Labor In Honey Bees Research Articles

Gut microbiota influences onset of foraging-related behavior but not physiological hallmarks of division of labor in honeybees.

The honeybee is emerging as a model system for studying gut microbiota-host interactions. Previous studies reported gut microbiota effects on multiple worker bee phenotypes, all of which change during behavioral maturation-the transition from nursing to foraging. We tested whether the documented effects may stem from an effect of the microbiota on behavioral maturation. The gut microbiota only subtly affected maturation: it accelerated the onset of foraging without affecting the overall proportion of foragers or their average output. We also found no effect of the microbiota on host weight, cuticular hydrocarbon (CHC) profile, hypopharyngeal gland size, and the expression of behavioral maturation-related genes. These results are inconsistent with previous studies reporting effects of the gut microbiota on bee weight and CHC profile. Our experiments revealed that co-housed bees tend to converge in behavior and physiology, suggesting that spurious associations may emerge when rearing environments are not replicated sufficiently or accounted for analytically.

Possible interactions between gut microbiome and division of labor in honey bees.

Recent studies have provided new insights into the role of the microbiome in shaping host behavior. However, the relationship between the temporal division of labor among honey bees (Apis mellifera) and their gut microbial community has not been widely studied. Therefore, we aimed to evaluate the link between the gut microbiome and division of labor in honey bees by examining the microbial absolute abundance and relative composition of 7-day-old nurse bees and 28-day-old forager bees from a natural hive, as well as those of worker bees of the same 14-day-old age showing different behaviors in a manipulated hive. We found that forager bees had fewer core bacteria, particularly gram-positive fermentative genera such as Lactobacillus and Bifidobacterium, with Bifidobacterium asteroides being the most sensitive to host behavioral tasks. Our results showed that forager bees have lower gut community stability compared to nurse bees, suggesting that their gut community is more susceptible to invasion by non-core members. Furthermore, a pollen limitation experiment using caged honey bees indicated that dietary changes during behavioral shifts may be a driving factor in honey bee microbial diversity. This study contributes to a greater understanding of the interaction between the gut microbiome and behavioral tasks and provides a foundation for future assays.

Major royal jelly proteins influence the neurobiological regulation of the division of labor among honey bee workers

Age-based division of labor among workers is a fundamental life-history trait of many social insects, including the Western honey bee, Apis mellifera L. Extensive studies of the causation of the most pronounced transition from performing tasks in the nest to outside foraging indicate hormonal regulation of complex physiological changes. However, the proximate neurobiological mechanisms that cause the behavioral repertoire to change are still not understood and require novel approaches to be fully characterized. Thus, we established the first comprehensive monoclonal antibody microarray in honey bees with 16,320 antibodies to directly identify proteins in the brain that regulate the transition to foraging. Major royal jelly protein (MRJP) 1 and MRJP3 were identified as potential protein effectors and further investigated. A series of experimental manipulations of the workers' behavioral transition led to changes in MRJP1 and MRJP3 quantities in accordance with their presumed functional role. Injection of MRJPs into the brain resulted in increased task-reversal from foraging to nursing and decreased task-progression from nursing to foraging, while the latter was increased by injection with MRJP antibodies. Finally, down-regulation of MRJP1 and MRJP3 expression via RNAi injection into the brain increased the transition from in-hive nursing to outside foraging, confirming a causal role of these two proteins in the proximate regulation of behavior and life-history of honey bee workers. Interaction partners of MRJP1 and MRJP3 in the honey bee brain included other regulators of honey bee behavior and life history. Thus, our transformative methodological advancement of proteome analysis in honey bees reveals novel regulators of honey bee behavior, extends our understanding of the functional pleiotropy of MRJPs, and supports a general nutrition-based model of the regulation of the age-based division of labor in honey bees.

Behavioral genetics and genomics: Mendel’s peas, mice, and bees

The question of the heritability of behavior has been of long fascination to scientists and the broader public. It is now widely accepted that most behavioral variation has a genetic component, although the degree of genetic influence differs widely across behaviors. Starting with Mendel’s remarkable discovery of “inheritance factors,” it has become increasingly clear that specific genetic variants that influence behavior can be identified. This goal is not without its challenges: Unlike pea morphology, most natural behavioral variation has a complex genetic architecture. However, we can now apply powerful genome-wide approaches to connect variation in DNA to variation in behavior as well as analyses of behaviorally related variation in brain gene expression, which together have provided insights into both the genetic mechanisms underlying behavior and the dynamic relationship between genes and behavior, respectively, in a wide range of species and for a diversity of behaviors. Here, we focus on two systems to illustrate both of these approaches: the genetic basis of burrowing in deer mice and transcriptomic analyses of division of labor in honey bees. Finally, we discuss the troubled relationship between the field of behavioral genetics and eugenics, which reminds us that we must be cautious about how we discuss and contextualize the connections between genes and behavior, especially in humans.

