Divergent Response of Two Bark Beetle–Fungal Symbiotic Systems to Host Monoterpenes Reflects Niche Partitioning Strategies

The successful establishment of bark beetle–fungus symbionts on plants is required to overcome host defenses. However, little is known about how different bark beetle–fungus symbionts adapt to different niches on the same host plant. Here, we investigated the niche partitioning mechanism of two co-occurring bark beetle–fungus symbiotic systems, Ips nitidus–Ophiostoma bicolor and Dendroctonus micans–Endoconidiophora laricicola, on Qinghai spruce (Picea crassifolia) tree. The lower niche of the spruce trunk inhabited by D. micans showed a higher content of monoterpenes than the upper niche of the trunk inhabited by I. nitidus. Dendroctonus micans showed greater tolerance and higher metabolic efficiency toward monoterpenes than I. nitidus. However, both beetle species showed a similar metabolic profile toward α-pinene, albeit with different levels of metabolites. Additionally, O. bicolor, transmitted by I. nitidus, showed a significantly higher tolerance to monoterpenes and pathogenicity to spruce trees than E. laricicola, transmitted by D. micans. In particular, monoterpenoid metabolites were observed to attenuate the inhibitory effect of high-dose α-pinene on E. laricicola, thus increasing its fitness in a high-dose monoterpene microhabitat. These results show that these two bark beetle–fungus symbionts have adapted to different niches, leading to fitness differences in niche distribution that are at least partly related to the different distribution of monoterpene concentration in the spruce trunk. This research provides a novel perspective for understanding the coevolution between bark beetle–fungus symbionts and their host plants.