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Abstract: Division of labor in social groups can be influenced by differential nutrition. Consumption of more food or higher-quality food often affects individuals’ capacities for reproduction. In social insects, nutrients consumed during immature (e.g., larval) stages often affect adult reproductive capacity, but adult nutrition may also impact reproductive status. This study tested whether ovary development, an indicator of reproductive status, corresponded to higher trophic-level feeding for adults in the primitively eusocial paper wasp Mischocyttarus mastigophorus. Our main prediction was that females’ ovary development would correlate positively with evidence of feeding at higher trophic levels, as indicated by stable isotope ratios of nitrogen (δ15N) and carbon (δ13C). We first asked whether isotope ratios of mature females co-varied with ovary development. δ15N values were higher for mature females with better-developed ovaries, as expected if they fed on a diet richer in animal tissue. There was a negative relationship of δ13C with ovary development in mature females, as would be expected if females with developed ovaries had higher body lipid stores. To test for evidence of nutritional biasing of caste during immature development, we measured changes in isotope ratios across pupal development leading up to early adulthood (i.e., immediately before and after adult eclosion). The δ15N and δ13C values for mature pupae were similar to those of newly emerged adults and to those of mature adults lacking developed ovaries. In contrast, mature females with developed ovaries showed N-isotope signatures of a more prey-based diet and C-isotope signatures of elevated lipid content. We conclude the N and C isotopic signatures of ovary-developed mature females diverged from their levels at the end of immature development. The findings suggest reproductive caste status was associated with differences in nutrient acquisition and reflects differences in consumption of animal-derived versus plant-based foods during adulthood.Significance statement: Pre-adult nutrition is known to affect caste development, and thereby influence division of labor, in diverse insect societies. In temperate independent-founding (IF) paper wasps, the effects of larval nutrition on adult caste may reflect adaptations for overwintering and diapause by reproductive females. We asked whether adult nutritional content showed caste-related trophic differences in the Neotropical IF paper wasp Mischocyttarus mastigophorus. Previous studies suggested interactions among adult nest-mates affected food sharing and caused biased nutrient flow within colonies. Our data suggest adult nutrition affected reproductive physiology. We propose this pattern may be widespread in tropical IF paper wasps, where opportunities for adult reproductive plasticity are favored by long colony cycles and relatively aseasonal nest founding. [ABSTRACT FROM AUTHOR]

Dominance interactions affected patterns of non-reproductive division of labor (polyethism) in the eusocial wasp Mischocyttarus mastigophorus. Socially dominant individuals foraged for food (nectar and insect prey) at lower rates than subordinate individuals. In contrast, dominant wasps performed most of the foraging for the wood pulp used in nest construction. Social dominance also affected partitioning of materials collected by foragers when they returned to the nest. Wood pulp loads were never shared with nest mates, while food loads, especially insect prey, were often partitioned with other wasps. Dominant individuals on the nest were more likely to take food from arriving foragers than subordinate individuals. The role of dominance interactions in regulating polyethism has evolved in the eusocial paper wasps (Polistinae). Both specialization by foragers and task partitioning have increased from basal genera (independent-founding wasps, including Mischo-cyttarus spp.) to more derived genera (swarm-founding Epiponini). Dominance interactions do not regulate forager specialization or task partitioning in epiponines. I hypothesize that these changes in polyethism were enabled by the evolution of increased colony size in the Epiponini. [ABSTRACT FROM AUTHOR]

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. [ABSTRACT FROM AUTHOR]

Age polyethism is widespread among social insects and, as a rule, safe tasks are performed by workers earlier in life than are risky ones. Mathematical models were used to compare expected longevity of workers in colonies with and without age polyethism. The results of the models suggest that if aging does not depend on activity then age polyethism is profitable when safer tasks are performed earlier in life. If, however, aging depends on activity, age polyethism is profitable when safer tasks are performed earlier in life and if they are associated with higher aging-related mortality. On the other hand, age polyethism is not profitable if safer tasks are performed later in life, and if they are associated with lower aging-related mortality. Furthermore, if there is no aging, then age polyethism does not bring any benefits. Electronic supplementary material to this paper can be obtained by using the Springer Link server located at http://dx.doi.org/10.1007/s00265-001-0429-z [ABSTRACT FROM AUTHOR]

A well-regulated division of labor has been one of the core adaptations leading to the success of the social insects. Honeybee division of labor has been classically viewed as a sequence of age-related changes in task performance. Kolmes questioned this view arguing that his studies did not support the existence of any age-related within-nest specialization. To resolve this controversy, Kolmes and Seeley conducted a joint study with mixed results. They found support for a cell cleaning caste, but diverged on whether their results supported distinct nursing and middle age castes. In this paper, I follow up on their work to resolve the question of caste number in within-nest honey bees. To determine whether nurses (typically aged 4–12 days) and middle-aged bees (aged 12–20 days) have distinct task repertoires, I conducted focal animal observations on a large number of workers in both age groups working within the same nests at the same time. The results support their being two castes of within-nest bees. Young bees specialized on brood care tasks, while middle-aged bees specialized on nectar processing and nest maintenance. Middle-aged bees were observed caring for brood in less than 1% of the observations. Moreover, both castes exhibited movement patterns that correspond to the traditional view that nurses stay within the broodnest, while middle-aged bees move around a great deal in search of work throughout the nest. A review of studies conducted since the debate of Seeley and Kolmes supports the reliability of these results. This work has relevance for proximate models of temporal polyethism, as it is often assumed by such models that there is only one within-nest caste in the honeybee. [ABSTRACT FROM AUTHOR]

