Multitrophic interaction facilitates parasite–host relationship between an invasive beetle and the honey bee

Colony defense by honey bees, Apis mellifera, is associated with stinging and mass attack, fueled by the release of alarm pheromones. Thus, alarm pheromones are critically important to survival of honey bee colonies. Here we report that in the parasitic relationship between the European honey bee and the small hive beetle, Aethina tumida, the honey bee's alarm pheromones serve a negative function because they are potent attractants for the beetle. Furthermore, we discovered that the beetles from both Africa and the United States vector a strain of Kodamaea ohmeri yeast, which produces these same honey bee alarm pheromones when grown on pollen in hives. The beetle is not a pest of African honey bees because African bees have evolved effective methods to mitigate beetle infestation. However, European honey bees, faced with disease and pest management stresses different from those experienced by African bees, are unable to effectively inhibit beetle infestation. Therefore, the environment of the European honey bee colony provides optimal conditions to promote the unique bee-beetle-yeast-pollen multitrophic interaction that facilitates effective infestation of hives at the expense of the European honey bee.