Diversity (Insects)

Division of Labor in Insect Societies

Division of labor is fundamental to the organization of the insect societies and is thought to be one of the principal factors in their ecological success. Different activities are performed simultaneously by specialized individuals in social insect colonies, which is more efficient than if tasks are performed sequentially by unspecialized individuals.
Division of labor is one of the defining characteristics of the most extreme form of sociality in the animal kingdom, ” eusociality. ” Eusociality is defined by three traits: (1) cooperative care of young by members of the same colony, (2) an overlap of at least two generations of adults in the same colony, and (3) division of labor for reproduction, with (more or less) sterile individuals working on behalf of fecund colony members. It is now recognized by many biologists that eusociality extends to taxa beyond the ants, bees, wasps (Hymenoptera), and termites (Isoptera). This article focuses on the societies of the classic social insects, particularly the Hymenoptera, because they have the most elaborate and well-studied systems of division of labor.

DIVISION OF LABOR FOR REPRODUCTION

Females dominate the functioning of insect societies, even in termite societies, in which males play more diverse roles than in hymenop-teran societies. There are two types of females in an insect society, queens and workers. Queens specialize in reproduction and may lay up to several thousand worker eggs per day. Workers are either completely or partially sterile, engage in little, if any, personal reproduction, and perform all tasks related to colony growth and maintenance. Worker sterility occurs because the ovaries do not develop or because critical steps in oogenesis do not occur. Worker sterility occurs either during preadult stages or during adulthood.
In many species of social insects, queens and workers are distinguished by striking morphological differences. A queen can have huge ovaries and a sperm storage organ that maintains viable sperm for years. The most striking morphological differences between queens and workers occur as a result of caste determination, which occurs during preadult stages. Caste determination has an endocrine basis, involving juvenile hormone (JH), ecdysteroids, and insulin. There are caste-specific differences in the expression of genes that are associated with metabolism and protein synthesis, reflecting the fact that developing queens are metabolically more active than developing workers. Manipulating gene expression via RNA interference affects caste determination.
Little is known about how extrinsic factors act on endocrine-mediated developmental processes to influence caste determination. There is a strong circumstantial link between diet and JH in honey bee larvae; little is known about how nutritional information acts to elevate JH levels, but recent evidence implicates an epigenetic mechanism involving methylation of caste determination genes. In other species, extrinsic factors that influence caste determination include temperature and social factors such as behavioral interactions and pheromones released by adult colony members. These might affect the larvae directly or might influence the treatment accorded to them by a colony’s workers.
In societies in which queens and workers have strong morphological differences, primer pheromones produced by queens lead to the division of labor for reproduction. Only one queen primer pherom-one has been well characterized thus far, the mandibular pheromone of the queen honey bee. Workers exposed to queen pheromones show little or no ovary development or egg-laying behavior. In other species of social insects, the physical differences between queens and workers can be very slight. Division of labor for reproduction in these “primitively eusocial” species is achieved by a dominance hierarchy that is established and maintained by direct behavioral mechanisms, including pushing, biting, and physical prevention of egg laying. Behavioral domination is an ongoing process because some workers are physiologically capable of producing offspring and do so, under some circumstances.
Queen behavior and pheromones affect adult worker neuroendo-crine systems to reduce reproductive potential. These effects are likely mediated by changes in gene expression. Queen mandibular phe-romone has profound effects on brain gene activity in worker honey bees. JH has been implicated in the regulation of division of labor for reproduction in some, but not all, species studied to date, especially the bumble bee Bombus terrestris; the paper wasp, Polistes gallicus; and the fire ant, Solenopsis invicta. This is consistent with the function of JH in hormone-promoting reproductive development. JH does not appear to play this traditional role in adult honey bee, Apis mel-lifera. Ecdysteroids and biogenic amines also are suspected of being involved in the regulation of division of labor for reproduction among adult queens and workers, but a clear picture has not yet emerged.


