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

Abstract

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.

Fig. 1

Apis mellifera has two systems of social organization: temporal polyethism in the spring and summer and generalist workers in the winter. Solid arrows indicate natural caste transitions, while the dashed arrows show atypical caste transitions (experimentally induced or due to swarming).The push–pull model for temporal polyethism proposes that nurses are pushed from their caste by the emergence of newly emerged bees, while the middle-aged bees are pulled into the foraging caste via interactions with the foragers. Members of all castes are assumed to be able to switch to the winter state under the appropriate conditions

Fig. 2

Nurses and middle-aged bees (MAB) have overlapping work zones within the nest, which, along with strong individual-level variation in development rate, led to confusion over whether they were two separate castes. Johnson (2008a, b) showed, using focal animal observations, that nurses and MAB have distinct task repertoires. Nurses stay within the brood nest where they care for brood, while middle-aged bees ignore the brood and focus on all the many other tasks in the nest. That nectar receiving is a key task of MAB, but not nurses, and is apparent by noting the difference in walking between the two castes. Nectar receivers make long circuits from the dance floor to the honeycombs at the top of the nest, while nurses do not leave the brood zone

Fig. 3

General proximate model for temporal polyethism. Caste-specific anatomy and physiology is generated via a multifactorial mutually reinforcing priming mechanism. Transitions between castes are controlled by releasers that break the reinforcing mechanism and trigger an endocrinological cascade to the next caste. This simple model explains why so many different factors can all cause a change in caste because a break anywhere in the mutually reinforcing cascade will trigger a transition to the next caste

Fig. 4

Model for the priming mechanisms of the nursing caste. The central behavior, brood feeding, exposes bees to queen mandibular gland pheromone (QMP) and brood pheromone (BP), two pheromones with multiple priming effects. BP primes bees for the physiological demands of nursing, while QMP makes them unlikely to leave the brood zone and perhaps unresponsive to non-brood-care task stimuli. There are three key releasing mechanisms: pollen availability, forager pheromones, and most important, the nurse to brood ratio (all shown in bold). These releasers relate colony level information to the individual and trigger the adaptive transition to the middle-aged bees' caste

Fig. 5

The proximate basis of the middle-aged bees' (MAB) caste is hypothesized to be a long endocrinological cascade that controls the rate at which MAB acquire the capacity to forage. Too little research has focused on the MAB caste to allow for a mechanism as detailed as for nurses. However, there are four basic processes triggered by the following events: decreased exposure to brood pheromone, decreased exposure to queen mandibular gland pheromone, exposure to novel task stimuli, and an endogenous rise in neurochemical titers unrelated to the priming feedback mechanisms. Question marks stress portions of this process that are particularly poorly understood