Division of Labor
Individual workers perform different tasks at different ages
Clarence Collison
Colony life is organized by a complex and sophisticated division of labor. “Individual workers perform different tasks at different ages. Age-related division of labor is based on a form of behavioral development by workers known as age polytheism. Young individuals perform tasks in the nest such as brood care and nest maintenance, and then venture outside to collect food and defend the nest when they get older” (Robinson and Huang 1998).
After emergence as adults, usually the worker bees first clean cells, and as they age, they feed the larvae and queen, process and store food, secrete wax and construct comb, and guard the entrance. The most prominent behavioral change is observed when the bees are about three weeks old, the age when they start foraging (Seeley and Kolmes 1991). Plasticity is an important attribute of division of labor and colonies respond to changes in the internal and external environment by manipulating the ratios of individual workers involved in different tasks. Such plasticity in division of labor can be partially attributed to behavioral flexibility of the individual workers (Robinson 1992; Sagili et al. 2011).
There is a genetic component to plasticity in age polytheism in honey bee colonies, such that workers of some genotypes become precocious foragers more readily than workers of other genotypes, in colonies lacking older bees. Using colonies composed of workers from two identifiable genotype groups, we determined that intracolony differences in the likelihood of becoming a precocious forager are a consequence of differences in rates of behavioral development that are also evident under conditions leading to normal development. An alternative hypothesis, that differences in the likelihood of becoming a precocious forager are due to differences in general sensitivity to altered colony conditions, was not supported. In three out of three trials, workers from the genotype group that was more likely to exhibit precocious foraging in single cohort colonies also foraged at relatively younger ages in colonies in which workers exhibited normal behavioral development. In contrast, in three out of three trials, workers from the genotype group that was more likely to exhibit precocious foraging in single cohort colonies did not show disproportionately more overaged nursing in colonies in which workers exhibited delayed development. These results indicate that genotypic differences in plasticity in age-related division of labor are based on genotypic differences in rates of behavioral development (Giray and Robinson 1994).
Brillet et al. (2002) measured the age at onset of foraging in colonies derived from three races of European honey bees, Apis mellifera mellifera, Apis mellifera caucasica and Apis mellifera ligustica, using a cross-fostering design that involved six unrelated colonies of each race. There was a significant effect of the race of the introduced bees on the age at onset of foraging: cohorts of A. m. ligustica bees showed the earliest onset, regardless of the race of the colony they were introduced to. There also was a significant effect of the race of the host colony: cohorts of bees introduced into mellifera colonies showed the earliest onset of foraging, regardless of the race of the bees introduced. Significant inter-trial differences also were detected, primarily because of a later onset of foraging in trials conducted during the Autumn (September-October). These results demonstrate differences among European races of honey bees in one important component of colony division of labor.
The age at which worker honey bees begin foraging varies under different colony conditions. Previous studies have shown that juvenile hormone (JH) mediates this behavioral plasticity, and that worker-worker interactions influence both JH titers and age at first foraging. These results also indicated that the age at first foraging is delayed in the presence of foragers, suggesting that colony age demography directly influences temporal division of labor. Huang and Robinson (1996) tested this hypothesis by determining whether behavioral or physiological development can be accelerated, delayed or reversed by altering colony age structure. In three out of three trials, earlier onset of foraging was induced in colonies depleted of foragers, compared to colonies depleted of an equal number of bees across all age classes. In two out of three trials, delayed onset of foraging was induced in colonies in which foragers were confined compared to colonies with free-flying foragers. Finally, in three out of three trials, both endocrine and exocrine changes associated with reversion from foraging to brood care were induced in colonies composed of all old bees and devoid of brood; JH titers decreased and hypopharyngeal glands regenerated. These results demonstrate that plasticity in age-related division of labor in honey bee colonies is at least partially controlled by social factors.