Context-dependent influence of threat on honey bee social network dynamics and brain gene expression.

Adverse social experience affects social structure by modifying the behavior of individuals, but the relationship between an individual's behavioral state and its response to adversity is poorly understood. We leveraged naturally occurring division of labor in honey bees and studied the biological embedding of environmental threat using laboratory assays and automated behavioral tracking of whole colonies. Guard bees showed low intrinsic levels of sociability compared with foragers and nurse bees, but large increases in sociability following exposure to a threat. Threat experience also modified the expression of caregiving-related genes in a brain region called the mushroom bodies. These results demonstrate that the biological embedding of environmental experience depends on an individual's societal role and, in turn, affects its future sociability.

INSIGHTS OF CASTE DETERMINATIONS IN SOCIAL INSECTS

Eusocial insects display caste structures in which reproductive ability is possessed by a single or a few queens while all other colony members act as workers. In social insects like ants, bees, and termites, vital physiological processes are regulated at the colony scale. Females in social insects have at least one reproductive caste and one nonreproductive caste; many termites have at least two male castes. The castes have considerable anatomical, physiological, and behavioural differences in higher social insects. Organismal systems, such as pheromone sensing, hormone signaling, and brain signaling pathways, are deployed in novel circumstances to impact nestmate and colony behaviours due to physiological decentralization over evolutionary time. Significant morphogenesis with region-specific cellular proliferation and degradation occurs during soldier development through two moulting via a presoldier stage in termite. JH action has been developed, in which a high JH titer causes soldier differentiation and a low JH titer causes alate differentiation. A monogamous pair of primary reproductives (one king and one queen) generated from alates normally establishes termite colonies (winged adults). The nymph-alate pathway (sexual pathway) or the worker pathway differentiates larvae in Reticulitermes termites (neuter pathway). Haplo-diploid sex determination controls the first developmental transition, in which unfertilized (haploid) embryos become males and fertilized (diploid) embryos become females in the case of Cataglyphis ant genus. The queen’s mandibular gland secretion, a mix of fatty acids and aromatic chemicals, is critical for maintaining the reproductive division of labour in honeybees (Apis mellifera), suppressing ovary growth in workers. Besides this, the brood produced by the queen also inhibits ovary development in workers by emitting two pheromones: the brood pheromone (BP), mainly composed of esters, and the highly volatile E-b-ocimene.

The Biology of the Cape Honey Bee, Apis mellifera capensis (Hymenoptera: Apidae): A Review of Thelytoky and Its Influence on Social Parasitism and Worker Reproduction

Abstract Cohesion in social insect colonies is maintained by use of chemical signals produced by the queen, workers, and brood. In honey bees in particular, signals from the queen and brood are crucial for the regulation of reproductive division of labor, ensuring that the only reproductive female individual in the colony is the queen, whereas the workers remain reproductively sterile. However, even given this strict level of control, workers can, in principle, activate their ovaries and lay eggs. Although much is known about the behavioral and physiological traits that accompany the switch from worker sterility to being reproductively active, much less is known regarding the molecular changes that accompany this switch. This review will explore what is known about the genes and molecular pathways involved in the making of laying workers/false queens in the Cape honey bee, Apis mellifera capensis Eschscholtz, through an analysis of the basis for thelytoky in this subspecies, the exocrine glandular chemistry of reproductively dominant workers and what is known about the biosynthesis of their pheromone components. This review will contribute to our understanding of the genetic regulation of thelytoky and the molecular mechanisms that govern reproductive division of labor in honey bees and provide generalizations that may be applicable to other social hymenoptera using this evolutionary fascinating example of worker reproduction.

Division of labor in honey bees is associated with transcriptional regulatory plasticity in the brain.

