Task-specific expression of the foraging gene in harvester ants

In social insects, groups of workers perform various tasks such as brood care and foraging. Transitions in workers from one task to another are important in the organization and ecological success of colonies. Regulation of genetic pathways can lead to plasticity in social insect task behaviour. The colony organization of advanced eusocial insects evolved independently in ants, bees, and wasps and it is not known whether the genetic mechanisms that influence behavioural plasticity are conserved across species. Here we show that a gene associated with foraging behaviour is conserved across social insect species, but the expression patterns of this gene are not. We cloned the red harvester ant (Pogonomyrmex barbatus) ortholog (Pbfor) to foraging, one of few genes implicated in social organization, and found that foraging behaviour in harvester ants is associated with the expression of this gene; young (callow) worker brains have significantly higher levels of Pbfor mRNA than foragers. Levels of Pbfor mRNA in other worker task groups vary among harvester ant colonies. However, foragers always have the lowest expression levels compared to other task groups. The association between foraging behaviour and the foraging gene is conserved across social insects but ants and bees have an inverse relationship between foraging expression and behaviour.     

Individual experience alone can generate lasting division of labor in ants

Division of labor, the specialization of workers on different tasks, largely contributes to the ecological success of social insects [1, 2]. Morphological, genotypic, and age variations among workers, as well as their social interactions, all shape division of labor [1-12]. In addition, individual experience has been suggested to influence workers in their decision to execute a task [13-18], but its potential impact on the organization of insect societies has yet to be demonstrated [19, 20]. Here we show that, all else being equal, ant workers engaged in distinct functions in accordance with their previous experience. When individuals were experimentally led to discover prey at each of their foraging attempts, they showed a high propensity for food exploration. Conversely, foraging activity progressively decreased for individuals who always failed in the same situation. One month later, workers that previously found prey kept on exploring for food, whereas those who always failed specialized in brood care. It thus appears that individual experience can strongly channel the behavioral ontogeny of ants to generate a lasting division of labor. This self-organized task-attribution system, based on an individual learning process, is particularly robust and might play an important role in colony efficiency.     

Sucrose response thresholds of honey bee (Apis mellifera) foragers are not modulated by brood ester pheromone

Division of labor is a hallmark of eusocial insects and their ecological success can be attributed to it. Honey bee division of labor proceeds along a stereotypical ontogenetic path based on age, modulated by various internal and external stimuli. Brood pheromone is a major social pheromone of the honey bee that has been shown to affect honey bee division of labor. It elicits several physiological and behavioral responses; notably, regulating the timing of the switch from performing in-hive tasks to the initiation of foraging. Additionally, brood pheromone affects future foraging choice. In honey bees, sucrose response threshold is a physiological correlate of age of first foraging and foraging choice. Brood pheromone has been shown to modulate sucrose response threshold in young bees, but its effects on sucrose response thresholds of bees in advanced behavioral states (foragers) are not known. In this study we examined the sucrose response thresholds of two different task groups, foragers (pollen and non-pollen) and non-foraging bees, in response to honey bee brood pheromone. Sucrose response thresholds were not significantly different between brood pheromone treatment and controls among both non-pollen and pollen foragers. However, the sucrose response threshold of non-foraging bees was significantly higher in the brood pheromone treatment group than in the control group. The switch to foraging task is considered a terminal one, with honey bee lifespan being determined at least partially by risks and stress accompanying foraging. Our results indicate that foragers are physiologically resistant to brood pheromone priming of sucrose response thresholds.     

The gene vitellogenin has multiple coordinating effects on social organization

Temporal division of labor and foraging specialization are key characteristics of honeybee social organization. Worker honeybees (Apis mellifera) initiate foraging for food around their third week of life and often specialize in collecting pollen or nectar before they die. Variation in these fundamental social traits correlates with variation in worker reproductive physiology. However, the genetic and hormonal mechanisms that mediate the control of social organization are not understood and remain a central question in social insect biology. Here we demonstrate that a yolk precursor gene, vitellogenin, affects a complex suite of social traits. Vitellogenin is a major reproductive protein in insects in general and a proposed endocrine factor in honeybees. We show by use of RNA interference (RNAi) that vitellogenin gene activity paces onset of foraging behavior, primes bees for specialized foraging tasks, and influences worker longevity. These findings support the view that the worker specializations that characterize hymenopteran sociality evolved through co-option of reproductive regulatory pathways. Further, they demonstrate for the first time how coordinated control of multiple social life-history traits can originate via the pleiotropic effects of a single gene that affects multiple physiological processes.     

