Inducible pine rosin defense mediates interactions between an invasive insect-fungal complex and newly acquired sympatric fungal associates.

Abstract

Mutualism between insects and fungi drives insect evolutionary diversification and niche expansion; for invasive insects, however, mechanisms by which they maintain mutualistic relationships with beneficial fungi have not been clearly explored. Here, we report that an invasive herbivorous insect, the red turpentine beetle (RTB), with its co-invasive mutualistic fungus, Leptographium procerum, has newly acquired a set of sympatric fungi during invasion, which could potentially outcompete the RTB mutualistic fungus. Host pine Pinus tabuliformis exhibited more rosin-based responses to the sympatric fungi than to RTB mutualistic fungus and, in return, the rapidly induced rosin suppressed the sympatric fungi more significantly than L. procerum. In addition, from direct fungal pairing competitions, we found that the antagonistic effects of sympatric fungi on L. procerum were drastically reduced under induced rosin defense. Our results together with previous findings imply that pine oleoresin defense (turpentine and rosin) might have been exploited by the invasive mutualistic fungus L. procerum, which helps to explain its invasion success and, by extension, its mutualistic partner RTB in China.