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From Society to Genes with the Honey Bee: A combination of environmental, genetic,hormonal and neurobiological factors determine a bee's progression through a series of lifestagesAuthor(s): Gene E. RobinsonReviewed work(s):Source: American Scientist, Vol. 86, No. 5 (SEPTEMBER-OCTOBER 1998), pp. 456-462Published by: Sigma Xi, The Scientific Research SocietyStable URL: http://www.jstor.org/stable/27857099 .Accessed: 21/08/2012 14:40

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From Society to Genes with the Honey Bee

A combination of'environmental, genetic, hormonal and neurobiological factors determine a bees progression through a series of life stages

Gene E. Robinson

On September 9, 1997, an article in

The New York Times announced the

discovery of the "first gene for social be havior." Anthony Wynshaw-Boris, of the National Human Genome Research In

stitute, and his colleagues had discov ered odd behavior in laboratory mice

lacking a gene called disheveled-1. These mice interacted and huddled with oth ers less than normal, and they failed to

perform an important social duty, trim

ming the whiskers of fellow mice. Whether or not this is really the first gene discovered "for social behavior," no one should lean toward the notion that genes play an exclusive role in regulating be havior. Biologists long ago came to real ize that behavior is influenced by genes, the environment and interactions be tween the two. To better understand this

regulatory combination, scientists can turn to an organism, such as the honey bee, whose behavior can be studied in the field under natural conditions.

A discussion of "genes for behavior"

might raise anxiety over the implications of attributing so much control to strings of nucleic acids, or DNA. In particular, some people fear that the concept of bio

logical determinism?the notion that

genes play a dominant, if not exclusive, role in regulating behavior?might creep in and diminish our appreciation for the role of the environment in shap ing behavior. Nevertheless, genes never

Gene E. Robinson is professor in the Department of

Entomology and the Neuroscience Program at the

University of Illinois at Urbana-Champaign. He

earned his B.S. in 1977 at Cornell University, worked in the bee industry until 1980, and then

earned his M.S. and Ph.D. at Cornell in 1982 and

1986, respectively. His research employs honey bees

for interdisciplinary studies of mechanisms of social

behavior. Address: Department of Entomology,

University of Illinois, Urbana, IL 61801.

act alone. They must operate in an envi

ronment, where they code for proteins that participate in many systems in an

organism. In fact, genes themselves de

pend on many of those proteins for

replicating DNA and linking together amino acids, which are the fundamental units of proteins. Consequently, biolo

gists need to take a broad approach in

assessing the impact of any gene. To properly appreciate the influence

of genes on behavior, we need behav ioral studies that demonstrate?at the

molecular level?the influences of

genes, the environment and their inter actions. Social behavior is ideally suited for this challenge because it is especially sensitive to environmental influence.

Moreover, these influences are in many cases mediated by specific social signals communicated from individual to indi

vidual, which can make them easier to

study experimentally. Molecular-genet ic studies of social behavior will show how an animal's phenotype, which in cludes social behavior, arises from both its genotype and environment. Making that connection, however, requires iden

tifying genes that influence social behav ior, revealing how those genes regulate the neural and endocrine mechanisms

through the production of proteins, and,

finally, exploring how specific manipu lations of an animal's social environment affect gene expression.

My research group uses the Western

honey bee, Apis mellifera, to understand how genes and the environment gov ern social behavior. As I shall show, we

study the development of naturally oc

curring social behavior, from society to

gene. Honey bees are particularly use ful for studying social behavior be cause, like humans, they experience be havioral development. In other words,

honey bees pass through different life

stages as they age, and their genetically determined behavioral responses to en vironmental and social stimuli change in predictable ways. Often these re

sponses increase in complexity and in volve learning. We hope to explain the function and evolution of behavioral

mechanisms that integrate the activity of individuals in a society, neural and neuroendocrine mechanisms that regu late behavior within the brain of an in

dividual, and genes that influence be havior by encoding these mechanisms.