Studies in evolutionary and developmental biology show that relationships between transcription factors (TFs) and their target genes can be altered to result in novel regulatory relationships that generate phenotypic plasticity. We hypothesized that context-dependent shifts in the nervous system associated with behavior may also be linked to changes in TF-target relationships over physiological time scales. We tested this hypothesis using honey bee (Apis mellifera) division of labor as a model system by performing bioinformatic analyses of previously published brain transcriptomic profiles together with new RNAi and behavioral experiments. The bioinformatic analyses identified five TFs that exhibited strong signatures of regulatory plasticity as a function of division of labor. RNAi targeting of one of these TFs (broad complex) and a related TF that did not exhibit plasticity (fushi tarazu transcription factor 1) was administered in conjunction with automated analyses of foraging behavior in the field, laboratory assays of aggression and brood care behavior, and endocrine treatments. The results showed that changes in the regulatory relationships of these TFs were associated with behavioral state, social context and endocrine state. These findings provide the first empirical evidence that TF-target relationships in the brain are altered in conjunction with behavior and social context. They also suggest that one mechanism for this plasticity involves pleiotropic TFs high up in regulatory hierarchies producing behavior-specific transcriptional responses by activating different downstream TFs to induce discrete context-dependent transcriptional cascades. These findings provide new insights into the dynamic nature of the transcriptional regulatory architecture underlying behavior in the brain.

Levels and activity of cyclic guanosine monophosphate-dependent protein kinase in nurse and forager honeybees.

Age-dependent division of labour in honeybees was shown to be connected to sensory response thresholds. Foragers show a higher gustatory responsiveness than nurse bees. It is generally assumed that nutrition-related signalling pathways underlie this behavioural plasticity. Here, one important candidate gene is the foraging gene, which encodes a cyclic guanosine monophosphate-dependent protein kinase (PKG). Several roles of members of this enzyme family were analysed in vertebrates. They own functions in important processes such as growth, secretion and neuronal adaptation. Honeybee foraging messenger RNA expression is upregulated in the brain of foragers. In vivo activation of PKG can modulate gustatory responsiveness. We present for the first time PKG protein level and activity data in the context of social behaviour and feeding. Protein level was significantly higher in brains of foragers than in those of nurse bees, substantiating the role of PKG in behavioural plasticity. However, enzyme activity did not differ between behavioural roles. The mediation of feeding status appears independent of PKG signalling. Neither PKG content nor enzyme activity differed between starved and satiated individuals. We suggest that even though nutrition-related pathways are surely involved in controlling behavioural plasticity, which involves changes in PKG signalling, mediation of satiety itself is independent of PKG.

Mitochondrial capacity, oxidative damage and hypoxia gene expression are associated with age-related division of labor in honey bee (Apis mellifera L.) workers.

During adult life, honey bee workers undergo a succession of behavioral states. Nurse bees perform tasks inside the nest, and when they are about 2-3 weeks old they initiate foraging. This switch is associated with alterations in diet, and with the levels of juvenile hormone and vitellogenin circulating in hemolymph. It is not clear whether this behavioral maturation involves major changes at the cellular level, such as mitochondrial activity and the redox environment in the head, thorax and abdomen. Using high-resolution respirometry, biochemical assays and RT-qPCR, we evaluated the association of these parameters with this behavioral change. We found that tissues from the head and abdomen of nurses have a higher oxidative phosphorylation capacity than those of foragers, while for the thorax we found the opposite situation. As higher mitochondrial activity tends to generate more H2O2, and H2O2 is known to stabilize HIF-1α, this would be expected to stimulate hypoxia signaling. The positive correlation that we observed between mitochondrial activity and hif-1α gene expression in abdomen and head tissue of nurses would be in line with this hypothesis. Higher expression of antioxidant enzyme genes was observed in foragers, which could explain their low levels of protein carbonylation. No alterations were seen in nitric oxide (NO) levels, suggesting that NO signaling is unlikely to be involved in behavioral maturation. We conclude that the behavioral change seen in honey bee workers is reflected in differential mitochondrial activities and redox parameters, and we consider that this can provide insights into the underlying aging process.