The Gene vitellogenin Has Multiple Coordinating Effects on Social Organization

Temporal division of labor and foraging specialization are key characteristics of honeybee social organization. Worker honeybees (Apis mellifera) initiate foraging for food around their third week of life and often specialize in collecting pollen or nectar before they die. Variation in these fundamental social traits correlates with variation in worker reproductive physiology. However, the genetic and hormonal mechanisms that mediate the control of social organization are not understood and remain a central question in social insect biology. Here we demonstrate that a yolk precursor gene, vitellogenin, affects a complex suite of social traits. Vitellogenin is a major reproductive protein in insects in general and a proposed endocrine factor in honeybees. We show by use of RNA interference (RNAi) that vitellogenin gene activity paces onset of foraging behavior, primes bees for specialized foraging tasks, and influences worker longevity. These findings support the view that the worker specializations that characterize hymenopteran sociality evolved through co-option of reproductive regulatory pathways. Further, they demonstrate for the first time how coordinated control of multiple social life-history traits can originate via the pleiotropic effects of a single gene that affects multiple physiological processes.     

Nutrition and division of labor: Effects on foraging and brain gene expression in the paper wasp Polistes metricus

Deeply conserved molecular mechanisms regulate food-searching behaviour in response to nutritional cues in a wide variety of vertebrates and invertebrates. Studies of the highly eusocial honey bee have shown that nutritional physiology and some conserved nutrient signalling pathways, especially the insulin pathway, also regulate the division of labour between foraging and non-foraging individuals. Typically, lean workers leave the nest to forage for food, and well-nourished workers perform tasks inside the nest. Here we provide the first direct test of whether similar mechanisms operate in a primitively eusocial insect in an independently evolved social lineage, the paper wasp Polistes metricus. We found that food deprivation caused reduced lipid stores and higher levels of colony and individual foraging. Individuals with greatly reduced lipid stores foraged at extremely elevated levels. In addition, brain expression of several foraging-related genes was influenced by food deprivation, including insulin-like peptide 2 (ilp2). Together with previous findings, our results demonstrate that nutrition regulates foraging division of labour in two independently evolved social insect lineages (bees and wasps), despite large differences in social organization. Our results also provide additional support for the idea that nutritional asymmetries among individuals, based on differences in nutritional physiology and expression of conserved nutrient signalling genes in the brain, are important in the division of labour in eusocial societies.     

The curious case of aging plasticity in honey bees

As in all advanced insect societies, colony-organization in honey bees emerges through a structured division of labor between essentially sterile helpers called workers. Worker bees are sisters that conduct all social tasks except for egg-laying, for example nursing brood and foraging for food. Curiously, aging progresses slowly in workers that engage in nursing and even slower when bees postpone nursing during unfavorable periods. We, therefore, seek to understand how senescence can emerge as a function of social task performance. The alternative utilization of a common yolk precursor protein (vitellogenin) in nursing and somatic maintenance can link behavior and aging plasticity in worker bees. Beneficial effects of vitellogenin may also be mediated by inhibitory action on juvenile hormone and insulin-like signaling.     