A number of hypotheses have been proposed to explain the evolution of multiple mating in the honeybee queen. In particular, the consequences of reduced intracolonial relatedness provide plausible explanations for multiple mating with up to ten drones, but fail to account for the much higher mating frequencies observed in nature. In this paper, we propose an alternative mechanism which builds on non-linear relationships between intracolonial frequencies in genotypic worker specialization and colony fitness. If genes for any worker specialization confer an advantage on colony fitness only when they are rare, this would require a stable mix of sperm from a few drones which contribute that trait, and many which do not. To ensure both specific, low within-colony proportions of “rare specialist” genes, and to reduce random variation of these proportions would require mating with high numbers of drones. The quantitative implementation shows that moderate to very high numbers of matings are required to exploit colony advantages from genotypic allocation of workers to rare tasks. Extreme polyandry thus could result from colony selection dependent on the intracolonial frequency of rare genetic specialists. [ABSTRACT FROM AUTHOR]

The caterpillars of Eucheira socialis westwoodi cooperatively spin and maintain a hollow silken nest and an elaborate network of silken foraging trails on their host plant, madrone ( Arbutus spp.: Ericaceae). Nests typically contain several hundred larvae. Two populations are known to harbor a sex ratio distorter. The primary sex ratio in these two populations for four generations has been exceedingly male biased (64–79% male). Lepidoptera larvae are easily sexed using external morphology, allowing us to uniquely mark male and female larvae and to assemble larval groups of particular sex ratios. We report here the results of experiments on sex-specific larval behavior and physiology and the effect of colony sex ratio on individual behavior. We found that male larvae spent more time spinning silk on the nest and less time feeding than female larvae. Males were the first to emerge from the nest and the first to venture out along trails to feed. Male-biased nests had a significantly greater amount of silk deposited on their surfaces than female-biased nests. In the field, male-biased nests produced heavier male and female pupae than female-biased nests. Male and female larvae in 75% male nests became active earlier than males and females in other sex ratio treatments. [ABSTRACT FROM AUTHOR]

Mature colonies of many social insect species exhibit division of labor (DOL) where individual workers specialize in doing only a subset of the multiple tasks needed to maintain homeostasis. In newly initiated ant colonies, however, the first workers (called nanitics) are few in number and much smaller in size than those in mature colonies. This limited workforce must perform most of the tasks of mature colonies, but it is unknown if they also exhibit DOL. In this study, we tracked several inside-nest and outside-nest behaviors of nanitics in incipient Pogonomyrmex rugosus colonies. DOL arises in these colonies, whereby the relatively oldest workers (even if only by a few hours) are biased towards foraging, while younger nanitics concentrate on brood care. The addition of new nanitics shifts behavior in the oldest individual away from brood care but does not immediately increases its foraging. Conversely, nanitics left alone due to mortality of nest-mates forage more, but do not reduce brood care. The results suggest P. rugosus nanitics follow an age-related task specialization pattern that is broadly similar to mature colonies. The nanitic life stage may be, however, unique for ants in how fine-grained the DOL is in terms of absolute age differences and flexibility for task switching. Significance statement: The ecological success of ants is thought to be facilitated by workers dividing their labor across tasks. Commonplace in mature colonies is that individuals will perform safer, within-nest tasks such as brood care when young, and shift as they age towards riskier, outside-nest tasks such as foraging. Because many do the same task, the death of any single worker has minimal effect. We show, for the first time, a similar age-related, task specialization pattern also occurs in newly founded colonies. In this earliest life, history stage workers are small and few in number, precluding the massive task redundancy that characterizes mature colonies. Nevertheless, a division of labor correlating with relative age differences arises even when workers differ in age by only a few hours. This supports the hypothesis that a similar developmental pathway for task allocation in worker behavior occurs at all stages in colony life history. [ABSTRACT FROM AUTHOR]

Task partitioning allows for efficient coordination of behavior in social insect colonies. Many task allocation studies focus on social insect species with discrete morphological worker subcastes, such as those possessing major and minor workers with strongly differentiated body plans. Much less is known about task partitioning among size-variable workers lacking discrete morphological subcastes. We investigated task fidelity and its correlation with worker size in Formica species with differing degrees of body size variation. During a mark-recapture study that focused on three worker tasks (honeydew collection, nest building, and protein foraging) across 2 days, 98.6% of 3570 recaptured workers exhibited task fidelity. In species with high levels of worker size variation, worker size is strongly correlated with task performance. This size-task correlation is weaker, but still present, in species with less variably sized workers. Our results suggest that Formica use size-based task partitioning, a form of morphological polyethism. We expect social insects with and without discrete morphological worker subcastes to differ in ontogeny, evolutionary history, and degree of behavioral flexibility. Identifying the scope of variation in task partitioning mechanisms will facilitate comparative studies, thereby elucidating evolutionary histories and outcomes of alternative strategies. Significance statement: Division of labor is thought to increase the efficiency and success of animal societies by allowing the performance of multiple tasks in parallel, rather than sequentially. We investigated the task partitioning strategy employed by an ecologically dominant ant genus characterized by continuous worker size variation but lacking discrete morphological worker subcastes. We show that several species employ a form of morphological polyethism, wherein individuals specialize in tasks according to body size. Size-mediated morphological polyethism in the absence of discrete morphological worker subcastes has been demonstrated in a few other social insects. However, this task allocation strategy is likely more common than previously recognized, as most insect societies display natural worker size variation. Further, we argue that it is important to distinguish between size- and subcaste-based morphological polyethism. Alternative task partitioning strategies are likely to impact animal societies' resilience to environmental perturbations, which are becoming increasingly common in the face of global change. [ABSTRACT FROM AUTHOR]