Basics of Bee Behavior The so-called social insects, including honey bees, live in societies that rival our own in complexity and internal co hesion. For instance, honey bees al

ways follow three rules: They live in colonies with overlapping generations, they care cooperatively for offspring other than their own and they main tain a reproductive division of labor. A

colony arises from a queen that per forms one task, laying lots of eggs, sometimes as many as 2,000 in one day. Her daughters, called workers, basically take care of the colony?doing every thing from foraging for food to build

ing the hive?but they generally do not

reproduce. As one might expect, it takes many workers to run a hive, and some honey bee colonies consist of as

many as 60,000 workers. Finally, a col

ony's males, called drones, can usually be found in the hive, where they do es

sentially nothing. The drones special ize in reproduction, which takes just a

couple of hours on a sunny day when

they fly to mating areas away from the hive. Once a drone mates, he dies.

A further division of labor exists

among the workers. Although a work er's adult life span is just four to seven

weeks, it undergoes a series of transitions.

456 American Scientist, Volume 86

Kenneth Lorenzen

Figure 1. Honey bees pass through different life stages as they age, and their behavioral responses to environmental and social stimuli

change in predictable ways. For instance, older females forage for food, as shown by this bee collecting pollen from a passion flower. By

studying a honey bee's naturally occurring social behavior, from society to gene, the author hopes to explain the function and evolution of

behavioral mechanisms that integrate the activity of individuals in a society, of neural and neuroendocrine mechanisms that regulate behav

ior within the brain of an individual and of genes that influence this social behavior.

A worker usually spends its first few weeks tending to duties in the hive and its last few weeks foraging for food out side the hive. During the hive phase, a worker starts out with a couple of days of cell cleaning, literally removing debris from cells in the hive that are used to raise other bees or to store food. Next, a work er serves as a nurse, caring for and feed

ing larval bees. Toward the end of the hive phase, a worker spends its time pro cessing and storing food and maintain

ing the nest, including building new sec tions of hive. Some workers also perform a few other tasks along the way, includ

ing guarding the hive or removing corpses. Finally, a worker switches to for

aging, which is probably the most chal

lenging task of all. To be a successful for

ager, a bee must learn how to navigate in the environment and obtain nectar and

pollen from flowers. Foragers also com municate the location of new food sources by means of the famous "dance

language." These transitions in occupa tion typically do not arise abruptly For

example, a worker might slowly decrease its nursing duties and become gradually

more involved in maintaining the hive. Behavioral development in honey bees

is a powerful system for integrated analy sis. Although it occurs naturally in the

field, some underlying mechanisms can be analyzed in the laboratory. Moreover,

honey bees have been closely associated with humans for millennia because of their special status as prolific producers of

honey and wax and as premier pollina

tors for our food and fiber crops. As a re

sult, we know more about honey bees than just about any other animal on earth.

One consequence of this wealth of

knowledge is that the natural social life of

honey bees can be extensively manipu lated with unparalleled precision.

Colony Adjustments Although worker bees go through a rather consistent path of behavioral de

velopment, it is not rigidly determined. Bees can accelerate, retard or even re

verse their behavioral development in

response to changing environmental and colony conditions. For example, fa vorable environmental conditions in the late spring might cause a surge in

worker birth rates, and that could re

1998 September-October 457

Figure 2. Worker bees, daughters of the queen, go through a series of transitions in their

month-or-two-long lives. A worker bee starts as a hive cleaner and then advances to nursing larval bees (top). Next, a worker helps with maintaining a hive, including building new sec

tions (middle). Finally, the oldest workers forage for food (bottom).

suit in a colony with a reduced percent age of foragers. Under these circum stances, young bees compress their pe riod of hive work from three weeks to one week and become "precocious for

agers." Conversely, a new colony

founded by a swarm?a fragment of an old colony that leaves to establish a new colony?soon reaches a point at which it contains predominantly older individuals. In that case, some colony

members retard their development and serve as overaged

nurses. In those bees,

hypopharyngeal glands that produce food for larvae continue with this function rather than producing other substances.

