Hormonal Regulation Of Division Of Labor In Honey Bee Apis Mellifera L Colonies

Claire Detrain, Jean-Louis Deneubourg and Jacques Pasteels Studies on insects have been pioneering in major fields of modern biology. In the 1970 s, research on pheromonal communication in insects gave birth to the dis cipline of chemical ecology and provided a scientific frame to extend this approach to other animal groups. In the 1980 s, the theory of kin selection, which was initially formulated by Hamilton to explain the rise of eusociality in insects, exploded into a field of research on its own and found applications in the under standing of community structures including vertebrate ones. In the same manner, recent studies, which decipher the collective behaviour of insect societies, might be now setting the stage for the elucidation of information processing in animals. Classically, problem solving is assumed to rely on the knowledge of a central unit which must take decisions and collect all pertinent information. However, an alternative method is extensively used in nature: problems can be collectively solved through the behaviour of individuals, which interact with each other and with the environment. The management of information, which is a major issue of animal behaviour, is interesting to study in a social life context, as it raises addi tional questions about conflict-cooperation trade-oft's. Insect societies have proven particularly open to experimental analysis: one can easily assemble or disassemble them and place them in controllable situations in the laboratory.

Intraspecific communication involves the activation of chemoreceptors and subsequent activation of different central areas that coordinate the responses of the entire organism—ranging from behavioral modification to modulation of hormones release. Animals emit intraspecific chemical signals, often referred to as pheromones, to advertise their presence to members of the same species and to regulate interactions aimed at establishing and regulating social and reproductive bonds. In the last two decades, scientists have developed a greater understanding of the neural processing of these chemical signals. Neurobiology of Chemical Communication explores the role of the chemical senses in mediating intraspecific communication. Providing an up-to-date outline of the most recent advances in the field, it presents data from laboratory and wild species, ranging from invertebrates to vertebrates, from insects to humans. The book examines the structure, anatomy, electrophysiology, and molecular biology of pheromones. It discusses how chemical signals work on different mammalian and non-mammalian species and includes chapters on insects, Drosophila, honey bees, amphibians, mice, tigers, and cattle. It also explores the controversial topic of human pheromones. An essential reference for students and researchers in the field of pheromones, this is also an ideal resource for those working on behavioral phenotyping of animal models and persons interested in the biology/ecology of wild and domestic species.