Division of labor in social insects has been explained by response threshold models which are based on differential responses to task-specific stimuli. In the present study, we argue that other types of stimuli, such as location-related cues, which are correlated with but not directly linked to task performance, may be significant. Using the black garden ant Lasius niger as a model, we focused on three groups of workers that perform extranidal tasks: (1) scouts, which explore new and unmarked areas remote from the nest; (2) patrollers, which are not recruited by other ants, but nonetheless walk outside in the nest vicinity; and (3) recruits, which are temporary foragers whose exit is triggered by recruitment. We used standardized tests to investigate, in a context-independent way, whether differences in task performance by these three groups could be correlated to intrinsic differences in their responsiveness to trail pheromone or to nest-related stimuli such as the presence of nestmates or colony odor. Overall, we found that the task profile of workers was correlated neither with their tendency to explore unmarked areas nor with their social attraction to nestmates. Scouts showed a lower attraction to colony odor and lower scores of trail following than recruits. Conversely, recruits were more attracted to colony chemical cues and showed lower response threshold to trail pheromone. Patrollers displayed behaviors between those of recruits and scouts. Our study thus shows that differences in ant responsiveness to location-related cues and recruitment trails contribute to the regulation of extranidal tasks in ants. Significance statement: Work organization in insect societies has been explained by models of differential response thresholds to stimuli that are directly linked to the performance of specific tasks. However, the task performance of individuals could also depend on their responsiveness to social and location-related cues that are correlated but not directly linked to these tasks. Using standardized context-independent tests, we found that scout ants, which explore unknown areas, display a lower responsiveness to colony area marking and trail pheromone. Conversely, recruits, which forage outside the nest only during food exploitation, are the most attracted to nestmates, colony area marking and trail pheromone. Patrollers display intermediate levels of attraction. Location-related cues could therefore play a role in determining the level of task performance by ants and should be taken into consideration in threshold models of task allocation. [ABSTRACT FROM AUTHOR]

Social insect workers modify task performance according to age-related schedules of behavioral development, and/or changing colony labor requirements based on flexible responses that may be independent of age. Using known-age minor workers of the ant Pheidole dentata throughout 68 % of their 140-day laboratory lifespan, we asked whether workers found inside or outside the nest differed in task performance and if behaviors were correlated with and/or causally linked to changes in brain serotonin (5HT) and dopamine (DA). Our results suggest that task performance patterns of individually assayed minors collected at these two spatially different worksites were independent of age. Outside-nest minors displayed significantly higher levels of predatory behavior and greater activity than inside-nest minors, but these groups did not differ in brood care or phototaxis. We examined the relationship of 5HT and DA to these behaviors in known-age minors by quantifying individual brain titers. Both monoamines did not increase significantly from 20 to 95 days of age. DA did not appear to directly regulate worksite location, although titers were significantly higher in outside-nest than inside-nest workers. Pharmacological depletion of 5HT did not affect nursing, predation, phototaxis, or activity. Our results suggest that worker task capabilities are independent of age beyond 20 days, and only predatory behavior can be consistently predicted by spatial location. This could reflect worker flexibility or variability in the behavior of individuals collected at each location, which could be influenced by complex interactions between age, worksite location, social interactions, neuromodulators, and other environmental and internal regulators of behavior. Significance statement: Physiological changes associated with worker age are considered to be important regulators of task performance in social insects. The extent to which worker age is correlated with behavior, and the degree to which developmental changes in neuromodulators control worker labor, however, are poorly understood. We found that ant workers are behaviorally flexible in respect to task performance at a given age, but differ in predatory response and activity level based on their worksite location (within or outside of the nest). Dopamine level was higher in outside-nest workers; serotonin did not appear to be causally linked to any behavior we examined. Our findings suggest that worker task performance can be independent of age, and workers maintain task efficacy throughout their lifespan while differing in some aspects of behavioral performance that may change with worksite location. Relationships between age, worksite, and neuromodulator titers appear to be complex. [ABSTRACT FROM AUTHOR]

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. Significance statement: 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. [ABSTRACT FROM AUTHOR]

Group size has profound effects on the organization of work. In the social insects, larger colony size is consistently associated with lower mass-specific energy use; similar hypometric relationships between group size and per-gram energy use may extend across other social taxa. The specific mechanisms driving social metabolic scaling vary among species, but evidence suggests that it can be associated with organizational changes in work (task) performance that allow more efficient energy use by larger groups. In social insect colonies, larger group size allows stronger individual specialization, greater diversity in task performance, and likely gives improved resilience to stochastic events. Larger colonies often also allocate a larger proportion of workers to maintenance and reserve rather than to foraging and brood care tasks, potentially reducing costs. For the few species examined, these organizational changes seem to be associated with lower mean but higher variance in movement rates, providing a concrete connection to metabolic use. Interestingly, colony group size is not generally associated with changes in the proportional number of colony workers resting versus doing work, but this may vary across social systems. Colonies with hypometric metabolic scaling tend to show constant or greater efficiency of brood production, consistent with efficiency rather than constraint-based scaling models. These patterns of work and energetics in social groups show distinct parallels with organismal scaling. Investigation into social metabolic scaling could contribute to identifying unifying scaling theories for the disparate fields of animal behavior, physiology, and human sociology. [ABSTRACT FROM AUTHOR]