How does the behavior of thousands of individual bees generate a smoothly functioning colony? It seems unlikely that individual bees could monitor the state of their entire colony and then

perform the tasks that are needed. Al

though some workers play special roles in organizing specific tasks, such as

leading other bees to a new nest site

during swarming, there is no evidence for real leaders or individuals?not even the queen?that perceive all or most of a colony's requirements and di rect the activities of other colony mem bers from one task to another. The chal

lenge is understanding the mechanisms of integration that enable individual bees to respond to fragmentary infor mation with actions that are appropri ate to the state of the whole colony.

My colleagues and I and others have discovered that juvenile hormone?one of the most important hormones influ

encing insect development?helps to time the pace of behavioral maturation in honey bees. This hormone comes from the corpora aliata, a gland that lies near a honey bee's brain. Indirect evi dence for this hormone's role exists in the fact that young bees working in a hive have low levels of this hormone and older foragers have higher levels. Direct proof has also been obtained:

Young bees given juvenile-hormone treatments become precocious foragers. Recently, my University of Illinois col

league Susan Fahrbach, graduate stu dent Joseph Sullivan, undergraduate Omar Jassim and I found that remov

ing the corpora allata does not prevent a bee from developing into a forager but does delay it for a few days on av

erage. Juvenile-hormone treatments,

however, eliminate that delay. Manipulating hormone levels on a

bee-by-bee basis is one thing, but

demonstrating that bees alter hormone

458 American Scientist, Volume 86

levek themselves in response to chang ing conditions is another. To show how the environment can modulate hormone levels, Robert Page of the University of California at Davis, Colette and Alain Strambi of the Centre National de la Recherche Scientifique in Marseille, France, and I induced precocious forag ing by establishing colonies that consist ed of only very young bees. Then we tested their blood levels of juvenile hor

mone and found that one-week-old pre cocious foragers had approximately 100

nanograms of juvenile hormone per mil liliter of blood, which is about the same as that in three-week-old foragers and

higher than the 5-20 nanograms usually found in one-week-old nurses. Two

weeks later, we obtained overaged nurs es from these colonies by preventing new adults from emerging, and these old nurses had levels of juvenile hor mone that resembled young nurses, rather than foragers. From work with other experimental colonies, we found that bees that reverted from foraging to

nursing were also "young" in terms of their levels of juvenile hormone.

Inhibitory Interactions How do bees perceive changes in colo

ny needs and adjust their behavioral

development to perform the tasks most in demand? Postdoctoral associate

Zachary Huang and I found that the rate of endocrine-mediated behavioral

development is influenced by inhibito

ry social interactions. That is, older bees inhibit the behavioral development of

younger bees. Bees reared in isolation in a laboratory for seven days have for

ager-like levels of juvenile hormone and forage precociously when placed in colonies. By carefully manipulating a

colony's age demography but keeping other characteristics unchanged, we found that the rate of behavioral devel

opment is negatively correlated with the proportion of older bees in a colony. So depleting a colony's foragers stimu lates younger bees to forage earlier than normal. Conversely, younger bees for

age later than normal if a colony's for

agers stay in the hive for several days because a sprinkler aimed at the hive entrance makes them think it's raining.

Someone might imagine that bees could learn about their colony's condi tion by monitoring the combs in their hive. For instance, a young bee might notice a food shortage in the combs, which might result in a neuorendocrine

response that triggers precocious be

havioral development. To explore the

possibility that bees pay attention to the combs in this way, Huang, graduate student David Schulz and I recently tested the effects of starvation on the rate of behavioral development. Young bees from starved colonies do start for

aging a few days earlier than bees from well-fed colonies. This starvation effect, however, is not mediated by perceiving a shortage of food in the honeycomb.

