Convergent evolution of semiochemicals across Kingdoms: bark beetles and their fungal symbionts

Tao Zhao,Christian Schiebe,Suresh Ganji,Anna-Karin Borg-Karlson,Philip Weinstein,Paal Krokene,C Rikard Unelius,Björn Bohman

doi:10.1038/s41396-019-0370-7

Abstract

Convergent evolution of semiochemical use in organisms from different Kingdoms is a rarely described phenomenon. Tree-killing bark beetles vector numerous symbiotic blue-stain fungi that help the beetles colonize healthy trees. Here we show for the first time that some of these fungi are able to biosynthesize bicyclic ketals that are pheromones and other semiochemicals of bark beetles. Volatile emissions of five common bark beetle symbionts were investigated by gas chromatography-mass spectrometry. When grown on fresh Norway spruce bark the fungi emitted three well-known bark beetle aggregation pheromones and semiochemicals (exo-brevicomin, endo-brevicomin and trans-conophthorin) and two structurally related semiochemical candidates (exo-1,3-dimethyl-2,9-dioxabicyclo[3.3.1]nonane and endo-1,3-dimethyl-2,9-dioxabicyclo[3.3.1]nonane) that elicited electroantennogram responses in the spruce bark beetle Ips typographus. When grown on malt agar with 13C d-Glucose, the fungus Grosmannia europhioides incorporated 13C into exo-brevicomin and trans-conophthorin. The enantiomeric compositions of the fungus-produced ketals closely matched those previously reported from bark beetles. The production of structurally complex bark beetle pheromones by symbiotic fungi indicates cross-kingdom convergent evolution of signal use in this system. This signaling is susceptible to disruption, providing potential new targets for pest control in conifer forests and plantations.

Highlights

Symbiotic interactions between insects and microorganisms are widespread in nature
We investigated the production of bicyclic ketals by five common fungal symbionts of European bark beetles: Endoconidiophora polonica, Grosmannia europhioides, G. penicillata, Ophiostoma bicolor, and O. piceae
To determine if blue-stain fungi could produce bicyclic ketals while growing on fresh Norway spruce bark we analyzed volatile emissions from five common fungi associated with bark beetles: Endoconidiophora polonica, Grosmannia europhioides, G. penicillata, Ophiostoma bicolor, and O. piceae

Summary

Introduction

Symbiotic interactions between insects and microorganisms are widespread in nature. There is growing evidence that microbial symbionts play instrumental roles in animal ecology [1,2,3] and many of these roles are potentially mediated by microbe-produced chemical signals [4]. A potential explanation for these specific insectmicrobe associations can involve the convergent synthesis of chemical communication signals (semiochemicals) across Kingdoms [11, 12]. The key to the beetles’ ability to kill trees seems to be their complex chemical communication system and symbiotic relationship with phytopathogenic blue-stain fungi [13, 14]. The symbiotic relationship is obligate in so far as the fungi depend on the beetle for their own dispersal [19]. It would be adaptive, for the fungi and the beetle to use mutually intelligible signaling systems, despite belonging to different biological Kingdoms

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