Genomic basis of honey bee foraging behavior

Abstract

Honey bee workers, like those of most other social insects, change their behavior with age. Nevertheless, there are differences between individuals in an age cohort. The observed differences could be partly genetic, but also influenced by social factors such as interactions with other nest mates. Chemical signals play an important role in the communication of insect societies. Our data show that in honey bee colonies, the queen plays an important role by using her mandibular pheromone (QMP) to influence gene activity in workers (Chapter 1). The ability to perceive chemical signals with the antennae, and then process them in the brain, is responsible for variation in foraging strategies, as some workers follow the social signals of others (e.g., waggle dance), while others do not (Chapter 2). Finally, rewards may induce foragers to maintain a foraging strategy by influencing their motivation to engage in a particular behavior (Chapter 3). We have explored the genomic basis of foraging behavior in honey bees. While we know that many aspects of the colony environment influence worker behavior, the presence of the queen plays an important role in regulating the complex colony dynamics. Therefore, in Chapter 1, we investigated how exposure to the queen mandibular pheromone affects gene expression in different life stages of adult workers and how this affects later foraging. We found that there is a sensitive phase in early adulthood for responding to these queen signals that alters gene expression profiles but not foraging activity in foragers. The external environment plays an important role in regulating the behavior of honey bee workers. They may decide to forage at foraging sites advertised by their nestmates or seek out those they have stored in their memory. Previous studies have examined the various environmental factors that influence a forager to use either social or private information. The focus of Chapter 2 is to elucidate the molecular mechanisms underlying different information use strategies among foragers. We analyzed five tissues from the central and peripheral nervous systems: the antennae and in the brain: the antennal lobes, the mushroom bodies, the central brain, and the subesophageal ganglion. Surprisingly, we found no differences in gene expression in brain tissues between the two forager groups. However, we discovered that gene activity in the antennae was linked to foraging information use strategies. Our results suggest that honey bees do not rely on higher processing of cues in the central nervous system Summary 2 during foraging, but rather on differences in sensory perception to decide which foraging strategy to use. In Chapter 3, we wanted to further investigate whether the observed differences in gene expression patterns between foragers using different foraging strategies could be influenced by reward reinforcement. Differences in reward perception influence foraging and division of labor in honey bees. For example, regulation of pollen and nectar foraging in honey bees depends on reward perception. In turn, reward perception affects the use of memory in foraging by honey bees. We wanted to determine whether gene expression in the brain and antennae changes when foragers receive a reward for using a particular foraging strategy. We found that foragers that were consistently rewarded for using social or private information had a large number of differentially expressed genes, while the information use strategy itself had little effect on gene expression. Our results suggest that rewards elicit a strong gene expression signature in the brain, which increases the likelihood that a forager will use this foraging strategy again in the future. In summary, this dissertation expands our understanding of the role that colony dynamics, information use strategies, and reward perception, and the molecular and neurogenomic signatures underlying these processes, play in influencing honey bee foraging behavior. We show for the first time, a sensitive phase in adult worker behavioral development in which queen signals have a long-lasting effect on gene expression. We also show that differences in antennal sensory perception in foragers affect their information use strategies. Food rewards enhance the use of specific foraging strategies and alter gene expression in the antennae and brain. Taken together, our results reveal a high degree of plasticity in foraging behavior and its transcriptional basis. By using the honey bee as a model organism, which exhibits the highest complexity of sociality, we can deepen and extend evolutionary insights into social behavior.