Variation in individual worker honey bee behavior shows hallmarks of personality

The existence of personalities has been explored in various invertebrates, but a comprehensive investigation of personality differences across individuals in a eusocial insect has not yet been conducted. The study of personality differences across individuals within the same behavioral caste may contribute to an understanding of how social insects divide labor within the nest. Here, we define and investigate three dimensions of personality within the worker caste of a model social insect, the honey bee Apis mellifera, as follows: (1) consistent individual behavioral differences over time, (2) consistent individual behavioral differences across contexts, and (3) the presence of correlated suites of behaviors. To test whether honey bee workers exhibit dimensions 1 and 2, we repeatedly assessed responses of groups of same-age bees in cages to stimuli that are relevant to bee life history. To test for dimension 3, we examined behavior within a colony context by using observation hives to record the behaviors of individual bees across their lifetimes. Our results provide some evidence for all three dimensions of personality in honey bee workers. In particular, our data suggest some individuals may be more likely to be highly interactive with other workers (e.g., engaging in food sharing), while other individuals are consistently less interactive. These findings expand upon and contribute to previous models for the organization of worker division of labor in honey bees, suggesting that consistent behavioral differences (personalities) of workers within a behavioral caste have the potential to contribute to subcaste division of labor. Behavioral ecologists have become increasingly interested in animal personalities, individual behavioral differences that are consistent over time and in different contexts, with recent focus on understanding the occurrence of personalities across taxa and their adaptive value. The existence and function of personality differences among individuals in complex societies, such as eusocial insects, remain understudied. Here, we provide the first comprehensive investigation of whether workers of the highly eusocial honey bee show hallmarks of personality. Although these workers demonstrate well-documented behavioral changes as they age, we uncovered some aspects of their behavior, in particular, their tendency to physically interact with other bees, remain somewhat consistent even as they age and change roles within the colony. We suggest that individual-level personality differences have the potential to contribute to colony division of labor by creating variation in individual tendencies to perform different tasks.

From honeybees to robots and back: division of labour based on partitioning social inhibition

In this paper, a distributed adaptive partitioning algorithm inspired by division of labor in honeybees is investigated for its applicability in a swarm of underwater robots in one hand and is qualitatively compared with the behavior of honeybee colonies on the other hand. The algorithm, partitioning social inhibition (PSI), is based on local interactions and uses a simple logic inspired from age-polyethism and task allocation in honeybee colonies. The algorithm is analyzed in simulation and is successfully applied here to partition a swarm of underwater robots into groups demonstrating its adaptivity to changes and applicability in real world systems. In a turn towards the inspiration origins of the algorithm, three honeybee colonies are then studied for age-polyethism behaviors and the results are contrasted with a simulated swarm running the PSI algorithm. Similar effects are detected in both the biological and simulated swarms suggesting biological plausibility of the mechanisms employed by the artificial system.

Diet and endocrine effects on behavioral maturation-related gene expression in the pars intercerebralis of the honey bee brain.

Nervous and neuroendocrine systems mediate environmental conditions to control a variety of life history traits. Our goal was to provide mechanistic insights as to how neurosecretory signals mediate division of labor in the honey bee (Apis mellifera). Worker division of labor is based on a process of behavioral maturation by individual bees, which involves performing in-hive tasks early in adulthood, then transitioning to foraging for food outside the hive. Social and nutritional cues converge on endocrine factors to regulate behavioral maturation, but whether neurosecretory systems are central to this process is not known. To explore this, we performed transcriptomic profiling of a neurosecretory region of the brain, the pars intercerebralis (PI). We first compared PI transcriptional profiles for bees performing in-hive tasks and bees engaged in foraging. Using these results as a baseline, we then performed manipulative experiments to test whether the PI is responsive to dietary changes and/or changes in juvenile hormone (JH) levels. Results reveal a robust molecular signature of behavioral maturation in the PI, with a subset of gene expression changes consistent with changes elicited by JH treatment. In contrast, dietary changes did not induce transcriptomic changes in the PI consistent with behavioral maturation or JH treatment. Based on these results, we propose a new verbal model of the regulation of division of labor in honey bees in which the relationship between diet and nutritional physiology is attenuated, and in its place is a relationship between social signals and nutritional physiology that is mediated by JH.

Division of labour in honey bees: age- and task-related changes in the expression of octopamine receptor genes.

The honey bee (Apis mellifera L.) has developed into an important ethological model organism for social behaviour and behavioural plasticity. Bees perform a complex age-dependent division of labour with the most pronounced behavioural differences occurring between in-hive bees and foragers. Whereas nurse bees, for example, stay inside the hive and provide the larvae with food, foragers leave the hive to collect pollen and nectar for the entire colony. The biogenic amine octopamine appears to play a major role in division of labour but the molecular mechanisms involved are unknown. We here investigated the role of two characterized octopamine receptors in honey bee division of labour. AmOctαR1 codes for a Ca(2+) -linked octopamine receptor. AmOctβR3/4 codes for a cyclic adenosine monophosphate-coupled octopamine receptor. Messenger RNA expression of AmOctαR1 in different brain neuropils correlates with social task, whereas expression of AmOctβR3/4 changes with age rather than with social role per se. Our results for the first time link the regulatory role of octopamine in division of labour to specific receptors and brain regions. They are an important step forward in our understanding of complex behavioural organization in social groups.

