Home | Robinson Lab

The Robinson lab uses the Western honey bee, Apis mellifera, to understand the mechanisms and evolution of social behavior. Among the species of animals most attuned to their social environment are the social insects, which include the honey bee. They live in societies that rival our own in complexity and internal cohesion.

Social insects are "eusocial,” which is the most extreme form of animal social life on the planet. Bees and other eusocial insects (like ants, termites, and wasps) live in colonies with overlapping generations, cooperative brood care, and a reproductive division of labor. The queen reproduces, while the workers perform tasks related to colony growth and development and engage in little, if any, reproduction themselves.

Advanced eusocial species such as honey bees have the largest colonies, numbering tens or even hundreds of thousands of workers. They also live in the most complex societies, highlighted by an intricate division of labor among workers. It is this division of labor that has made possible the evolution of collective traits normally associated with human society: agriculture, warfare, and symbolic language.

Social insects are "extremists" in their constant expression of social behavior. They coordinate virtually all of their activities with other individuals to ensure colony survival. Like all other animals, bees must obtain and process information about their changing ecological and social milieu and act accordingly. But for species with active social lives, neural and behavioral plasticity is even more contingent upon social context. In social evolution, the sophistication of behavioral mechanisms for the essentials of life--food, shelter, and reproduction--stems from increased abilities to communicate and synchronize behavior with conspecifics. Social insects, especially honey bees, are exemplars for the discovery of general principles of brain function, behavior, and social organization.

Owing to its special status as a producer of honey and as the premier animal pollinator, the honey bee has been closely associated with humans for millennia. As a result, we know more about honey bee natural behavior than any other species on the planet besides ourselves! One consequence of this wealth of knowledge is that the natural social life of the honey bee, though as complex as in any vertebrate society, can be extensively manipulated with unparalleled precision.

Our goal is to explain how honey bee society evolved and operates, using an interdisciplinary approach that integrates evolutionary biology, behavioral biology, neuroscience, endocrinology, molecular biology, genetics, and genomics. We seek to understand the function and evolution of behavioral and pheromonal mechanisms that integrate the activity of individuals in a society, the neurochemical, neuroanatomical, and neuroendocrine mechanisms that regulate behavior within the brain of the individual, the genes that influence social behavior, and the means by which inherited variation and the environment act on the genome to orchestrate behavior and shape individual differences in behavior. To achieve these goals we couple the interdisciplinary approach outlined above with both naturalistic behavioral research in the field and behavioral assays in the laboratory.

We often study the most fundamental social behavior system in honey bee society, the division of labor among worker bees. This is based on the behavioral development of the individual worker bee. Behavioral development occurs in many animals, including humans. As animals age and pass through different life stages, their behavioral responses to environmental and social stimuli change in predictable ways. Often these responses increase in complexity and involve learning. With just a 4-7 week adult lifespan, worker honey bees display a rich, vertebrate-like pattern of behavioral development, which underlies age-related division of labor in the colony. This behavioral development is regulated by changes in brain structure, brain chemistry, and circulating hormones, which themselves are regulated by massive changes in the expression of genes in the brain. The coordination of these changes in gene expression by transcription factors and epigenetic factors are only beginning to be understood, and represent compelling questions for future study.

The Robinson lab also investigates other behaviors using the same integrative approaches, including dance language, colony defense, social networks, reproductive behavior, and how social experience affects the expression of these and other behaviors. Members of our lab often develop new tools to facilitate this research, such as automated methods to track bee behavior with RFID or barcode tags and automated methods of rearing bees in the laboratory.

Especially in the current social and political climate, we are mindful of the broader societal issues related to understanding the relationship between genes and behavior. We strive to show how our work illustrates that the relationship between genes and behavior is dynamic and environmentally responsive, rather than purely deterministic. Our comparative genomics research, conducted within the Gene Networks and Neural Plasticity (GNDP) Research Theme at the Carl R. Woese Institute for Genomic Biology (IGB), also has revealed that this conclusion holds for humans as well as bees.

The following sections provide brief descriptions of some of our past and present research, to give a flavor of our research program.