Efficient division of labor is one of the main reasons for the success of the social insects. In honey bees the division of labor is principally achieved by workers changing tasks as they age. Typically, young adult bees perform a series of tasks within the colony before ultimately making the transition to foraging outside the hive for resources. This lifelong behavioral development is a well-characterized example of naturally occurring behavioral plasticity, but its neural bases are not well understood. Two techniques were used to assess the role of biogenic amines in the transition from in-hive work to foraging, which is the most dramatic and obvious transition in honey bee behavioral development. First, associations between amines and tasks were determined by measuring the levels of amines in dissected regions of individual bee brains using HPLC analysis. Second, colonies were orally treated with biogenic amines and effects on the onset of foraging were observed. Octopamine concentration in the antennal lobes of the bee brain was most reliably associated with task: high in foragers and low in nurses regardless of age. In contrast, octopamine in the mushroom bodies, a neighboring neuropil, was associated with age and not behavior, indicating independent modulation of octopamine in these two brain regions. Treating colonies with octopamine resulted in an earlier onset of foraging in young bees. In addition, octopamine levels were not elevated by non-foraging flight, but were already high on return from the first successful foraging trip and subsequently remained high, showing no further change with foraging experience. This observation suggests that octopamine becomes elevated in the antennal lobes in anticipation of foraging and is involved in the release and maintenance of the foraging state. Foraging itself, however, does not modulate octopamine levels. Behaviorally related changes in octopamine are modulated by juvenile hormone, which has also been implicated in the control of honey bee division of labor. Treatment with the juvenile hormone analog methoprene elevated octopamine and octopamine treatment ‘rescued’ the delay in behavioral development caused by experimentally depleting juvenile hormone in bees. Although the pathways linking juvenile hormone and octopamine are presently unknown, it is clear that octopamine acts ‘downstream’ of juvenile hormone to influence behavior and that juvenile hormone modulates brain octopamine levels. A working hypothesis is that octopamine acts as an activator of foraging by modulating responsiveness to foraging-related stimuli. This is supported by the finding that octopamine treatment increased the response of bees to brood pheromone, a stimulator of foraging activity. Establishing a role for octopamine in honey bee behavioral development is a first step in understanding the neural bases of this example of naturally occurring, socially mediated, behavioral plasticity. The next level of analysis will be to determine precisely where and how octopamine acts in the nervous system to coordinate this complex social behavior (Schulz et al. 2002).
Forager honey bees have higher brain levels of octopamine than do bees tending larvae in the hive. To test the hypothesis that octopamine influences honey bee division of labor, they treated bees orally with octopamine or its immediate precursor tyramine and determined whether these treatments increased the probability of initiating foraging. Octopamine treatment significantly elevated levels of octopamine in the brain and caused a significant dose-dependent increase in the number of new foragers. This effect was seen for precocious foragers in single-cohort colonies and foragers in larger colonies with more typical age demographies. Tyramine treatment did not increase the number of new foragers, suggesting that octopamine was exerting a specific effect. Octopamine treatment was effective only when given to bees old enough to forage, i.e., older than four days of age. Treatment when bees were one to three days of age did not cause a significant increase in the number of new foragers when the bees reached the minimal foraging age. These results demonstrate that octopamine influences division of labor in honey bee colonies. They speculate that octopamine is acting in this context as a neuromodulator (Schultz and Robinson 2001).
Molecular analysis of a complex behavioral phenotype is facilitated by dissecting it into simpler behavioral components. Using this approach, Ben-Shahar et al. (2004) present evidence implicating increased manganese transport by the malvolio (mvl) gene into brain cells as one factor that influences age-related division of labor in honey bee colonies. They studied mvl because manganese affects sucrose responsiveness in Drosophila melanogaster (fruit flies), and sucrose responsiveness is related to division of labor in honey bee colonies. Honey bee foragers are more responsive to sucrose in the laboratory than are younger nurse bees, and pollen foragers are more responsive to sucrose than nectar foragers. Levels of mvl mRNA in the brain and manganese in the head were higher in pollen foragers compared with nurses, with nectar foragers intermediate. Manganese treatment increased honey bee sucrose responsiveness and caused precocious foraging. Manganese levels showed a similar pattern to mvl mRNA but manganese treatment did not increase pollen foraging. These results suggest that, while there are molecular pathways common to sucrose responsiveness and division of labor, linkages between a complex behavior and some of its simpler behavioral components are not obligatory.