Birth weight and sucrose responsiveness predict cognitive skills of honeybee foragers

Honeybees, Apis mellifera , can differ considerably in their birth weights but the consequences of these weight differences for behaviour are unknown. I investigated how these birth weight differences affected their cognitive skills when the bees reached foraging age. Individual sucrose responsiveness measured by the proboscis extension response is a strong determinant of appetitive olfactory learning performance in honeybees. Most of the observed learning differences between individuals or between genetic bee strains correlate with differences in their sucrose responsiveness. My second aim was therefore to investigate whether the sucrose responsiveness of newly emerged bees could predict the learning behaviour of the bees 3 weeks later. Both birth weight and sucrose responsiveness measured at emergence could predict olfactory learning scores as demonstrated by significant positive correlations. Heavy bees and bees with high sucrose responsiveness later learned better than lighter individuals or bees with lower responsiveness to sucrose at emergence. These results demonstrate for the first time a fundamental relationship between sensory responsiveness and morphology at emergence and later cognitive skills in insects. Because sensory responsiveness is closely linked to division of labour in honeybees, differences in weight and sucrose responsiveness at emergence might be involved in regulating division of labour. ► I studied the relationship of birth weight, sensitivity and learning in honeybees. ► Heavy newly emerged bees learned better in later life than lighter bees. ► Sucrose-sensitive bees learned better at foraging age than insensitive bees.

The involvement of the antennae in mediating the brood influence on circadian rhythms in “nurse” honey bee (Apis mellifera) workers

Age-related division of labor in honey bees is associated with plasticity in circadian rhythms. Forager bees that are typically older than 3weeks of age show strong behavioral and molecular circadian rhythms with higher activity during the day. Younger bees that typically care for (“nurse”) the brood are active around the clock with similar brain clock gene levels throughout the day. However, nurses that are caged on brood-less combs inside or outside the hive show robust circadian rhythms with higher activity during the day, suggesting that direct contact with the brood mediates the plasticity in the circadian system. The nature of the brood signals affecting the workers’ circadian system and the modalities by which they are detected are unknown. Given that the antennae are pivotal sensory organs in bees, we hypothesized that they are involved in mediating the brood influence on the plasticity in circadian rhythms. The flagella of the antennae are densely covered with diverse sensory structures able to detect a wide range of signals. To test our hypothesis, we removed the flagella of nurses and observed their behavior in isolation and in free-foraging colonies. We found that individually-isolated flagella-less bees under constant laboratory conditions show robust circadian rhythms in locomotor activity. In observation hives, flagella-less bees cared for the brood, but were more active during the day. By contrast, sham-treated bees were active around the clock as typical of nurses. Detailed video recordings showed that the brood-tending behavior of flagella-less and sham-treated bees is similar. These observations suggest that the difference in the patterns of brood care activity is not because the flagella-less bees did not contact the brood. Our results suggest that nurses are able to find the brood in the dark environment of the hive without their flagella, perhaps by using other sensory organs. The higher activity of flagella-less bees during the day further suggests that the flagella are involved in mediating the brood signals modulating plasticity in the circadian system.

Individual-level patterns of division of labor in honeybees highlight flexibility in colony-level developmental mechanisms

Honeybee division of labor (DOL) has become a model system for exploring the genetic basis of complex traits and phenotypic plasticity. Although many highly informative behavioral studies have been conducted on this topic (both at the cohort and individual levels), most studies have focused on a few behavioral acts, such as the age of first foraging. Few studies have recorded large numbers of relatively complete individual-level patterns of DOL. Such fine-scale patterns would lay the foundation for rigorous molecular analyses of this phenomenon and allow us to differentiate between competing mechanistic models of DOL. Here, we record over 100 individual-level DOL patterns of bees living under natural conditions. We found that the transitions between castes (polyphenism states) are often gradual, with bees being in multiple castes at once. This is contrary to the traditional view that changes are abrupt. We also found that bees often skip castes, a key prediction of a recent model of DOL. We further confirm variation in the rate at which bees pass through castes and the age of first foraging. Taken together, these results greatly improve our understanding of this model system and allow for a strong revision of current models of honeybee DOL.

