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Robinson Lab
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 * Publications
 * Lab Members
 * Useful Links
 * Cover Stories


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RESEARCH AREAS: FROM SOCIETY TO GENES

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

 * Robinson and colleagues launch Earth BioGenome Project, to sequence the
   genomes of all species on the planet
 * Research provides genetic links between socially unresponsive honey bees and
   human autism
 * Barcoded bees reveal surprising properties of honey bee social network
 * Genomic analyses reveal that the rapid evolution of gentle Africanized honey
   bees in Puerto Rico involved a novel "soft selective sweep."
 * Robinson and Barron publish thought piece on epigenetics and the evolution of
   instincts.
 * Lab Alum Chelsey Coombs writes for The Atlantic!
 * IGB renamed Carl R. Woese Institute of Genomic Biology, says Director
   Robinson
 * Honey bees help uncover genetic toolkits for social behavior
 * No glass ceiling for worker bees in the hive
 * Robinson gives Congressional Testimony on Value of Brain and Behavior
   Research
 * Robinson lab's discovery of the "sociable genome" profiled in Pacific
   Standard
 * Robinson and Amro Zayed describe first principles of the relationship between
   genes and social behavior
 * Robinson interviewed on BBC about lab's bee personality research
 * Cover Stories Section!
 * Robinson publishes New York Times Op-Ed piece on genes and behavior
 * Cocaine Makes Bees Dance More
 * Cocaine Research Reported on Colbert Report
 * Robinson describes an idea for how neurons and genes work together to
   regulate behavior in The Conversation
 * Farahany and Robinson publish Washington Post Op-Ed piece on the rise and
   fall of the Warrior Gene defense 

 

 


ITEMS OF INTEREST

 * Genomics used to understand the roots of instincts
 * Study of bees links gene regulatory networks in the brain to behavior
 * University of Illinois Bees and Beekeeping Short Course -- next offered in
   2020
 * Robinson Lab part of interdisciplinary research theme at Carl R. Woese
   Institute for Genomic Biology
 * Honey Bee Genome Project
 * Hymenoptera Genome Database: Home of the honey bee genome
 * Genome on a Tree: Powerful new database and computational platform for
   comparative genomics
 * Robinson and colleagues launch i5K: an initiative to sequence the genomes of
   5000 insects and other arthropods
 * Brains of scout bees wired for adventure
 * Nature Outlook: Bee Instincts
 * Nature Outlook: Bee History

 

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.




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