Research has shown that age-related division of labor is associated with changes in activity rhythms; young adult bees perform hive tasks with no daily rhythms, whereas older bees forage with strong daily rhythms. Toma et al. (2000) reported that this division of labor is also associated with differences in both circadian rhythms and mRNA of period, a gene well known for its role in circadian rhythms. The level of period mRNA in the brain oscillated in bees of all ages, but was significantly higher at all times in foragers. Elevated period mRNA levels cannot be attributed exclusively to aging, because bees induced to forage precociously because of a change in social environment had levels similar to normal age foragers. These results extend the regulation of a ‘‘clock gene’’ to a social context and suggest that there are connections at the molecular level between division of labor and chronobiology in social insects.
Division of labor is highlighted by adult bees making a transition at two to three weeks of age from working in the hive to foraging for nectar and pollen outside. This behavioral development involves acquisition of new tasks that may require advanced learning capabilities. Because acetylcholinesterase (AChE) hydrolyzes acetycholine, a major neurotransmitter associated with learning in the insect brain, Shapira et al. (2001) searched for changes in AChE expression in the brain during bee behavioral development. Biochemical aspects of the AChE protein were similar in foragers and “nurse” bees that work in the hive tending brood. However, catalytic AChE activity was significantly lower in foragers. Cloning of bee AChE cDNA enabled mRNA analysis, which demonstrated that the forager-related decrease in AChE activity was associated with decreased AChE mRNA levels. This was particularly apparent in the mushroom bodies, a brain region known to be involved with olfactory and visual learning and memory. In addition, treatment with the AChE-inhibitor metrifonate improved performance in an olfactory-learning assay. These findings demonstrate long-term, naturally occurring developmental downregulation of AChE gene expression in the bee brain, and suggest that this genomic plasticity can contribute to facilitated learning capabilities in forager bees.
Division of labor has been claimed to benefit fitness. In honey bees, the adult work force may be viewed as divided between non-foraging hive bees that rear brood and maintain the nest, and foragers that collect food outside the nest. Honey bee brood pheromone is a larval pheromone that serves as an excellent empirical tool to manipulate foraging behaviors and thus division of labor in the honey bee. Sagili et al. (2011) used two different doses of brood pheromone to alter the foraging stimulus environment, thus changing demographics of colony division of labor, to demonstrate how division of labor associated with brood rearing affects colony growth rate. They examined the effects of these different doses of brood pheromone on individual foraging ontogeny and specialization, colony level foraging behavior and individual glandular protein synthesis. Low brood pheromone treatment colonies exhibited significantly higher foraging population, decreased age of first foraging and greater foraging effort, resulting in greater colony growth compared to other treatments. This study demonstrates how division of labor associated with brood rearing affects honey bee colony growth rate, a token of fitness.
References
Ben-Shahar, Y., N.L. Dudek, and G.E. Robinson 2004. Phenotypic deconstruction reveals involvement of manganese transporter malvolio in honey bee division of labor. J. Exp. Biol. 207: 3281-3288.
Brillet, C., G.E. Robinson, R. Bues and Y. Le Conte 2002. Racial differences in division of labor in colonies of the honey bee (Apis mellifera). Ethology 108: 115-126.
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Schulz, D.J., A.B. Barron, and G.E. Robinson 2002. A role for octopamine in honey bee division of labor. Brain Behav. Evol. 60: 350-359.
Seeley, T.D. and S.A. Kolmes 1991. Age polytheism for hive duties in honeybees-illusion or reality? Ethiology 87: 284-297.
Shapira, M., C.K. Thompson, H. Soreq and G.E. Robinson 2001. Changes in neuronal acetylcholinesterase gene expression and division of labor in honey bee colonies. J. Mol. Neurosci. 17: 1-12.
Toma, D.P., G. Bloch, D. Moore and G.E. Robinson 2000. Changes in period mRNA levels in the brain and division of labor in honey bee colonies. Proc. Natl. Acad. Sci. USA 97: 6914-6919.
Clarence Collison is an Emeritus Professor of Entomology and Department Head Emeritus of Entomology and Plant Pathology at Mississippi State University, Mississippi State, MS.