Specialization Does Not Predict Individual Efficiency in an Ant

The ecological success of social insects is often attributed to an increase in efficiency achieved through division of labor between workers in a colony. Much research has therefore focused on the mechanism by which a division of labor is implemented, i.e., on how tasks are allocated to workers. However, the important assumption that specialists are indeed more efficient at their work than generalist individuals—the “Jack-of-all-trades is master of none” hypothesis—has rarely been tested. Here, I quantify worker efficiency, measured as work completed per time, in four different tasks in the ant Temnothorax albipennis: honey and protein foraging, collection of nest-building material, and brood transports in a colony emigration. I show that individual efficiency is not predicted by how specialized workers were on the respective task. Worker efficiency is also not consistently predicted by that worker''s overall activity or delay to begin the task. Even when only the worker''s rank relative to nestmates in the same colony was used, specialization did not predict efficiency in three out of the four tasks, and more specialized workers actually performed worse than others in the fourth task (collection of sand grains). I also show that the above relationships, as well as median individual efficiency, do not change with colony size. My results demonstrate that in an ant species without morphologically differentiated worker castes, workers may nevertheless differ in their ability to perform different tasks. Surprisingly, this variation is not utilized by the colony—worker allocation to tasks is unrelated to their ability to perform them. What, then, are the adaptive benefits of behavioral specialization, and why do workers choose tasks without regard for whether they can perform them well? We are still far from an understanding of the adaptive benefits of division of labor in social insects.     

Division of Labor Associated with Brood Rearing in the Honey Bee: How Does It Translate to Colony Fitness?

Division of labor is a striking feature observed in honey bees and many other social insects. Division of labor has been claimed to benefit fitness. In honey bees, the adult work force may be viewed as divided between non-foraging hive bees that rear brood and maintain the nest, and foragers that collect food outside the nest. Honey bee brood pheromone is a larval pheromone that serves as an excellent empirical tool to manipulate foraging behaviors and thus division of labor in the honey bee. Here we use two different doses of brood pheromone to alter the foraging stimulus environment, thus changing demographics of colony division of labor, to demonstrate how division of labor associated with brood rearing affects colony growth rate. We examine the effects of these different doses of brood pheromone on individual foraging ontogeny and specialization, colony level foraging behavior, and individual glandular protein synthesis. Low brood pheromone treatment colonies exhibited significantly higher foraging population, decreased age of first foraging and greater foraging effort, resulting in greater colony growth compared to other treatments. This study demonstrates how division of labor associated with brood rearing affects honey bee colony growth rate, a token of fitness.     

Sensory response system of social behavior tied to female reproductive traits

Background

Honey bees display a complex set of anatomical, physiological, and behavioral traits that correlate with the colony storage of surplus pollen (pollen hoarding). We hypothesize that the association of these traits is a result of pleiotropy in a gene signaling network that was co-opted by natural selection to function in worker division of labor and foraging specialization. By acting on the gene network, selection can change a suite of traits, including stimulus/response relationships that affect individual foraging behavior and alter the colony level trait of pollen hoarding. The ‘pollen-hoarding syndrome’ of honey bees is the best documented syndrome of insect social organization. It can be exemplified as a link between reproductive anatomy (ovary size), physiology (yolk protein level), and foraging behavior in honey bee strains selected for pollen hoarding, a colony level trait. The syndrome gave rise to the forager-Reproductive Ground Plan Hypothesis (RGPH), which proposes that the regulatory control of foraging onset and foraging preference toward nectar or pollen was derived from a reproductive signaling network. This view was recently challenged. To resolve the controversy, we tested the associations between reproductive anatomy, physiology, and stimulus/response relationships of behavior in wild-type honey bees.

Methodology/Principal Findings

Central to the stimulus/response relationships of honey bee foraging behavior and pollen hoarding is the behavioral trait of sensory sensitivity to sucrose (an important sugar in nectar). To test the linkage of reproductive traits and sensory response systems of social behavior, we measured sucrose responsiveness with the proboscis extension response (PER) assay and quantified ovary size and vitellogenin (yolk precursor) gene expression in 6–7-day-old bees by counting ovarioles (ovary filaments) and by using semiquantitative real time RT-PCR. We show that bees with larger ovaries (more ovarioles) are characterized by higher levels of vitellogenin mRNA expression and are more responsive to sucrose solutions, a trait that is central to division of labor and foraging specialization.

Conclusions/Significance

Our results establish that in wild-type honey bees, ovary size and vitellogenin mRNA level covary with the sucrose sensory response system, an important component of foraging behavior. This finding validates links between reproductive physiology and behavioral-trait associations of the pollen-hoarding syndrome of honey bees, and supports the forager-RGPH. Our data address a current evolutionary debate, and represent the first direct demonstration of the links between reproductive anatomy, physiology, and behavioral response systems that are central to the control of complex social behavior in insects.     