Animals may face a tradeoff between enhanced cognitive ability and the cost of maintaining larger and more energetically expensive brains. In social species, this tradeoff could be influenced by energy-reducing benefits of cooperation and collective cognition. Greater social complexity in ants is hypothesized to be associated with smaller brain size, a pattern opposite that found in some social vertebrates. Ants vary in worker and colony size, and worker size-frequency distributions; larger workers have larger, more costly, brains. Colony-level foraging performance and its energetic consequence to fitness depend on individual cognitive capabilities as well as collective behaviors. To explore the impact of diet, behavioral ability, and social organization on brain evolution, we developed a model incorporating food availability, foraging behavior and related energetic gain, colony size, worker size and polymorphism, and brain size. Colonies could increase energy intake through foraging performance by increasing worker size, and by correlation, brain size and expanded task capability, or by increasing colony size and collective foraging. Results show that resource-poor environments favored small colonies of relatively large-bodied and thus large-brained pluripotent workers that had higher energetic costs. In contrast, large colonies of relatively small-bodied and small-brained workers in resource-rich environments harvested food with lower brain investment and hence decreased metabolic costs. Worker size-related behavioral specialization and covarying brain investment also influenced fitness. The energetic advantage of polymorphism depended on the degree of association of the navigational abilities employed during foraging and worker brain size. Our study suggests that diet, colony size, and worker size may influence tradeoffs between individual and collective cognition and the evolution of brain size and division of labor in eusocial insects such as ants. [ABSTRACT FROM AUTHOR]

Division of labor in insect societies relies on simple behavioral rules, whereby individual colony members respond to dynamic signals indicating the need for certain tasks to be performed. This in turn gives rise to colony-level phenotypes. However, empirical studies quantifying colony-level signal-response dynamics are lacking. Here, we make use of the unusual biology and experimental amenability of the queenless clonal raider ant Cerapachys biroi to jointly quantify the behavioral and physiological responses of workers to a social signal emitted by larvae. Using automated behavioral quantification and oocyte size measurements in colonies of different sizes and with different worker-to-larvae ratios, we show that the workers in a colony respond to larvae by increasing foraging activity and inhibiting ovarian activation in a progressive manner and that these responses are stronger in smaller colonies. This work adds to our knowledge of the processes that link plastic individual behavioral/physiological responses to colony-level phenotypes in social insect colonies. [ABSTRACT FROM AUTHOR]

Division of labor (DOL) in the social insects is one of nature's most derived examples of phenotypic plasticity. Here, we explore the regulatory genomics of DOL in honey bees using RNA-Seq between nurses and foragers for eight tissues. We begin to test the hypothesis that caste-specific gene expression may be controlled in a manner analogous to how sex-specific gene expression is controlled. Specifically, we look for candidate master caste regulators that could play a role in controlling caste-specific gene expression analogous to the role played by double sex in sex-specific gene expression. We make significant first steps towards testing this hypothesis by showing that only a small number of regulatory genes show widespread differential expression across many tissues and are thus candidates for genes that could coordinate widespread patterns of gene expression in response to endocrine signals responsive to social needs. Two strong candidates are kruppel homolog-1 and double sex. Double sex, in particular, has previously been associated with sex linked phenotypic plasticity in other insects and is a promising candidate for future work. In addition to testing this primary hypothesis, we also show that the control of DOL has a complex genetic basis such that the same regulatory genes are used repeatedly in different tissues at the same caste transition in an independent manner. We further show that most regulatory genes only show differential expression in a single tissue. Overall, this study suggests candidate genes for the key regulators of social behavior in honey bees. [ABSTRACT FROM AUTHOR]

Social insect colonies are often considered to be highly efficient collective systems, with division of labor at the root of their ecological success. However, in many species, a large proportion of a colony's workers appear to spend their time completely inactive. The role of this inactivity for colony function remains unclear. Here, we investigate how inactivity is distributed among workers and over time in the ant Temnothorax rugatulus. We show that the level of inactivity is consistent for individual workers, but differs significantly among workers, that is, some workers effectively specialize on 'inactivity'. We also show that workers have circadian rhythms, although intra-nest tasks tend to be performed uniformly across the whole day. Differences in circadian rhythms, or workers taking turns resting (i.e., working in shifts), cannot explain the observation that some workers are consistently inactive. Using extensive individual-level data to describe the overall structure of division of labor, we show that 'inactive workers' form a group distinct from other task groups. Hierarchical clustering suggests that inactivity is the primary variable in differentiating both workers and tasks. Our results underline the importance of inactivity as a behavioral state and the need for further studies on its evolution. [ABSTRACT FROM AUTHOR]

In many species of social insects, division of non-reproductive labor is to some extent affected by age, in that younger individuals engage in activities in the nest, whereas older individuals forage. While the link between age and task is less robust than originally thought, the transition from nursing to foraging is associated with large changes in gene expression, neuroanatomy, and physiology and therefore seems largely irreversible. Here, we investigate division of labor in the thelytokous ant Platythyrea punctata. Since it forms clonal colonies, it is an ideal model to investigate the behavioral flexibility of individuals and the proximate mechanisms underlying division of labor, while avoiding confounding factors, such as variation in genotype or morphology. We found that nurses and foragers of P. punctata differ in residual life span, fat content, fecundity, and the propensity to engage in dominance interactions. However, age-based division of labor appears to be flexible: foragers can revert to nursing and egg laying, even though they appear less fecund than original nurse workers. Interestingly, the transition from foraging to nursing seemed to slow down aging and senescence. [ABSTRACT FROM AUTHOR]

Senescence, the decline in physiological and behavioral function with increasing age, has been the focus of significant theoretical and empirical research in a broad array of animal taxa. Preeminent among invertebrate social models of aging are ants, a diverse and ecologically dominant clade of eusocial insects characterized by reproductive and sterile phenotypes. In this review, we critically examine selection for worker life span in ants and discuss the relationship between functional senescence, longevity, task performance, and colony fitness. We did not find strong or consistent support for the hypothesis that demographic senescence in ants is programmed, or its corollary prediction that workers that do not experience extrinsic mortality die at an age approximating their life span in nature. We present seven hypotheses concerning how selection could favor extended worker life span through its positive relationship to colony size and predict that large colony size, under some conditions, should confer multiple and significant fitness advantages. Fitness benefits derived from long worker life span could be mediated by increased resource acquisition, efficient division of labor, accuracy of collective decision-making, enhanced allomaternal care and colony defense, lower infection risk, and decreased energetic costs of workforce maintenance. We suggest future avenues of research to examine the evolution of worker life span and its relationship to colony fitness and conclude that an innovative fusion of sociobiology, senescence theory, and mechanistic studies of aging can improve our understanding of the adaptive nature of worker life span in ants. [ABSTRACT FROM AUTHOR]

