Mechanisms of Nestmate Recognition Cue Production in the European Honey Bee, Apis mellifera.

Social insects are some of the world’s most ecologically successful animal groups, and their complex societies are considered one of the pinnacles of animal evolution. Since these organisms live in colonies composed of many individuals and stored resources, they are a target for intruders, such as parasites, predators and conspecific robbers. Therefore, many social insect species have evolved mechanisms for nest defense, including nestmate recognition, where guarding individuals at the entrance of the colony use cues on incoming individuals to determine whether they are nestmates or intruders. Although nestmate recognition is incredibly important for maintaining colony integrity and fitness, the behavioral and physiological mechanisms that underlie this behavior remain unknown for most species. My dissertation work focused on elucidating the mechanisms of colony-specific nestmate recognition cue production in the economically important honey bee. Previously, it was assumed that the colony-specific chemical signatures used for nestmate recognition are acquired by individual workers through the homogenization of cuticular chemicals, called cuticular hydrocarbons (CHCs), via interactions with other colony members or hive materials. Although this mechanism seems to be used by few ant species, my dissertation work shows that in honey bee colonies, the CHC profiles of workers develop through a sequence of stereotypic qualitative and quantitative chemical transitions driven by environmentally-sensitive biosynthetic pathways, which result in the final mature colony-specific nestmate recognition cue in forager bees, independent of their genetic background (Chapter 2). These data suggest that, rather than acquiring cues via CHC homogenization mechanisms, honey bees intrinsically produce colony specific CHC profiles via environmentally-sensitive mechanisms. To further understand how hive-specific environmental factors might define the colony-level specificity of the nestmate recognition cue, independent of the bee’s genetics, I subsequently show that colony-specific gut microbial communities contribute to the development and perception of nestmate recognition cues in honey bee colonies (Chapter 3). My work highlights the link between gut microbial community and cue production in honey bees, but also remarkably suggests a link between gut microbial community and cue perception, implying a pleiotropic role of the gut microbiome in this recognition behavior. Overall, my dissertation work supports the model that colony-specific gut microbial communities drive the intrinsic production of colony-specific nestmate recognition cues across foragers of the same colony, as well as the ability to identify colony-specific cues in guard bees