Deceptive Aristolochia Trap-Flowers Pollinated by Male Phorid Flies Mimic Volatiles Specific to Female Phorids

Abstract Background and Aims Floral mimicry is a form of deceptive pollination in which flowers or inflorescences imitate specific resources relevant to potential flower visitors, such as food, brood sites, or mating partners (sexual mimicry). A plant genus containing many unstudied species with potentially highly diverse deceptive systems is fly-pollinated Aristolochia (Aristolochiaceae), famous for its trap flowers. A few species with strongly male-biased pollinator assemblages have been suggested to mimic the female sex pheromones of flies. However, so far, neither the floral scents nor the female sex pheromones of the fly species involved are known. Methods In this study on the Mediterranean Aristolochia lutea and A. paucinervis, we identified male-biased pollinator assemblages, analyzed the floral scents and female-specific fly volatiles by gas chromatography/mass spectrometry (GC/MS) and (enantioselective) synthetic chemistry, and performed field bioassays with synthetic floral scents to characterize these pollination systems. Key Results We found that the two Aristolochia species were pollinated by different assemblages of exclusively or primarily male phorid species (mostly Megaselia). The floral scents of both Aristolochia species were dominated by a small, largely overlapping set of structurally related short-chain, methyl-branched aliphatic alcohols and ketones, several of which we also identified as female-specific compounds in phorids (e.g., 4-methyl-2-pentanone, (E)-3-methyl-3-penten-2-one, 5-methyl-3-hexanone). In field bioassays, synthetic floral scent resembling A. lutea attracted males of two pollinator species of A. lutea (Megaselia giraudii, M. pleuralis) and the main pollinator of A. paucinervis (M. pumila). A mixture resembling A. paucinervis attracted also a pollinator of A. lutea (M. giraudii). No female phorids were attracted in these assays. Conclusions Both Aristolochia species mimic female-specific volatiles to deceive male phorid pollinators. Future studies must test whether the compounds involved function as female sex pheromones of the pollinating flies. If confirmed, this would be the first case of sex pheromone mimicry outside of orchids.