Like organisms, cohesive social groups such as insect colonies grow from a few individuals to large and complex integrated systems. Growth is driven by the interplay between intrinsic growth rates and environmental factors, particularly nutritional input. Ecologically inspired population growth models assume that this relationship remains constant until maturity, but more recent models suggest that it should be less stable at small colony sizes. To test this empirically, we monitored worker population growth and fungal development in the desert leafcutter ant, Acromyrmex versicolor, over the first 6 months of colony development. As a multitrophic, symbiotic system, leafcutter colonies must balance efforts to manage both fungus production and the growth of the ants consuming it. Both ants and fungus populations grew exponentially, but the shape of this relationship transitioned at a size threshold of 89 ± 9 workers. Above this size, colony mortality plummeted and colonies shifted from hypometric to hypermetric growth, with a distinct stabilization of the relationship between the worker population and fungus. Our findings suggest that developing colonies undergo key changes in organizational structure and stability as they grow, with a resulting positive transition in efficiency and robustness. [ABSTRACT FROM AUTHOR]

Honey bee workers exhibit an age-based division of labor (temporal polyethism, DOL). Younger bees transition through sets of tasks within the nest; older bees forage outside. Components of temporal polyethism remain unrevealed. Here, we investigate the timing and pattern of pre-foraging behavior in distinct strains of bees to (1) determine if a general pattern of temporal DOL exists in honey bees, (2) to demonstrate a direct genetic impact on temporal pacing, and (3) to further elucidate the mechanisms controlling foraging initiation. Honey bees selected for differences in stored pollen demonstrate consistent differences in foraging initiation age. Those selected for increased pollen storage (high pollen hoarding strain, HSBs) initiate foraging earlier in life than those selected for decreased pollen storage (low pollen hoarding strain, LSBs). We found that HSBs both initiate and terminate individual pre-foraging tasks earlier than LSBs when housed in a common hive environment. Unselected commercial bees (wild type) generally demonstrated intermediate behavioral timing. There were few differences between genotypes for the proportion of pre-foraging effort dedicated to individual tasks, though total pre-foraging effort differences differed dramatically. This demonstrates that behavioral pacing can be accelerated or slowed, but the pattern of behavior is not fundamentally altered, suggesting a general pattern of temporal behavior in honey bees. This also demonstrates direct genetic control of temporal pacing. Finally, our results suggest that earlier HSB protein (pollen) consumption termination compared to LSBs may contribute to an earlier decline in hemolymph vitellogenin protein titers, which would explain their earlier onset of foraging. [ABSTRACT FROM AUTHOR]

In many social insects, including bumblebees, the division of labor between workers relates to body size, but little is known about the factors influencing larval development and final size. We confirmed and extend the evidence that in the bumblebee Bombus terrestris the adult bee body size is positively correlated with colony age. We next performed cross-fostering experiments in which eggs were switched between incipient (before worker emergence) and later stage colonies with workers. The introduced eggs developed into adults similar in size to their unrelated nestmates and not to their same-age full sisters developing in their mother colony. Detailed observations revealed that brood tending by the queen decreases, but does not cease, in young colonies with workers. We next showed that both worker number and the queen presence influenced the final size of the developing brood, but only the queen influence was mediated by shortening developmental time. In colonies separated by a queen excluder, brood developmental time was shorter in the queenright compartment. These findings suggest that differences in body size are regulated by the brood interactions with the queen and workers, and not by factors inside the eggs that could vary along with colony development. Finally, we developed a model showing that the typical increase in worker number and the decrease in brood contact with the queen can account for the typical increase in body size. Similar self-organized social regulation of brood development may contribute to the optimization of growth and reproduction in additional social insects. [ABSTRACT FROM AUTHOR]

The pollen hoarding syndrome consists of a large suite of correlated traits in honey bees that may have played an important role in colony organization and consequently the social evolution of honey bees. The syndrome was first discovered in two strains that have been artificially selected for high and low pollen hoarding. These selected strains are used here to further investigate the phenotypic and genetic links between two central aspects of the pollen hoarding syndrome: sucrose responsiveness and pollen hoarding. Sons of hybrid queen offspring of these two strains were tested for sucrose responsiveness and used to produce colonies with either a highly responsive or an unresponsive father. These two colony groups differed significantly in the amount of pollen stored on brood combs and with regard to their relationship between brood and pollen amounts. Additionally, four quantitative trait loci (QTL) for pollen hoarding behavior were assessed for their effect on sucrose responsiveness. Drone offspring of two hybrid queens were phenotyped for responsiveness and genotyped at marker loci for these QTL, identifying some pleiotropic effects of the QTL with significant QTL interactions. Both experiments thus provided corroborating evidence that the distinct traits of the pollen hoarding syndrome are mechanistically and genetically linked and that these links are complex and dependent on background genotype. The study demonstrates genetic worker-drone correlations within the context of the pollen hoarding syndrome and establishes that an indirect selection response connects pollen hoarding and sucrose responsiveness, regardless of which trait is directly selected. [ABSTRACT FROM AUTHOR]

