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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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Previous research showed that the presence of older workers causes a delayed onset of foraging in younger individuals in honey bee colonies, but a specific worker inhibitory factor had not yet been identified. Here, we report on the identification of a substance produced by adult forager honey bees, ethyl oleate, that acts as a chemical inhibitory factor to delay age at onset of foraging. Ethyl oleate is synthesized de novo and is present in highest concentrations in the bee's crop. These results suggest that worker behavioral maturation is modulated via trophallaxis, a form of food exchange that also serves as a prominent communication channel in insect societies. Our findings provide critical validation for a model of self-organization explaining how bees are able to respond to fragmentary information with actions that are appropriate to the state of the whole colony.

The voltage-gated sodium channel is the primary target site of pyrethroids, which constitute a major class of insecticides used worldwide. Pyrethroids prolong the opening of sodium channels by inhibiting deactivation and inactivation. Despite numerous attempts to characterize pyrethroid binding to sodium channels in the past several decades, the molecular determinants of the pyrethroid binding site on the sodium channel remain elusive. Here, we show that an F-to-I substitution at 1519 (F1519I) in segment 6 of domain III (IIIS6) abolished the sensitivity of the cockroach sodium channel expressed in Xenopus laevis oocytes to all eight structurally diverse pyrethroids examined, including permethrin and deltamethrin. In contrast, substitution by tyrosine or tryptophan reduced the channel sensitivity to deltamethrin only by 3-to 10-fold, indicating that an aromatic residue at this position is critical for the interaction of pyrethroids with sodium channels. The F1519I mutation, however, did not alter the action of two other classes of sodium channel toxins, batrachotoxin (a site 2 toxin) and Lqh␣-IT (a site 3 toxin). Schild analysis using competitive interaction of pyrethroid-stereospecific isomers demonstrated that the F1519W mutation and a previously known pyrethroid-resistance mutation, L993F in IIS6, reduced the binding affinity of 1S-cispermethrin, an inactive isomer that shares the same binding site with the active isomer 1R-cis-permethrin. Our results provide the first direct proof that Leu993 and Phe1519 are part of the pyrethroid receptor site on an insect sodium channel.

BackgroundHoney bees (Apis mellifera L.) are the most important pollinators of many agricultural crops worldwide and are a key test species used in the tiered safety assessment of genetically engineered insect-resistant crops. There is concern that widespread planting of these transgenic crops could harm honey bee populations.Methodology/Principal FindingsWe conducted a meta-analysis of 25 studies that independently assessed potential effects of Bt Cry proteins on honey bee survival (or mortality). Our results show that Bt Cry proteins used in genetically modified crops commercialized for control of lepidopteran and coleopteran pests do not negatively affect the survival of either honey bee larvae or adults in laboratory settings.Conclusions/SignificanceAlthough the additional stresses that honey bees face in the field could, in principle, modify their susceptibility to Cry proteins or lead to indirect effects, our findings support safety assessments that have not detected any direct negative effects of Bt crops for this vital insect pollinator.