Individual versus social complexity, with particular reference to ant colonies

Insect societies colonies of ants, bees, wasps and termites--vary enormously in their social complexity. Social complexity is a broadly used term that encompasses many individual and colony-level traits and characteristics such as colony size, polymorphism and foraging strategy. A number of earlier studies have considered the relationships among various correlates of social complexity in insect societies; in this review, we build upon those studies by proposing additional correlates and show how all correlates can be integrated in a common explanatory framework. The various correlates are divided among four broad categories (sections). Under 'polyphenism' we consider the differences among individuals, in particular focusing upon 'caste' and specialization of individuals. This is followed by a section on 'totipotency' in which we consider the autonomy and subjugation of individuals. Under this heading we consider various aspects such as intracolony conflict, worker reproductive potential and physiological or morphological restrictions which limit individuals' capacities to perform a range of tasks or functions. A section entitled 'organization of work' considers a variety of aspects, e.g. the ability to tackle group, team or partitioned tasks, foraging strategies and colony reliability and efficiency. A final section, 'communication and functional integration', considers how individual activity is coordinated to produce an integrated and adaptive colony. Within each section we use illustrative examples drawn from the social insect literature (mostly from ants, for which there is the best data) to illustrate concepts or trends and make a number of predictions concerning how a particular trait is expected to correlate with other aspects of social complexity. Within each section we also expand the scope of the arguments to consider these relationships in a much broader sense of'sociality' by drawing parallels with other 'social' entities such as multicellular individuals, which can be understood as 'societies' of cells. The aim is to draw out any parallels and common causal relationships among the correlates. Two themes run through the study. The first is the role of colony size as an important factor affecting social complexity. The second is the complexity of individual workers in relation to the complexity of the colony. Consequently, this is an ideal opportunity to test a previously proposed hypothesis that 'individuals of highly social ant species are less complex than individuals from simple ant species' in light of numerous social correlates. Our findings support this hypothesis. In summary, we conclude that, in general, complex societies are characterized by large colony size, worker polymorphism, strong behavioural specialization and loss of totipotency in its workers, low individual complexity, decentralized colony control and high system redundancy, low individual competence, a high degree of worker cooperation wher tackling tasks, group foraging strategies, high tempo, multi-chambered tailor-made nests, high functional integration, relatively greater use of cues and modulatory signals to coordinate individuals and heterogeneous patterns of worker-worker interaction.     

Social inhibition and the regulation of temporal polyethism in honey bees.

Honey bee division of labor is characterized by temporal polyethism, in which young workers remain in the hive and perform tasks there, whereas old workers perform more risky outside tasks, mainly foraging. We present a model of honey bee division of labor based on (1) an intrinsic process of behavioral development and (2) inhibition of development through social interactions among the workers in a colony. The model shows that these two processes can explain the main features of honey bee temporal polyethism: the correlation between age and task performance; the age at which a worker first forages and how this age varies among hives; the balanced allocation of workers to hive tasks and foraging; the recovery of a colony from demographic perturbations; and the differentiation of workers into different behavioral roles. The model provides a baseline picture of individual and colony behavior that can serve as the basis for studies of more fine-grained regulation of division of labor.     

Nutritional asymmetries are related to division of labor in a queenless ant

Eusocial species exhibit pronounced division of labor, most notably between reproductive and non-reproductive castes, but also within non-reproductive castes via morphological specialization and temporal polyethism. For species with distinct worker and queen castes, age-related differences in behavior among workers (e.g. within-nest tasks versus foraging) appear to result from physiological changes such as decreased lipid content. However, we know little about how labor is divided among individuals in species that lack a distinct queen caste. In this study, we investigated how fat storage varied among individuals in a species of ant (Dinoponera australis) that lacks a distinct queen caste and in which all individuals are morphologically similar and capable of reproduction (totipotent at birth). We distinguish between two hypotheses, 1) all individuals are physiologically similar, consistent with the possibility that any non-reproductive may eventually become reproductive, and 2) non-reproductive individuals vary in stored fat, similar to highly eusocial species, where depletion is associated with foraging and non-reproductives have lower lipid stores than reproducing individuals. Our data support the latter hypothesis. Location in the nest, the probability of foraging, and foraging effort, were all associated with decreased fat storage.     