How social insect colonies behave results from the actions of their workers. Individual variation among workers in their response to various tasks is necessary for the division of labor within colonies. A worker may be active in only a subset of tasks (specialist), perform all tasks (elite), or exhibit no particular pattern of task activity (idiosyncratic). Here we examine how worker activity is distributed among and within tasks in ants of the genus Temnothorax. We found that workers exhibited elitism within a situation, i.e., in particular sets of tasks, such as those associated with emigrations, nest building, or foraging. However, there was weak specialization for working in a particular situation. A few workers exhibited elitism across all situations, i.e., high performance in all tasks in all situations. Within any particular task, the distribution of activity among workers was skewed, with few ants performing most of the work and most ants performing very little of the work. We further found that workers persisted in their task preference over days, with the same individuals performing most of the work day after day. Interestingly, colonies were robust to the removal of these highly active workers; they were replaced by other individuals that were previously less active. This replacement was not short-lived; when the removed individuals were returned to the colony, not all of them resumed their prior high activity levels, and not all the workers that replaced them reduced their activity. Thus, even though some workers specialize in tasks within a particular situation and are persistent in performing them, task allocation in a colony is plastic and colonies can withstand removal of highly active individuals. [ABSTRACT FROM AUTHOR]

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. [ABSTRACT FROM AUTHOR]

Division of labor in social insects is determinant to their ecological success. Recent models emphasize that division of labor is an emergent property of the interactions among nestmates obeying to simple behavioral rules. However, the role of evolution in shaping these rules has been largely neglected. Here, we investigate a model that integrates the perspectives of self-organization and evolution. Our point of departure is the response threshold model, where we allow thresholds to evolve. We ask whether the thresholds will evolve to a state where division of labor emerges in a form that fits the needs of the colony. We find that division of labor can indeed evolve through the evolutionary branching of thresholds, leading to workers that differ in their tendency to take on a given task. However, the conditions under which division of labor evolves depend on the strength of selection on the two fitness components considered: amount of work performed and on worker distribution over tasks. When selection is strongest on the amount of work performed, division of labor evolves if switching tasks is costly. When selection is strongest on worker distribution, division of labor is less likely to evolve. Furthermore, we show that a biased distribution (like 3:1) of workers over tasks is not easily achievable by a threshold mechanism, even under strong selection. Contrary to expectation, multiple matings of colony foundresses impede the evolution of specialization. Overall, our model sheds light on the importance of considering the interaction between specific mechanisms and ecological requirements to better understand the evolutionary scenarios that lead to division of labor in complex systems. [ABSTRACT FROM AUTHOR]

Within-group conflict may influence the degree to which individuals within a group cooperate. For example, the most dominant individuals within a group often gain access to the best resources and may be less inclined to perform risky tasks. We monitored space use and division of labor among all workers in three colonies of bumblebees, Bombus impatiens, during the ergonomic and queenless phases of their colony cycle. We then measured the two largest oocytes in each worker to estimate each individual's reproductive potential at the end of the colony cycle. We show that workers that remained farther from the queen while inside the nest and avoided risky or more energy-expensive tasks during the ergonomic phase developed larger oocytes by the end of the colony cycle. These individuals also tended to be the largest, oldest workers. After the queen died, these workers were more likely than their nestmates to increase brood incubation. Our results suggest that inactive bumblebees may be storing fat reserves to later develop reproductive organs and that the spatial organization of workers inside the nest, particularly the distance workers maintain from the queen, may predict which individuals will later have the greatest reproductive potential in the colony. [ABSTRACT FROM AUTHOR]

Insect societies are important models for evolutionary biology and sociobiology. The complexity of some eusocial insect societies appears to arise from self-organized task allocation and group cohesion. One of the best-supported models explaining self-organized task allocation in social insects is the response threshold model, which predicts specialization due to inter-individual variability in sensitivity to task-associated stimuli. The model explains foraging task specialization among honeybee workers, but the factors underlying the differences in individual sensitivity remain elusive. Here, we propose that in honeybees, sensory sensitivity correlates with individual differences in the number of sensory structures, as it does in solitary species. Examining European and Africanized honeybees, we introduce and test the hypothesis that body size and/or sensory allometry is associated with foraging task preferences and resource exploitation. We focus on common morphological measures and on the size and number of structures associated with olfactory sensitivity. We show that the number of olfactory sensilla is greater in pollen and water foragers, which are known to exhibit higher sensory sensitivity, compared to nectar foragers. These differences are independent of the distribution of size within a colony. Our data also suggest that body mass and number of olfactory sensilla correlate with the concentration of nectar gathered by workers, and with the size of pollen loads they carry. We conclude that sensory allometry, but not necessarily body size, is associated with resource exploitation in honeybees and that the differences in number of sensilla may underlie the observed differences in sensitivity between bees specialized on water, pollen and nectar collection. [ABSTRACT FROM AUTHOR]

Division of labor is common across social groups. In social insects, many studies focus on the differentiation of in-nest and foraging workers and/or the division of foraging tasks. Few studies have specifically examined how workers divide in-nest tasks. In the bumble bee, Bombus impatiens, we have shown previously that smaller workers are more likely to feed larvae and incubate brood, whereas larger workers are more likely to fan or guard the nest. Here, we show that in spite of this, B. impatiens workers generally perform multiple tasks throughout their life. The size of this task repertoire size does not depend on body size, nor does it change with age. Further, individuals were more likely to perform the task they had been performing on the previous day than any other task, a pattern most pronounced among individuals who guarded the nest. On the other hand, there was no predictable sequence of task switching. Because workers tend to remain in the same region of the nest over time, in-nest workers may concentrate on a particular task, or subset of tasks, inside that region. This division of space, then, may be an important mechanism that leads to this weak specialization among in-nest bumble bee workers. [ABSTRACT FROM AUTHOR]