The transcription factor Krüppel homolog 1 is linked to hormone mediated social organization in bees.

BackgroundRegulation of worker behavior by dominant queens or workers is a hallmark of insect societies, but the underlying molecular mechanisms and their evolutionary conservation are not well understood. Honey bee and bumble bee colonies consist of a single reproductive queen and facultatively sterile workers. The queens' influences on the workers are mediated largely via inhibition of juvenile hormone titers, which affect division of labor in honey bees and worker reproduction in bumble bees. Studies in honey bees identified a transcription factor, Krüppel-homolog 1 (Kr-h1), whose expression in worker brains is significantly downregulated in the presence of a queen or queen pheromone and higher in forager bees, making this gene an ideal candidate for examining the evolutionary conservation of socially regulated pathways in Hymenoptera.ResultsIn contrast to honey bees, bumble bees foragers do not have higher Kr-h1 levels relative to nurses: in one of three colonies levels were similar in nurses and foragers, and in two colonies levels were higher in nurses. Similarly to honey bees, brain Kr-h1 levels were significantly downregulated in the presence versus absence of a queen. Furthermore, in small queenless groups, Kr-h1 levels were downregulated in subordinate workers with undeveloped ovaries relative to dominant individuals with active ovaries. Brain Kr-h1 levels were upregulated by juvenile hormone treatment relative to a vehicle control. Finally, phylogenetic analysis indicates that KR-H1 orthologs are presence across insect orders. Though this protein is highly conserved between honey bees and bumble bees, there are significant differences between orthologs of insects from different orders.ConclusionsOur results suggest that Kr-h1 is associated with juvenile hormone mediated regulation of reproduction in bumble bees. The expression of this transcription factor is inhibited by the queen and associated with endocrine mediated regulation of social organization in two species of bees. Thus, KR-H1 may transcriptionally regulate a conserved genetic module that is part of a pathway that has been co-opted to function in social behavior, and adjusts the behavior of workers to their social environmental context.

Nutritional regulation of division of labor in honey bees: toward a systems biology perspective

Organisms adapt their behavior and physiology to environmental conditions through processes of phenotypic plasticity. In one well-studied example, the division of labor among worker honey bees involves a stereotyped yet plastic pattern of behavioral and physiological maturation. Early in life, workers perform brood care and other in-hive tasks and have large internal nutrient stores; later in life, they forage for nectar and pollen outside the hive and have small nutrient stores. The pace of maturation depends on colony conditions, and the environmental, physiological, and genomic mechanisms by which this occurs are being actively investigated. Here we review current knowledge of the mechanisms by which a key environmental variable, nutritional status, influences worker honey bee division of labor. These studies demonstrate that changes in individual nutritional status and conserved food-related molecular and hormonal pathways regulate the age at which individual bees begin to forage. We then outline ways in which systems biology approaches, enabled by the sequencing of the honey bee genome, will allow researchers to gain deeper insight into nutritional regulation of honey bee behavior, and phenotypic plasticity in general.

Division of labor in honeybees: form, function, and proximate mechanisms

Honeybees exhibit two patterns of organization of work. In the spring and summer, division of labor is used to maximize growth rate and resource accumulation, while during the winter, worker survivorship through the poor season is paramount, and bees become generalists. This work proposes new organismal and proximate level conceptual models for these phenomena. The first half of the paper presents a push–pull model for temporal polyethism. Members of the nursing caste are proposed to be pushed from their caste by the development of workers behind them in the temporal caste sequence, while middle-aged bees are pulled from their caste via interactions with the caste ahead of them. The model is, hence, an amalgamation of previous models, in particular, the social inhibition and foraging for work models. The second half of the paper presents a model for the proximate basis of temporal polyethism. Temporal castes exhibit specialized physiology and switch caste when it is adaptive at the colony level. The model proposes that caste-specific physiology is dependent on mutually reinforcing positive feedback mechanisms that lock a bee into a particular behavioral phase. Releasing mechanisms that relate colony level information are then hypothesized to disrupt particular components of the priming mechanisms to trigger endocrinological cascades that lead to the next temporal caste. Priming and releasing mechanisms for the nursing caste are mapped out that are consistent with current experimental results. Less information-rich, but plausible, mechanisms for the middle-aged and foraging castes are also presented.