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Persistent exposure to mite pests, poor nutrition, pesticides, and pathogens threaten honey bee survival. In healthy colonies, the interaction of the yolk precursor protein, vitellogenin (Vg), and endocrine factor, juvenile hormone (JH), functions as a pacemaker driving the sequence of behaviors that workers perform throughout their lives. Young bees perform nursing duties within the hive and have high Vg and low JH; as older bees transition to foraging, this trend reverses. Pathogens and parasites can alter this regulatory network. For example, infection with the microsporidian, Nosema apis, has been shown to advance behavioral maturation in workers. We investigated the effects of infection with a recent honey bee pathogen on physiological factors underlying the division of labor in workers. Bees infected with N. ceranae were nearly twice as likely to engage in precocious foraging and lived 9 days less, on average, compared to controls. We also show that Vg transcript was low, while JH titer spiked, in infected nurse-aged bees in cages. This pattern of expression is atypical and the reverse of what would be expected for healthy, non-infected bees. Disruption of the basic underpinnings of temporal polyethism due to infection may be a contributing factor to recent high colony mortality, as workers may lose flexibility in their response to colony demands.

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...

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