and odour resemblance, coupled with the deposition of eggs on the flowers, provides evidence that the beetles were deceived into pollinating the flowers. Behavioural experiments showed that the pollinator was attracted to both aerial litter and M. heteropetala flowers. The beetles were also attracted to 1,8-cineole and synthetic mixes of floral odour and MhCINS products. The beetles were unable to distinguish floral scent from MhCINS products, nor from 1,8-cineole, suggesting MhCINS alone sufficed to attract the pollinator olfactorily. The beetles, however, preferred aerial litter over flowers. The beetles likely categorised the flower as a general, but not the most preferred brood substrate. Synthesis. This study reports the first case of floral mimicry of aerial litter and characterises the biochemical process responsible for olfactory mimicry.