We showed this by keeping a colony well fed from a sugar feeder while we

constantly?but discretely?vaoiumed

any stored food out of their honeycomb. This was accomplished by drilling small holes at the base of each honeycomb cell. Well-fed bees in an empty hive started to forage at ages similar to bees in colonies with ample food stores and not nearly as early in life as did bees in

truly starved colonies.

Inhibitory social interactions that in fluence the rate of behavioral develop ment involve chemical communication between colony members. This is strik

ingly similar to pheromone regulation of sexual maturation in rodent societies. For example, a queen's mandibular

glands produce a pheromone that in hibits behavioral development. (See "The Essence of Royalty: Honey Bee

Queen Pheromone" by Mark Winston and Keith Slessor in the July-August 1992 issue of American Scientist.) Queen mandibular pheromone has been known for some time to exert long-lasting ef fects on worker physiology and behav ior by inhibiting the rearing of new

queens. More recently, Mark Winston and Tanya Pankiw of Simon Fraser

University, Huang and I demonstrated that queen mandibular pheromone de

presses blood levels of juvenile hor mone and, more important, delays the onset of foraging.

The primary modulator of behavioral

development, however, appears to come from the workers themselves. The

mandibular glands of workers contain

compounds similar to those found in

queen mandibular glands. Huang, Eri ka Plettner, a graduate student at Simon Fraser University, and I recently found that there must be direct social contact between bees for older ones to inhibit the development of younger ones.

Moreover, older bees with their man dibular glands removed do not inhibit behavioral development. The mandibu lar glands of workers contain com

pounds similar to those found in queen mandibular glands. The inhibition that

Figure 3. Hormones play a fundamental role

in a worker's behavioral development. For

example, the corpora allata (purple)?two

tiny glands located just beneath a bee's

brain (shown in close-up on the right)?pro duce juvenile hormone, which helps to time

a bee's rate of maturation. Young workers in

the hive have low levels of juvenile hor

mone in comparison with the older foragers. Moreover, juvenile-hormone treatments

cause young workers to forage precociously.

10 20 30 40 percentage of old bees

in a colony

Figure 4. Older bees inhibit the development of younger ones. The author and his postdoc toral associate Zachary Huang varied a colo

ny's age demography?producing a range of

percentages of older bees in a hive?and

then measured the percentage of experimen tal bees that became foragers by 14-32 days of age. The resulting data show that this per

centage, a measure of the rate of behavioral

development, is negatively correlated with

the proportion of older bees in a colony. The

primary modulator of behavioral develop ment appears to come from the workers

themselves, perhaps through chemical com

munication, because there must be direct

social contact for older bees to inhibit the

development of younger ones.

results from worker-worker interactions

might come from exchanging a phero mone, which might be in the mandibu lar glands or somewhere else. When we removed the glands, that could have eliminated the inhibition because it re moved the source of the pheromone or it simply blocked the pheromone's flow from another location. Clearly, more

work must be done here.

1998 September-October 459

mushroom bodies 80

W? one-day-old bees

I nurses

I foragers

Figure 5. Changes in a bee's brain accompany its behavioral development. For example, por tions of the mushroom bodies (left), a region essentially in the middle of a bee's brain, increase in size by as much as 20 percent as a worker matures from a 1-day-old to a nurse to a

forager (right). This size increase apparently arises from expanding connections between the

neurons, which probably affects how information gets processed in this region.

Consequently, increases in the size of this brain structure?considered to be the center of

learning and memory in insects?might allow bees to perform new behaviors.

Brain Remodeling How does a bee's brain support the

striking changes in behavior that take

place during maturation? A small part of the answer lies in the mushroom bod ies, a brain region thought to be the center of learning and memory in in sects. Graduate student Ginger With ers, Fahrbach and I discovered about a 20 percent increase in the volume of a

specific area of the mushroom bodies as worker honey bees mature. This vol ume increase occurs in a mushroom

body subregion where synapses, or

connections, are made between neu

rons from other brain regions that are devoted to sensory input. This was the first report of such brain plasticity in an invertebrate, and it was particularly exciting because volume increases in brain regions in vertebrates reflect in creases in certain cognitive abilities.