Polymorphism frequently correlates with specialized labor in social insects, but extreme morphologies may compromise behavioral flexibility and thus limit caste evolution. The ant genus Pheidole has dimorphic worker subcastes in which major workers appear limited due to their morphology to performing defensive or trophic functions, thus providing an ideal model to investigate specialization and plasticity. We examined worker morphology, brood-care flexibility, and subcaste ratio in 17 species of tropical twig-nesting Pheidole by quantifying nursing by major workers in natural colonies and in subcolonies lacking minors, in which we also measured brood survival and growth. Across species, majors performed significantly less brood care than minors in intact colonies, but increased rates of brood care 20-fold in subcolonies lacking minors. Brood nursed by majors had lower survival than brood tended by minors, although rates of brood growth did not vary between subcastes. Significant interspecific variation in rates of brood care by major workers did not lead to significant differences in brood growth or survival. Additionally, we did not find a significant association between the degree of major worker morphometric specialization and rates of nursing, growth, or survival of brood among species. Therefore, major workers showed reduced efficacy of brood care, but the degree of morphological specialization among species did not directly compromise task plasticity. The compact nests and all-or-nothing consequences of predation or disturbance on colony fitness may have influenced the evolution of major worker brood-care competency in twig-nesting Pheidole. [ABSTRACT FROM AUTHOR]

Here, we study distribution of workload and its relationship to colony size among worker ants of Temnothorax albipennis, in the context of colony emigrations. We find that one major aspect of workload, number of items transported by each worker, was more evenly distributed in larger colonies. By contrast, in small colonies, a small number of individuals perform most of the work in this task (in one colony, a single ant transported 57% of all items moved in the emigration). Transporters in small colonies carried more items to the new nest per individual and achieved a higher overall efficiency in transport (more items moved per transporter and unit time). Our results suggest that small colonies may be extremely dependent on a few key individuals. In studying colony organisation and division of labour, the amount of work performed by each individual, not just task repertoire (which tasks are performed at all), should be taken into account. [ABSTRACT FROM AUTHOR]

Honeybee colonies are highly integrated functional units characterized by a pronounced division of labor. Division of labor among workers is mainly age-based, with younger individuals focusing on in-hive tasks and older workers performing the more hazardous foraging activities. Thus, experimental disruption of the age composition of the worker hive population is expected to have profound consequences for colony function. Adaptive demography theory predicts that the natural hive age composition represents a colony-level adaptation and thus results in optimal hive performance. Alternatively, the hive age composition may be an epiphenomenon, resulting from individual life history optimization. We addressed these predictions by comparing individual worker longevity and brood production in hives that were composed of a single-age cohort, two distinct age cohorts, and hives that had a continuous, natural age distribution. Four experimental replicates showed that colonies with a natural age composition did not consistently have a higher life expectancy and/or brood production than the single-cohort or double-cohort hives. Instead, a complex interplay of age structure, environmental conditions, colony size, brood production, and individual mortality emerged. A general tradeoff between worker life expectancy and colony productivity was apparent, and the transition from in-hive tasks to foraging was the most significant predictor of worker lifespan irrespective of the colony age structure. We conclude that the natural age structure of honeybee hives is not a colony-level adaptation. Furthermore, our results show that honeybees exhibit pronounced demographic plasticity in addition to behavioral plasticity to react to demographic disturbances of their societies. [ABSTRACT FROM AUTHOR]

Empirical evidence suggests that division of labor in insect societies is positively related to group size both within and across taxa. Response threshold models (RTM) have been commonly used to analyze patterns of division of labor. However, these models have been explored empirically and theoretically for only a limited number of tasks, and few studies have examined predictions of the model as colony size and work availability change. We theoretically examine how group size influences division of labor using a fixed response-threshold model. We simultaneously explore how expected by-products of increased colony size, including demand (total work need relative to total work force available) and task number, affect this relationship. Our results indicate that both low demand and high task number positively influence division of labor. We suggest that these changes parallel what is observed within social groups as their size increases, and that, in part, the commonly observed increased division of labor with increasing group size is emergent. [ABSTRACT FROM AUTHOR]

A honeybee colony needs to divide its workforce so that each of the many tasks it performs has an appropriate number of workers assigned to it. This task allocation system needs to be flexible enough to allow the colony to quickly adapt to an ever-changing environment. In this study, we examined possible mechanisms by which a honeybee colony regulates the division of labor between scouts (foragers that search for new food sources without having been guided to them) and recruits (foragers that were guided via recruitment dances toward food sources). Specifically, we examined the roles that the availability of recruitment dances and worker genotype has in the colony-level regulation of the number of workers engaged in scouting. Our approach was threefold. We first developed a mathematical model to demonstrate that the decision to become a scout or a recruit could be regulated by whether a potential forager can find a recruitment dance within a certain time period. We then tested this model by investigating the effect of dance availability on the regulation of scouts in the field. Lastly, we investigated if the probability of being a scout has a genetic basis. Our field data supported the hypothesis that scouts are those foragers that have failed to locate a recruitment dance as predicted by our model, but we found no effect of genotype on the propensity of foragers to become scouts. [ABSTRACT FROM AUTHOR]

The controversy concerning the extent to which the organization of division of labor in social insects is a developmental process or is based on task allocation dynamics that emerge from colony need independent of worker age and endocrine or neural state has yet to be resolved. We present a novel analysis of temporal polyethism in the ant Pheidole dentata, demonstrating that task attendance by minor workers does not shift among spatially associated sets of behaviors that minimally overlap but rather expands with age. Our results show that the number of tasks performed by older minors increases through the addition and retention of behaviors, with up to a sixfold increase in repertoire size from day 1 to day 20 of adult life. We also show that older minors respond to colony needs by performing significantly more brood care as its demand increases, indicating that they can quickly upregulate nursing according to labor requirements. This level of plasticity was absent in younger siblings. The breadth of responsiveness to task-related olfactory stimuli increased with age. In a binary choice test in which young and old minor workers could orient toward odorants from brood or food, older workers responded to both brood and food, whereas young workers responded only to brood. These dissimilar responses to stimuli associated with nursing and foraging indicate age-related differences in sensory ability and provide a physiological basis for the age-related repertoire expansion model. We discuss repertoire expansion in P. dentata in light of behavioral development and caste flexibility in ants. [ABSTRACT FROM AUTHOR]