DIVISION OF LABOR AMONG WORKERS

In most insect societies, there is also a division of labor among the workers for tasks related to colony growth and maintenance. The evolution of a highly structured worker force is generally seen as an evolutionary consequence of the developmental divergence between queens and workers. Once workers were limited to serving largely as helpers, their characteristics could be shaped further by natural selection acting at the level of the colony to increase colony fitness. This perspective is consistent with the observation that the most intricate systems of division of labor among workers are found in species with the strongest division of labor for reproduction.
Age-related division of labor is the most common form of worker organization. Workers typically work inside the nest when they are young and shift to defending the nest and foraging outside when they are older. In the more elaborate forms of age-related division of labor, such as in honey bee colonies, workers perform a sequence of jobs in the nest before they mature into foragers. Physiological changes accompany this behavioral development to increase the efficiency with which particular tasks are performed. Among these are changes in metabolism, diet, and glandular secretions.
A less common but more extreme form of division of labor among workers is based on differences in worker morphology. This is seen in a minority of ant species and nearly all termites. Morphological differences among workers result from processes similar to worker-queen caste determination, and morphologically distinct worker castes are recognized. For example, small ant workers (minors) typically labor in the nest, whereas bigger individuals (majors) defend and forage. Sometimes this form of division of labor also involves dramatic morphological adaptations in some worker castes, such as soldiers with huge and powerful mandibles and the ability to release a variety of potent defensive compounds.
A third form of division of labor among workers involves individual variability independent of age or morphology that results in an even finer grained social system. There are differences in the rate at which individual workers mature; some show precocious behavioral development, while others mature more slowly. There are also differences between individuals in the degree of task specialization. For example, foragers may specialize in the collection of a particular resource, such as some honey bees that collect only nectar or only pollen. It also has been found that some workers simply work harder than others.
The prevailing behavioral explanation for these three forms of division of labor among workers involves the application of the stimulus-response concept. Workers are thought to differ in behavior because of differences in exposure to, perception of, or response thresholds to, stimuli that evoke the performance of a specific task. These differences can result from differences in worker genotype, age, experience, or morphological caste. There is some behavioral evidence for differences among workers in stimulus perception and response thresholds; challenges for the future are to more precisely define the nature of the stimuli and extend these analyses to the neural levels.
Several endocrine and neural mechanisms regulating age-related division of labor have been discovered, primarily in honey bees. Changes in hemolymph titers of JH act to influence the rate and timing of behavioral development, but JH is not required for a worker to mature into a forager. Evidence for a similar role for JH has been found in the advanced eusocial tropical wasp Polybia occidentalis. JH also affects the activity of exocrine glands that produce brood food and alarm pheromones in honey bees, apparently acting to ensure that physiological changes are coordinated with behavioral development. As JH receptors have not yet been identified in any insect, it is not known whether JH exerts its effects on division of labor directly in the brain, on other target tissues, or at a variety of sites. Octopamine acts as a neuromodulator in honey bees. Higher levels of octopamine, particularly in the antennal lobes of the brain, increase the likelihood of foraging. Changes in brain structure also occur as a worker bee matures into a forager, particularly in the antennal lobes and mushroom bodies, but the functional significance of these changes is unknown. As with caste determination, molecular analyses of behavioral development have been initiated. Differences in the expression of thousands of genes have been detected in the brains of younger and older honey bee workers. The orchestration of the neural and behavioral plasticity that underlies age-related division of labor is based on changes in the expression of many genes in the brain and other tissues as well. Several genes already have been found to play a causal role in the regulation of age-related division of labor: foraging, malvolio, vitellogenin, and genes in the insulin signaling pathway.
Mechanisms underlying morphologically based systems of worker division of labor also have been studied. Morphological differences among adult workers have their origin in pathways of development that diverge during the larval stage. Information on worker caste differentiation, drawn largely from studies of Pheidole ants, suggests mechanisms similar to those involved in queen-worker caste determination. Both larval nutrition and JH have been implicated in the differentiation of Pheidole minors and soldiers. Genes regulating this form of division of labor also have been identified.
Heritable genetic variation is one factor influencing the third form of division of labor among workers, individual variability among workers that is independent of age or morphology. Genotypic variation within colonies arises as a consequence of multiple mating by queens or multiple queens in a colony. This genotypic variation is strongly associated with behavioral differences between individuals within a colony. Genotypic variation in honey bee colonies is known to influence how specialized a worker becomes on a particular task or the age at which it shifts from nest work to foraging. For example, Quantitative Trait Loci have been found that are associated with variation in the tendency of honey bees to collect either nectar or pollen. Genotypic effects on division of labor also have been documented in several ant and wasp species.