Working-class royalty: bees beat the caste system

The struggle among social classes or castes is well known in humans. Here, we show that caste inequality similarly affects societies of ants, bees and wasps, where castes are morphologically distinct and workers have greatly reduced reproductive potential compared with queens. In social insects, an individual normally has no control over its own fate, whether queen or worker, as this is socially determined during rearing. Here, for the first time, we quantify a strategy for overcoming social control. In the stingless bee Schwarziana quadripunctata, some individuals reared in worker cells avoid a worker fate by developing into fully functional dwarf queens.     

Division of labour and seasonality in the ant Leptothorax albipennis: worker corpulence and its influence on behaviour

We address the organization of workers in social insect societies. We distinguish between changes in behavioural role over the nurse to forager role sequence, which may depend on changes in physiology, and potentially more rapid changes of task within role. We investigated the association between role and nutrient status in the ant Leptothorax albipennis. Worker lipid stores were quantified using a new body size-controlled method, and were related to worker behaviour. Worker lipid stores were evenly distributed amongst colony members at the end of winter, splitting rapidly into two distinct modes (replete nurses and lean foragers) in spring. The proportion of lean foragers increased throughout spring and summer, until most colonies contained only workers of this type. Callow workers then eclosed with intermediate lipid stores. We developed a computer vision system that tracks all nest ants to extract detailed behaviour of individuals of known lipid stores. Lipid storage was negatively correlated with a worker's foraging propensity, and with measures of spatial occupation in the nest and of activity. Different colonies showed a similar quantitative correlation between lipid stores and behavioural role, suggesting that lipid stores were not only correlated with the relative organization of individuals within each nest, but may also have influenced their absolute role. We reviewed the literature and found evidence that nutrient status influences role predisposition in social insect workers. We conclude that the distribution of worker roles may be linked to the balance between foraging income and energetic consumption within the colony directly via worker nutrient status. Copyright 2000 The Association for the Study of Animal Behaviour.     

Methoprene does not affect food preferences and foraging performance in honey bee workers

The fundamental determinants of division of labor among honey bee workers are age, genotype, and environment. These determinants work through intermediate physiological channels to realize particular patterns of division of labor. The change of juvenile hormone (JH) titer in worker bees is one such channel. Previous studies concentrated on the impact of JH on timing of in-hive and foraging activity. Here we examined the effects of JH on task specialization and the collection of pollen or nectar by same-age bees and we tested the possible impact on JH titer on foraging performance. Methoprene treatments were conducted after workers began to forage inside a flight room. We found that methoprene, a JH analogue, had no effect on preferences for pollen or nectar and, also, did not influence nectar foraging rate, nectar load size, and foraging span.     

Effects of selection for honey bee worker reproduction on foraging traits

The “reproductive ground plan” hypothesis (RGPH) proposes that reproductive division of labour in social insects had its antecedents in the ancient gene regulatory networks that evolved to regulate the foraging and reproductive phases of their solitary ancestors. Thus, queens express traits that are characteristic of the reproductive phase of solitary insects, whereas workers express traits characteristic of the foraging phase. The RGPH has also been extended to help understand the regulation of age polyethism within the worker caste and more recently to explain differences in the foraging specialisations of individual honey bee workers. Foragers that specialise in collecting proteinaceous pollen are hypothesised to have higher reproductive potential than individuals that preferentially forage for nectar because genes that were ancestrally associated with the reproductive phase are active. We investigated the links between honey bee worker foraging behaviour and reproductive traits by comparing the foraging preferences of a line of workers that has been selected for high rates of worker reproduction with the preferences of wild-type bees. We show that while selection for reproductive behaviour in workers has not altered foraging preferences, the age at onset of foraging of our selected line has been increased. Our findings therefore support the hypothesis that age polyethism is related to the reproductive ground plan, but they cast doubt on recent suggestions that foraging preferences and reproductive traits are pleiotropically linked.