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

• Published in: The ISME Journal Vol. 13; no. 6; pp. 1535 - 1545
• Main Authors: Zhao, Tao, Ganji, Suresh, Schiebe, Christian, Bohman, Björn, Weinstein, Philip, Krokene, Paal, Borg-Karlson, Anna-Karin, Unelius, C. Rikard
• Format: Journal Article
• Language: English
• Published: London Nature Publishing Group UK 01.06.2019; Nature Publishing Group
• Subjects: 101/58; 631/158/2454; 631/326/193/2539; 631/45/320; Animals; Bark; Beetles; Biological Evolution; Biomedical and Life Sciences; Blue stain; Bridged Bicyclo Compounds, Heterocyclic - metabolism; Child custody; Coleoptera; Coleoptera - growth & development; Coleoptera - microbiology; Coleoptera - physiology; Coniferous forests; Convergence; Disruption; Ecological chemistry; Ecology; Ekologisk kemi; Evolution; Evolutionary Biology; Fungi; Fungi - classification; Fungi - genetics; Fungi - isolation & purification; Fungi - physiology; Gas chromatography; Glucose; Life Sciences; Malt; Mass spectrometry; Mass spectroscopy; Microbial Ecology; Microbial Genetics and Genomics; Microbiology; Pest control; Pheromones; Pheromones - chemistry; Pheromones - metabolism; Picea - microbiology; Picea - parasitology; Pine trees; Plant Bark - microbiology; Plant Bark - parasitology; Plantations; Semiochemicals; Symbionts; Symbiosis; Trees - microbiology; Trees - parasitology
• ISSN: 1751-7362; 1751-7370; 1751-7370
• DOI: 10.1038/s41396-019-0370-7

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 13 C d -Glucose, the fungus Grosmannia europhioides incorporated 13 C 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.