PLASTICITY IN COLONY

DIVISION OF LABOR

Colony division of labor, though highly structured, also shows great plasticity. Colonies respond to changing needs by adjusting the ratios of individual workers engaged in different tasks. There is plasticity in age-related division of labor, with workers able to respond to changes in colony age demography with accelerated, retarded, or reversed behavioral development. Workers also can shift to emphasizing a different task that is part of their age-specific repertoire, or they can simply work harder. Morphologically specialized workers can be induced to shift their behavior; majors, normally specialized in foraging or defense, can care for the brood in the absence of minor workers. This plasticity in division of labor contributes to the reproductive success of a colony by enabling it to continue to grow, develop, and ultimately produce a new generation of reproductive males and females during changing colony conditions.
Plasticity in division of labor in advanced eusocial species is achieved by a variety of mechanisms of behavioral integration. These mechanisms enable workers to respond to fragmentary information with actions that are appropriate to the state of the whole colony. This makes sense because it is unlikely that any individual workers have the cognitive abilities to monitor the state of their whole colony and then perform the tasks that are needed most or direct others to do so.
Mechanisms of worker behavioral integration often involve social interactions. For example, in many species, including Polybia wasps and honey bees, nest workers routinely relieve the foragers of their newly acquired loads, whether nest material or food. Foragers that are unloaded immediately upon their return to the nest are likely to continue foraging for the same resource, apparently because the quick unloading signals to them that they have brought something of high value back to the colony. In contrast, foragers that experience a significant time delay before being unloaded respond by changing their behavior, perhaps shifting to the collection of another resource. The nutritional status of a fire ant colony strongly influences the behavior of its foragers, with the relevant information transferred during social feeding. In colonies of the desert-dwelling red harvester ant, Pogonomyrmex barbatus, workers obtain information on the needs of the colony by changes in their encounter patterns with members of various task specialist groups. For example, red harvester ant foragers are more likely to leave the nest to forage when they encounter greater numbers of successful returning foragers.
Social inhibition is a potent mechanism of integration in insect colonies. In colonies of honey bees, social inhibition acts to keep the division of labor synchronized with changes in colony age demography. Older workers inhibit the rate of maturation of younger workers. Some young workers in a colony deficient in older workers, for example, exposed to lower levels of social inhibition, respond by becoming precocious foragers. The specific honey bee worker factor that causes this inhibition has been identified, and it is a pheromone produced by older bees and transferred to younger bees by food sharing. The regulation of the size of the soldier force in Pheidole colonies also is based on a process of social inhibition. In this case, the presence of adult soldiers inhibits the production of new soldiers.
The integration of activity in primitively social insect societies appears to be more centralized than in advanced eusocial societies. Primitively eusocial colonies often contain only a few dozen individuals, making centralized control more feasible. Queens act as central pacemakers and modulate worker activity via behavioral interactions in sweat bees and polistine wasps. Queens do not appear to be able to get workers to shift to different tasks, but they do cause them to work harder at the tasks they are already doing.
Good progress is being made understanding how the behavior of individual workers is integrated into a well-functioning colony. Studies of behavioral integration are aided by various kinds of theoretical models. In some models, an insect colony is likened to a developing organism, that is, the “superorganism” metaphor. In other models, an insect colony is analyzed with perspectives from neural network theory, with individual workers serving as analogs of individual neurons. Still other models view an insect colony as a self-organizing entity and use complex systems theory to develop ideas on colony function.

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