It seemed that the increase in the mushroom bodies might be learning related. Young workers take orientation

flights prior to the onset of foraging to learn their way around outside the hive, and the increase in volume in the mushroom bodies begins at that time. To test flying's effect on mushroom

body volume, Withers, Fahrbach and I made what we called "big-back bees."

By attaching a large tag to each bee's back and placing a screen at the hive's entrance, we prevented some workers from flying out of the hive but allowed them to interact with other bees. Big

back bees showed normal increases in

mushroom-body volume despite their

deprivation from orientation flights. So

far, the volume increase is unstoppable. Fahrbach, Darrell Moore of East Ten nessee State University, graduate stu dent Sarah Farris, postdoctoral associ ate Elizabeth Capaldi and I showed that it takes place even in bees reared in social isolation and complete darkness in a laboratory.

Still, it might be premature to ex clude the idea of a connection between the plasticity of the mushroom bodies and orientation flights in honey bees. Our results indicate that a bee's mush room bodies need not increase because of taking orientation flights, but we have not ruled out a volume increase that prepares a bee for those flights. In other words, the mushroom bodies

might need to increase in volume to

provide the necessary brain space for a bee to learn how to get around outside its hive, and how to get back.

After learning to orient outside the

hive, a bee learns to forage, and that

might also involve an increase in the mushroom bodies. Withers, Fahrbach and I showed that the mushroom bod ies increase in volume more rapidly in

precocious foragers than in nurse bees of the same age. This result has been confirmed in the laboratory of Randolf

Menzel in Berlin, using a somewhat dif ferent neuroanatomical analysis. These results suggest that the structure of the

mushroom bodies might be sensitive to

changes in social context that are associ ated with the onset of foraging. While we continue our efforts to un

ravel the significance of a volume in crease in the mushroom bodies, we also wonder how the region gets bigger. The number of cells in the mushroom bod ies is highly stable in adult life. The pro duction of new neurons is not de

tectable, and there is no evidence for cell death, according to research with Fahrbach that was performed by un

dergraduates Jennifer Strande and Jen nifer Mehren. Accordingly, the volume increase in the mushroom bodies prob ably represents an increased arboriza tion of some subpopulation of brain cells that already exists. This increased

proliferation of neuronal branches would likely result in an increase in the number of synapses per neuron, which would impact the processing of infor mation in the mushroom bodies.

Beyond structural changes in a work er bee's brain, neurochemical analyses have revealed striking changes in levels of biogenic amines, which are well known as modulators of nervous-sys tem function and organismal behavior in animals, including humans. Alison

Mercer, her colleagues from the Univer

sity of Otago in New Zealand and I found changes in brain levels of two

biogenic amines?dopamine and sero

tonin?during behavioral development. Jeffrey Harris and Joseph Woodring at Louisiana State University reported similar findings. Recently, graduate stu dents Christine Wagener-Hulme and David Schulz, research technician Jack Kuehn and I showed that another bio

genic amine, octopamine, appears to be most important in honey bee behavioral

development. When a bee receives treatments of juvenile hormone, levels of octopamine increase, but dopamine and serotonin do not. Looking specifi cally at the antenn?i lobes, a brain region that receives sensory information from a bee's antennae, we found high levels of

octopamine in the antenn?i lobes of for

agers as compared with nurse bees, re

gardless of worker age. In contrast, lev els of all three amines in the mushroom bodies are intimately associated with worker age, but not behavioral status.

