Spiroacetals and the rise of Campanula specialists: Receptor sensitivity to host-specific floral scents

Campanula flowers (Campanulaceae) are visited by generalist and specialist bees of different families. While generalists rely on common volatiles within the floral scent of Campanula, specialist Megachilidae mainly use unusual spiroacetals for host flower recognition, usually reported only in insect communication. Although the evolution of specialization in Megachilidae and the underlying sensory adaptations have long been a topic of interest, the evolution of olfactory sensitivity of antennal receptors for spiroacetals has never been investigated before. In this study, we integrated electrophysiology and phylogenetics to evaluate the evolution of olfactory sensitivity to spiroacetals in Campanula specialist megachilids compared with other bees, including generalists and specialists foraging on flowers other than Campanula. We show that megachilid Campanula specialists are highly sensitive to spiroacetals and that these compounds can be sensed by most other Megachilidae and the generalist Andrena bicolor (Andrenidae). Further, our phylogenetic analyses suggest that the capacity to sense spiroacetals might be an ancestral trait in Megachilidae and the similarities in antennal sensitivity cannot be explained by phylogenetic relatedness alone. We conclude that the capacity to sense spiroacetals was an exaptation in Megachilidae, representing a condition prior to the evolution of Campanula specialists resulting from the role of spiroacetals in insect communication, while the high sensitivity in Campanula specialists has evolved later as a response to the low emission rates of these compounds in their host flowers. Read the free Plain Language Summary for this article on the Journal blog.