Chemical Communication

Bees show very structured behavioral development, but they also show a lot of flexibility. They speed up, slow down, or even reversing their trajectories in response to the needs of their colony. How do they do it? Our research on this topic, much of it conducted in collaboration with the lab of Dr. Yves LeConte in France, demonstrated that how fast a bee grows up and becomes a forager is regulated with exquisite complexity, and it depends greatly on chemical communication. We have identified several pheromones that are involved, including a pheromone we discovered produced by older bees that inhibits behavioral development in younger bees. Genomic analyses have revealed that these pheromones work by regulating the expression of genes in the brain that are associated with behavioral development.

Brain Plasticity

How does a bee's brain support the striking changes in behavior that take place during maturation? One part of the answer lies in the mushroom bodies, a brain region that is the center of learning and memory in insects. Together with the laboratory of Prof. Susan Fahrbach, formerly at Illinois and now at Wake Forest University, we discovered about a 20% increase in the volume of a specific area of the mushroom bodies as worker bees mature. This volume increase occurs in a mushroom-body subregion where synapses (connections) are made between neurons from other brain regions that are devoted to sensory input. At the time this was the first report of such brain plasticity in an invertebrate! It was particularly exciting because volume increases in brain regions in vertebrates reflect increases in certain cognitive abilities. The increase in the mushroom bodies might be learning-related.

Molecular Basis of Honey Bee Dance Language

The honey bee is the only non-mammal to have a symbolic language; honey bee dance language shatters our perception of what an insect brain can accomplish and provides a great challenge to discovering how a small brain can generate complex behavior. We have used neuroanatomical, neurochemical and new genomic tools developed in our laboratory to help in this quest. One early breakthrough was the discovery that cocaine, acting on endogenous brain reward pathways, makes bees dance more!

Molecular Signatures of Social Evolution in Bees

Social insects live in extraordinarily complex and cohesive societies, where many individuals sacrifice their personal reproduction to become helpers in the colony. Identifying adaptive molecular changes involved in eusocial evolution in insects is important for understanding the mechanisms underlying transitions from solitary to social living, and the maintenance and elaboration of social life. We have developed large-scale genomic resources to address these issues, in wasps and bees. These resources include brain transcriptomes and whole genomes. Drawing from whole genome comparisons, candidate gene approaches, and a genome-scale, comparative analysis of protein-coding sequence, we have made novel discoveries related to several major biological processes, including chemical signaling, brain development and function, reproduction, and metabolism and nutrition. Working with a large international research team we sequenced and analyzed genomes for 10 bee species that show different levels of sociality, and found evidence that gene regulatory networks have become more complex during social evolution.

Neurons for Today, Genes for Tomorrow

As for all types of environmental stimuli, important social information is perceived, encoded, and then processed in the nervous system to initiate adaptive behavior. This involves “biological embedding,” the process by which social experience affects the brain to influence future behavior. For example, we have shown that colony defense involves instantaneous behavioral responses to intruders, but then also is associated with distinct waves of gene expression in key regions of the honey bee brain that are exhibited hours later. How do these changes in gene expression relate to colony defense? As described in a recent Annual Review of Neuroscience chapter written by Traniello and Robinson, we hypothesized that social stimuli provoke short-term changes in neural activity that lead to changes in gene expression on longer timescales. This process enables experience to modify future behavior in anticipation of environmental changes. Tests of this model are ongoing, including explorations of early life deprivation on brain and behavior.

Behavioral Gene Regulatory Networks: A New Level of Organization in the Brain

While exploring the molecular basis of division of labor in honey bees, we discovered over 20 years ago in one of the very first behavioral transcriptomic experiments that changes in the social environment exert massive effects on brain gene expression. This discovery enabled us to show how networks of co-regulated genes in the brain are altered (“rewired”) by social behavior, mediated by a particular set of transcription factors. These findings suggest that understanding how genes influence behavior can be achieved through a framework that integrates behaviorally related gene regulatory networks (GRNs). along with GRNs related to brain development.

Announcements

Items of Interest

The Robinson lab expects that all lab members will be engaged, hardworking, and respectful of everyone else in the lab. We strive to create a laboratory environment where people of different race, ethnicity, sexuality, gender identity, ability, and religious backgrounds feel comfortable and succeed. Prospective lab members can request to read our document of expectations, guidelines, and policies.

Research Areas: From Society to Genes