These results suggest that octopamine might influence behavioral develop ment by modulating a bee's sensitivity to the stimuli that elicit the performance of age-specific tasks. We presume that these stimuli are mostly chemical, be

460 American Scientist, Volume 86

cause bees live in a dark hive and pos sess modest auditory acuity, at least rel ative to their renowned chemosensory prowess. That is why we are so en

couraged to find behaviorally related

changes specifically in the antenn?i lobes. The hypothesis that octopamine is playing a causal role in behavioral de

velopment is currently being tested by chronic adn nistration of octopamine to the brain, followed by behavioral assays. Studies of biogenic amines might also

provide some of the missing links be tween endocrine regulation and behav ioral development in honey bees.

Sociogenomics Molecular-genetic research in my labo

ratory has only recently begun, and it

currently involves selecting candidate

genes and exploring their possible in volvement in social behavior. This is done by studying whether differences in social behavior?within and between in dividuals?are correlated with variation in gene-transcription regulation, gene structure or both. Graduate student Daniel Toma and I are exploring the role of the period (per) gene in honey bee be havioral development. In the fruit fly Drosophila melanogaster, per is a principal component of the fly's circadian clock. The protein that per encodes is thought to help create circadian rhythms of ac

tivity by orchestrating the transcription of other genes according to a precisely timed schedule. We chose per because

we have found intriguing links between division of labor and circadian behav ioral rhythms in honey bees. Moore, Fahrbach, undergraduates Iain

Cheeseman and Jennifer Angel and I dis covered that foragers have pronounced circadian rhythms of activity?including being more active during the day than the night?but workers in the early part of their hive phase do not show such

rhythms. This difference is obvious both in beehives and in assays of individually isolated bees in the laboratory. For exam

ple, consider the behavior of nurse bees that need to feed bee larvae around the clock. How is this accomplished? If nurse bees have a circadian rhythm of brood care, one might expect to find evidence of "shift work," or groups of nurse bees on different schedules. Alternatively, if nurse bees perform brood care with no circadi an rhythm, one might expect to find them

performing it randomly with respect to time. Monitoring individually tagged bees every three hours around the dock in glass-walled observation hives, we

I I I 0 0.1 0.2 0.3 0.4 0.5 0.6 0.7 0.8 0.9

nursing ratio

Figure 6. Younger bees show no overt behavioral circadian rhythms, but older bees do. The author and his associates monitored patterns of task performance in glass-walled observa tion hives at regular intervals around the clock. The results for nursing behavior are shown here. The nursing ratio was calculated for each bee by dividing the number of observations of nursing during the day by those in both the day and night. A ratio of 0.5 indicates

arrhythmicty, or no difference in the number of times nursing was performed in the day ver sus the night; a ratio of 0.0 indicates that a bee had only nocturnal nursing activity; and a

ratio of 1.0 indicates that a bee had only diurnal nursing activity. A statistical analysis demonstrated that nursing is not performed according to a circadian rhythm: There was no

difference (P > 0.5) in the observed distribution (orange) of bees compared to an expected binomial distribution (black) with a probability of 0.5. By exploring the changes in gene expression that underlie these and other developmental changes in behavior, the author

expects to find that two-way interactions between the nervous system and the genome con

tribute fundamentally to the control of social behavior. (Adapted from Moore et al.)

found no evidence of rhythmicity or shift work for nursing. Nurse bees were ar

rhythmic in the performance of this task. Moreover, genetic factors appear to

influence both the plasticity in a honey bee's behavioral development and its circadian rhythm. Using colonies com

posed of workers with identifiable

genotypes, graduate student Tugrul Giray and I learned that workers of some genotypes are more likely to con

sistently mature rapidly and forage precociously, even in different social environments, and workers of other

genotypes are more apt to develop into

overaged nurses. Working with such "fast" and "slow" genotypes, Moore, Giray and I found that fast-genotype bees developed a circadian rhythm of locomotor behavior in the laboratory at younger ages than did slow-geno type bees. Fast-genotype bees also had a periodicity to their rhythm of loco

motor activity that was faster than that of slow-genotype bees. These results are reminiscent of the strikingly di verse effects of the per gene in fruit flies. This gene governs not only circa dian rhythms in flies but some ele ments of their mating song as well.

