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The evolution of bark beetle–fungus mutualisms : insights from a hardwood system Wertman, Debra Lindsay

Abstract

In mutualisms with bark beetles (Coleoptera: Curculionidae; Scolytinae), fungi benefit from dispersal to new habitats while granting their insect vectors access to resources via their phytopathogenic activities and supplementation of beetle nutrition. Alniphagus aspericollis, the alder bark beetle, is a bole-infesting beetle that kills red alder, Alnus rubra, a nitrogen-fixing hardwood native to the Pacific Coast of North America. Unlike most tree-killing bark beetles, the alder bark beetle is not regularly associated with ophiostomatoid fungi (Ophiostomatales and Microascales), but is instead associated with a previously undescribed species of Neonectria fungus (Hypocreales). I hypothesized that the alder bark beetle–Neonectria sp. nov. association represents a unique bark beetle–fungus mutualism that is similar to bark beetle–ophiostomatoid mutualisms in conifers. I first characterized the branch-overwintering component of the alder bark beetle life cycle, described Neonectria sp. nov. as Neonectria bordenii sp. nov., and developed a qPCR assay to enable detection of N. bordenii from alder bark beetle DNA. I then evaluated the following predictions, at five sites throughout southwestern British Columbia, Canada: (1) the alder bark beetle vectors N. bordenii; and (2) the beetle uses both an aggregation pheromone and N. bordenii to facilitate spatially-clustered mass-attacks on red alders. I tested prediction (1) according to Leach’s postulates, using qPCR and culturing methods to reveal that N. bordenii was present on emergent alder bark beetles at frequencies consistent with established bark beetle–fungus mutualisms, and that attacking beetles transmitted N. bordenii into red alders. To test prediction (2), I quantified patterns of host colonization by alder bark beetles in one-hectare plots, demonstrating spatial clustering of attacks on trees that supports the existence of an alder bark beetle aggregation pheromone. Previously attacked trees were more likely to be attacked and produced more offspring than previously unaffected trees, suggesting a mutualistic function of N. bordenii. Potentially high rates of alder bark beetle population increase were observed, raising concerns of widespread red alder decline. My research provides valuable insights into the evolution of bark beetle–fungus mutualisms by expanding upon known associations to include a hardwood-killing bark beetle and its unique putative mutualist.

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Attribution-NonCommercial-NoDerivatives 4.0 International