Phenotypic plasticity 0́3 one genotype producing alternative phenotypes 0́3 is increasingly understood to be an important force in phenotypic evolution, but its mechanistic basis remains poorly understood. This thesis describes research into the molecular mechanisms underlying age-related behavioral and physiological plasticity in worker honey bees. Many animals are able to alter their behavior and physiology in response to changes in the environment. At times, these changes in behavior and physiology are stable for long periods, a phenomenon known as phenotypic plasticity [1]. For instance, short periods of food deprivation stimulate feeding and the mobilization of stored nutrients to meet an individual0́9s immediate energetic needs. But prolonged food deprivation can also lead to much longer-term effects, causing individuals to enter extended periods of inactivity, alter their reproductive strategy, or lose their position in a dominance hierarchy. In humans, chronic food deprivation early in life may lead to a propensity toward obesity and diabetes in later life (for an expanded and fully-referenced discussion of nutritionally-mediated phenotypic plasticity see Chapter 4). The mechanisms that enable and constrain plasticity in behavior and physiology are not well understood, but it is clear that they often involve coordinated and long-lasting changes in gene expression, brain circuitry, brain chemistry, and endocrine signaling [2]. My doctoral research has focused on understanding the molecular basis for nutritionally- and hormonally-mediated plasticity in the behavior and physiology of worker honey bees. Honey bees are social insects, living together in colonies containing tens of thousands of individuals [3]. Colony life is organized by a complex and sophisticated division of labor. Each colony contains a single queen, who is specialized for reproduction and spends most of her time laying eggs. Males, called drones, are relatively rare, and their sole role is to mate. The vast majority of the individuals in the hive are sterile worker bees that are responsible for all of the other tasks performed by the colony. The tasks performed by worker bees are further divided up among individuals via a process of behavioral maturation that is the focus of this thesis. For the first 2-3 weeks of adult life, worker bees specialize on broodcare (0́−nursing0́+). They then switch for a few days to any of a number of more specialized tasks such as building honeycomb cells, storing food in honeycomb cells, or guarding the hive entrance against intruders. Finally, for the remaining 1-2 weeks of their life, worker bees forage outside the hive for nectar and pollen, the colony0́9s sole sources of food. The work presented in this thesis builds on previous findings demonstrating links between worker honey bee division of labor and nutrition (reviewed in Chapter 4). Behavioral maturation in worker bees is coupled to changes in nutritional physiology, including a dramatic and stable loss of abdominal lipid that occurs prior to the onset of foraging. Moreover, previous studies had demonstrated that nutritional status can have causal influences on the timing of behavioral maturation and manipulations of a few feeding- or nutritionally-related genes accelerates or delays the age at onset of foraging. In the work described here, I first test the hypothesis that worker bee behavioral maturation, a highly derived trait, is regulated, in part, by conserved nutritionally-related hormones (Chapter 1). I demonstrate that genes related to insulin signaling are differentially expressed in the brains and fat bodies of nurses and foragers. Furthermore, I show that manipulation of the insulin-related TOR pathway influences the age at which bees initiate foraging. These results suggest that the evolution of honey bee social behavior involved new roles for ancient nutritionally-related pathways. However, my subsequent work shows that not all nutritionally-related pathways have been coopted in the same way. I describe a more complex, and less resolved, relationship between behavioral state, nutrition and brain gene expression for a second nutritionally-related hormone, Neuropeptide Y (Chapter 2). Next, using transcriptomic experiments, I demonstrate that maturation, as well as age-related stable lipid loss, involve massive changes in gene expression in the fat bodies (Chapter 3). I show that these changes in gene expression involve age-related changes in the responsiveness of hormonally and metabolically related pathways to nutrition, and roles for two evolutionarily novel, non-dietary factors: the storage protein vitellogenin and Queen Mandibular Pheromone, each of which influenced many maturationally-related genes in the fat bodies. These results also suggest the involvement in the responses to all these factors of a single nutritionally-related hormone, juvenile hormone (JH), which had previously been shown to pace behavioral maturation. In Chapter 4, I review my findings from chapters 1-2 of this thesis, and previous studies, and propose a molecular systems biology approach to understanding division of labor. Specifically, I propose that phenotypic plasticity in worker honey bees involves nutritionally- and hormonally-driven changes in transcriptional regulatory networks in the fat bodies (as well in the brain), and I suggest methodologies for their elucidation. Finally, in Chapter 5, I utilize the molecular systems biology approach outlined in Chapter 4 to show that a transcriptional regulatory network in the fat bodies underlies division of labor. I show that a juvenile hormone-related transcription factor, Ultraspiracle (USP), influences the age at onset of foraging. I then use a combination of chromatin immunoprecipitation0́4genomic tiling microarrays, RNAi and deep mRNA sequencing to develop a model of the USP transcriptional regulatory network in fat cells. My results suggest that JH and USP function together to induce and maintain alternative states of a transcriptional regulatory network. These alternative states may well underlie the two basic phases of worker bee life, the in-hive and foraging phases. Together, the studies presented in this thesis provide insights into the relationship between nutrition, hormones, transcriptional regulation, and phenotypic plasticity. References 1. West-Eberhard, MJ. Developmental Plasticity and Evolution. 2003. Oxford University Press, New York, NY. 794 pp. 2. Robinson, GE, Fernald, RD, Clayton, DF. Genes and social behavior. Science. 2008 Nov 7; 322(5903):896-900. doi:10.1126/science.1159277 3. Winston, ML. The Biology of the Honey Bee. 1987. Harvard University Press, Cambridge, MA. 294 pp.