Bark beetles locate fungal symbionts by detecting volatile fungal metabolites of host tree resin monoterpenes

Abstract

AbstractOutbreaks of bark beetles have decimated millions of hectares of conifer forest worldwide in recent years. The ability of these tiny 3-6 mm long insects to kill mature trees over a short period has been ascribed to two factors: (1) mass attacks on the host tree to overcome tree defenses and (2) the presence of fungal symbionts that support successful beetle development in the tree. While the role of pheromones in coordinating mass attacks has been well studied, the role of chemical communication in maintaining the fungal symbiosis is poorly understood. We previously demonstrated that Eurasian spruce bark beetles (Ips typographus) can recognize beneficial fungal symbionts of the genera Grosmannia, Endoconidiophora and Ophiostoma by their de novo synthesized volatile compounds. We hypothesized that the fungal symbionts of the bark beetles might metabolize spruce resin monoterpenes of the beetle’s host tree, Norway spruce (Picea abies), and that the volatile products could be used as cues by beetles for locating breeding sites with beneficial symbionts. Grosmannia penicillata and other fungal symbionts altered the profile of spruce bark volatiles by converting the major monoterpenes to oxygenated derivatives. Bornyl acetate was metabolized to camphor, and α- and β-pinene to trans-4-thujanol and other oxygenated products. Extensive electrophysiological measurements showed that bark beetles possess olfactory sensory neurons that are selective for these oxygenated symbiont metabolites. Compounds such as camphor and trans-4-thujanol attracted beetles at specific doses in olfactory experiments and stimulated the response of female beetles to a mixture of pheromones. Finally, the fungal symbiont was found to stimulate bark beetle tunneling on diets. Collectively, our results show that oxygenated metabolites of conifer monoterpenes produced by fungal symbionts are used by bark beetles as cues to find these essential microbial symbionts. The oxygenated metabolites may aid beetles in assessing the presence of the fungus, the defense status of the host tree and the density of conspecifics at potential feeding and breeding sites.