Honeybee colony integration: worker-worker interactions mediate hormonally regulated plasticity in division of labor.

Abstract

Adult workers in honeybee (Apis mellfera) colonies exhibit plasticity in hormonally regulated, age-based division of labor by altering their pattern of behavioral development in response to changes in colony conditions. One form of this plasticity is precocious development: levels of juvenile hormone increase prematurely and bees begin foraging as much as 2 weeks earlier than average. We used two experimental paradigms inspired by developmental biology to study how bees obtain information on changing colony needs that results in precocious foraging. An aniag of "cell culture," with bees reared outside of colonies in different sized groups, revealed that worker-worker interactions exert quantitative effects on endocrine and behavioral development. "Transplants" of older bees to colonies otherwise lacking foragers demonstrated that worker-worker interactions also affect behavioral development in whole colonies. These results provide insights to a long-standing problem in the biology of social insects and further hghlght s arites in the integration of activity that exist between individuals in insect colonies and cells in metazoans.A central question in insect sociobiology is how the activities of individual workers are integrated to enable colonies to develop and produce reproductives despite changing internal and external conditions. The regulation of age-based division of labor among workers demands a high level of colony integration. Honeybees (Apis mellifera) generally work in the nest for the first 3 weeks ofadult life and then spend their final 1-3 weeks foraging, but they can accelerate, retard, or reverse their behavioral development in response to changes in colony or environmental conditions, or both (1). It is important for colony survival and reproduction that bees respond accurately to the need for a particular worker activity because the shift from nest duties to foraging requires complex physiological changes (2).We studied how workers obtain information that influences one form of plasticity in behavioral development: precocious development, in which bees begin foraging as much as 2 weeks earlier than average (2). Precocious foraging may occur naturally in colonies deficient in foragers due to a seasonal surge in birth rates or because of the loss offoragers to predators; it can also be induced experimentally in colonies that lack older bees (1).It is unlikely that an individual worker has the capacity to acquire and integrate information on the global state of its colony, in which a dozen different activities, performed by tens of thousands of individuals, may be proceeding simultaneously. The regulation of-plasticity in worker behavioral development thus may be similar conceptually to the regulation of plasticity in cell development: workers, like cells, develop in response to local stimuli in ways that are appropriate at the global level. Cell development is mediated by interactions with the extracellular matrix (3,4) and with other cells (5-7). Similarly, worker development may be media...

Effects of social group size on information transfer and task allocation

“…In models of social behaviour that depend on interaction rates, this distinction is often built in. For example, recent models of foraging and patrolling behaviour refer to information transfer during interactions (Seeley et al, 1991;Adler and Gordon, 1992); others on age polyethism suggest there may be physiological effects of substances transmitted during interaction (Huang and Robinson, 1992). The work presented here suggests this distinction may be irrelevant to the dynamics of the group's behaviour.…”

“…Robinson's studies of age polyethism (e.g. Huang and Robinson, 1992) suggest that interactions between old and young honey bees determine which tasks a worker performs. Social behaviour that depends on interaction rates can be divided into two categories: (l) an interaction leads to information transfer, affecting the decisions of individuals involved in the interaction and (2) an interaction has some inevitable, physiological effect on the participants.…”

Order, Disorder, Death: Lessons from a Superorganism

“…The foragers synthesize a blend of cuticular hydrocarbons and pheromones that are specific to their stage (Leoncini et al, 2004b;Pankiw, 2004a). This signature is transferred by physical contact with the nurse bees (Huang and Robinson, 1992). Nurse bees and foragers antennate, groom, and feed each other (Winston, 1987), and though these social transfers the nurse bees can identify the relative size of the forager population (Huang and Robinson, 1996).…”

Age, caste, and behavior determine the replicative activity of intestinal stem cells in honeybees (Apis mellifera L.)

“…To decouple worker age and behavioral profile, a single-cohort colony (Huang and Robinson, 1992) was set up in an observation hive with newly emerged, individually tagged workers.…”