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Social Behavior

Communicating and learning from each other are part of the success of insect societies, but some of the most complex, self-organizing societies function on the basis of very simple processes of information transfer between individuals.

For social insects with larger colonies, queen dominance is often replaced by other forms of control. Indeed, usually workers of many species of ant, bee and wasp do not lay eggs, despite having functional ovaries. However, under certain circumstances, given an opportunity, workers will lay eggs. In a large colony, the queen could not successfully police all such behavior and often ignores it. Instead, other workers do the policing, destroying the eggs of their co-workers.

A comparative study of ten policing insect species revealed that altruism is modulated more by constraints on worker reproduction than by relatedness. The species with the highest fraction of fully committed altruistic workers - those that do not lay eggs - tend to be those with lower relatedness, contrary to simple expectation. Instead, more workers are fully committed when policing is most effective, as measured by the fraction of worker-laid eggs eaten by either queens or other workers. Workers are not leaping at every opportunity to be altruistic; they are coerced into that role, often by their fellow workers.

Thus, cooperation among workers and their seeming altruism result from strict policing by nest mates. With honey bees, workers refrain from laying eggs in the presence of a fecund queen. The mechanism by which workers switch off their ovaries is cued by pheromones, but there are genetically-based variations among individuals: some workers have high thresholds for ovary activation while for others the response threshold is lower.

Genetic variation for threshold response by workers to ovary-suppressing cues is most evident in 'anarchist' colonies in which mutant patrilines have a proportion of workers that activate their ovaries and lay eggs despite the presence of a queen. As long as other workers police and eat these eggs, there is no problem. However, if this process breaks down, the colony is usually headed to unsuccessful queen supercedure, resulting in the demise of the colony.

Many social conflicts create winners and losers. But only kinship allows evolution to make creative use of the social losers, turning them into non-reproductive police, exquisite communicators and heroic defenders. The honey bee will not hasten to sting unless danger is imminent and definite. The stinging honey bee worker commits suicide when her sting is torn out, but this saves her kin. She is not 'making an escape from outrageous fortune' (like Shakespeare's Hamlet), but making the best of it - not fearful of what dreams may come, but hopeful for what genes may come. However socially constrained her life may have been, her last action makes her own clear statement: long live the kin!

In the 1932 novel Brave New World, Aldous Huxley created a society where fetuses develop in bottles and are treated with chemicals to modify their bodies and mentalities. Later, children are sleep-conditioned to their future task in society. This procedure creates people who have clear roles, putting them in castes, ranging from alphas (the leaders) to epsilons (the drones). Among other things, lower castes are programmed not to be aggressive against higher caste members. A treatment with neurotoxic chemicals during development leads to the appropriate brain changes.

Within the animal kingdom, social insects have evolved the most stable caste societies. Many ant species have a wide range of castes, from workers to foragers, from groomers to soldiers. Individuals all develop from eggs laid by the same mother--the colony's queen. Generally, the food supplied to each egg is the biological signal that leads the embryo to develop into one caste or another, a situation reminiscent of Huxley's fictional world. Thus, if we take as an example the leaf-cutter ant, Atta texana, small individuals tend to the fungus garden within the nest, intermediate-sized individuals search and collect leaves from the forest to feed the fungus, and large individuals with strong mandibles defend the colony.

Honey bees have evolved a different caste system. The individual worker bees are always females because male drones do not contribute to social life apart from mating with queens during nuptial flights. The workers perform different tasks in the course of their lives and start off as nurses tending to the hive right after emergence, continue with tasks such as nest-building and hive defense, and then end their lives as foragers by collecting nectar and pollen to make honey and feed their sisters.
How is this developmental polyethism organized? Age is the main factor that determines the task that an individual will perform, mediated by regulation with juvenile hormones, but feedback from the hive is also important. Much information is delivered by pheromones. For example, when a hive loses the queen, her queen mandibular pheromone (QMP) will also disappear, leading to rapid changes in behavior among the worker bees who start raising new queens to replace her.

However, the life of a honey bee is not hard-wired. Bees are amazingly intelligent animals and learn a lot about their environment. Their context adaptation beyond age-related caste is phenomenal. Recent results have created an unprecedented link from molecules all the way to complex behavior, and some of the molecular effects of QMP are now understood. It turns out that QMP directly influences the chemistry of the brain in an age-dependent manner, contributing to developmental polyethism.

One major component of QMP is homovanillyl alcohol (HVA), a substance with a striking chemical similarity to the biogenic amine dopamine, the neurotransmitter that mediates aversive learning. Indeed, QMP acts directly on the dopamine pathway: Levels of dopamine in the brain are reduced in young bees exposed to QMP, and this effect is amplified by a concurrent reduction in the levels of dopamine-sensitive receptors. Thus, exposure of a nurse bee to the queen's odor down-regulates the brain's dopamine networks and reduces activity levels. Indeed, the fact that neurotransmitters affect human behavior and the role of hormones and environment in eliciting such behavioral modification is well known to all parents dealing with teenagers.

Thus, the presence of the queen, through her pheromone, influences the behavior, and indeed the brain pharmacology, of her hive. Young workers remain in the hive, are docile, and display less motor activity, whereas older guards and foragers leave the hive and become more motile and aggressive.

Why would aversive learning be blocked in a young nurse bee? Within the hive, the sting reflex can only have negative effects. Thus, preventing nurse bees from developing aversive memories against the odors in the hive, which include the queen's own odor, makes the colony more secure. With increasing age, bees start to leave the colony, fly to distant foraging sites, and perform tasks outside the hive where they need to learn not only about sweet nectar but also about nasty dangers. It is useful, under these circumstances, that the effect of QMP blocks aversive learning wanes. This is a wonderful example in which the effect of a releaser pheromone can be followed all the way to the neurons that are being modulated, and then to behavioral modifications. It also goes a long way to explain how behavioral context is governed at the molecular level.

Thus, honey bees differ substantially from the beings in Huxley's world because individuals are not trapped within their castes for their entire life span. The manipulation of brain activity by the queen, modulating learning capacity in young bees to make them more docile, is a different view of parenthood. As the saying goes: "When children are young, give them roots; when they grow, give them wings." The bee mother seems to have evolved to appreciate and execute exactly this strategy for her family.

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