Toma and I have cloned a putative bee homologue of the per gene. We

hope to determine whether variation in

gene expression and gene structure is correlated with variation in the ontoge ny of behavioral circadian rhythmicity and the rate of behavioral develop ment. The next step is to manipulate a hive's age demography to determine the association between gene expres sion and behavioral status.

Another approach to discovering genes involved in a honey bee's behav ioral development is to build on our neuroanatomical work by identifying molecular mechanisms that contribute

1998 September-October 461

to the increase in the volume of the mushroom bodies. We hope to deter mine whether variation in the expres sion or structure of genes preferentially expressed in a honey bee's mushroom bodies affects the functioning of this brain structure, which in turn may affect behavioral development in honey bees.

Luckily, it is relatively easy to find be havioral variation that is correlated with

genotypic variation in honey bees. Sev eral laboratories, including mine, have demonstrated that variation in a work er's genotype influences many aspects of the division of labor in honey bee colo

nies, including the tendency to special ize in rare tasks such as removing corpses and guarding a nesf s entrance. In addition, controlled mating via instru

mental insemination facilitates research on honey bee behavioral genetics.

The molecular-genetic analysis of so cial behavior in general is a fertile new field. Results of classical quantitative ge netic studies have indicated that there are strong correlations between genetic variation and variation in social behav ior among individuals, but none of the

genes has been identified. (Much more work must be done on disheveled-1 be fore it could meet these criteria.) The idea that gene expression in the brain is sensitive to social context is supported by recent findings from the laboratories of Fernando Nottebohm of Rockefeller

University and David Clayton of the

University of Illinois on bird song, Don ald Pfaff of Rockefeller University and Thomas Insel of Emory University on

rodents, Russell Fernald of Stanford

University on cichlid fish and Edward Kravitz of Harvard University and Don ald Edwards of Georgia State University on lobsters. I propose that two-way in teractions between the nervous system and the genome contribute fundamen

tally to the control of social behavior. In formation about social conditions that is

acquired by the nervous system is likely to induce changes in genomic function that in turn adaptively modify the struc ture and function of the nervous system. With the presence of abundant ge

netic variation in behavior and a grow ing selection of tools needed to exploit it, the prospects are good that honey bees can be used as a new model for molecular genetic analyses of social be havior. Nevertheless, I believe that the

difficulty in studying the genetic basis of social behavior demands a bold, new initiative, which I call socioge nomics. In essence, this means taking a

wide-ranging approach to identify genes that influence social behavior, determining the influence of these

genes on underlying neural and en docrine mechanisms and exploring the effects of the environment?particular ly the social environment?on gene ac

tion. Implicit in the name socioge nomics is the realization that many genes must be studied simultaneously to decipher the complexity behind so cial behavior. Such an approach could be based on the revolutionary ad vances that are emerging from the Hu man Genome Project. For example, there are new

techniques for sequence variation analysis and simultaneously screening large numbers of genes for differences in expression that are corre lated with differences in behavioral state that can contribute significantly to gene discovery in bees.

In continued studies of honey bees, in

vestigators will probably find common mechanisms that govern life in both in vertebrate and vertebrate societies. If so, the identification of genes influencing so cial behavior in honey bees?guided by our emerging understanding of the un

derlying neural and endocrine mecha nisms?will likely yield insights that go well beyond a beehive.

Acknowledgments Work in the author's laboratory has been

supported by grants from the National Insti tute of Mental Health, National Institutes of

Health, National Science Foundation and U.S. Department of Agriculture. The author thanks his colleagues, postdoctoral associates, technician and graduate and undergraduate students for their contributions, and in par ticular Professors Susan Fahrbach and Robert Page for outstanding collaboration and stimulating camaraderie over the years.

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Links to Internet resources for further

exploration of "From Society to Genes

with the Honey Bee" are available on the

American Scientist Web site:

http: / / www.amsci.org/amsei/ articles/98articles/robinson.html

462 American Scientist, Volume 86