In temperate regions, older eusocial hymenopteran females with annual life cycles (annual-temperate) tend to dominate younger females, a behavior demonstrated by many Polistes. However, in queenless ponerine ants and primitively eusocial tropical wasps (perennial/tropical), a younger female can be dominant and occasionally takes over from the older, most dominant reproductive female, the alpha. We investigated these patterns using an inclusive fitness model. The most important difference between the above two cases lay in the length of individual life compared with colony life. Colonies dissolve before winter in the annual-temperate case, so the expected future tenure of the replacement alpha is never longer than that of the original alpha. This makes the non-reproductive subordinate tactic more advantageous for individuals that emerge later in the season because of the fitness cost of superseding. The perennial/tropical case does not have a clear upper limit for colony longevity, so the model predicts that late-born younger daughters are more likely to challenge their mother-alpha because of the expected long future tenure of the new alpha compared with the small indirect cost of the mother’s reproductive failure. To switch tactics from being a subordinate to being the new alpha is only optimal in some situations. The high mortality rate of subordinate workers does not qualitatively alter the above pattern. The specific sexual production schedule of the colony sometimes affects the optimal behavior of females in the perennial/tropical case, and older individuals can dominate younger ones when the end of current round of sexual production is imminent. [ABSTRACT FROM AUTHOR]

Division of labor is a key factor in the ecological success of social groups. Recent work suggests that division of labor can emerge even without specific adaptations for task specialization and that it can appear in incipient social groups as a self-organizational property. We investigated experimentally how selection and self-organization may interact during the evolution of division of labor by examining task performance in groups of normally solitary versus normally social ant queens. We created social pairs of colony-founding queens from two populations of the ant Pogonomyrmex californicus, one in which queens are normally solitary and one in which queens form foundress groups, and observed their behavior during nest excavation. In both populations, one of the two queens usually performed most of the excavation, becoming the excavation specialist. We could predict which queen would become the specialist based on their relative propensities to perform the task in other contexts, consistent with a variance-based model of task specialization. The occurrence of specialization even when group members were not adapted to social life suggests that division of labor may well have been present in incipient queen groups. However, division of labor can result in cost skew among group members, and thus, paradoxically, within-group selection may constrain or even reduce specialization. Consistent with this effect, pairs of normally solitary queens were significantly more asymmetrical in their task performance than normally social pairs, in which both queens nearly always performed the behavior to some degree. [ABSTRACT FROM AUTHOR]

The sponge-dwelling shrimp Synalpheus regalis and several congeners exhibit monogynous, eusocial colony structures, and field data suggest that these social species may have a competitive advantage in crowded environments. We explored mechanisms of colony defense, a likely contributor to such a social advantage, by measuring responses of resident shrimp to conspecific and heterospecific intruders in experimental nests. To test for behavioral differentiation among classes of individuals, we compared responses of juvenile, large male, and breeding female (queen) S. regalis to each intruder type. Colony residents discriminated nestmates from both foreign conspecific and heterospecific intruders, making more aggressive snaps and fewer contacts with such intruders than with controls from the same colony. S. regalis colonies also exhibited behavioral differentiation among classes of individuals: most snaps against intruders were by large males. Thus, large males defended the colony, allowing juveniles and the queen to feed and grow unmolested. On a per-individual basis, intruders more frequently contacted the queen than either large males or juveniles, possibly indicating that signals from the queen provide information about colony status as they do in many social insects. Sampling of unmanipulated field colonies showed that colony reproductive output increased linearly, by a factor of 177 times, throughout the range in sampled colony sizes (2–356 individuals), whereas average per capita reproductive output decreased by only 61% over the same range. These data suggest that non-breeding colony members may gain inclusive fitness benefits by remaining in and helping defend the natal sponge. Differentiation among individuals in reproductive and defensive behavior may enhance the efficiency and productivity of S. regalis colonies and contribute to their apparent competitive advantage over less social congeners. [ABSTRACT FROM AUTHOR]

The effect of demographic structure on disease resistance was studied in experimental colonies of the dampwood termite Zootermopsis angusticollis Hagen. Instar and group demography were found to be significant and independent predictors of susceptibility to infection after termites were exposed to 101–107 spores/ml suspension of the fungus Metarhizium anisopliae (or a spore-free medium) and subsequently maintained in isolation, or in homogeneous and heterogeneous instar groups. Nymphs, which were the oldest and largest individuals, had the highest survivorship. The youngest termites (instars III and IV) had approximately 3.6 and 2.0 times the hazard ratio of death of nymphs and were the most likely to succumb to disease. Termites in instar V had a hazard ratio of death 1.2-fold that of nymphs; termites in instar VI did not differ significantly from nymphs in susceptibility. Analysis of the survivorship patterns of each instar showed that (1) isolated termites exposed to fungal spores were significantly more susceptible to infection than similarly exposed individuals maintained in same-instar social groups, and (2) spore-exposed termites living in same-instar groups were significantly more susceptible to disease than similarly exposed individuals maintained in mixed-instar groups. Survivorship indices of spore-exposed termites in mixed-instar groups were the highest among all experimental treatments, approaching those of unexposed controls. Colony demography thus had a significant influence on individual survivorship and reduced mortality risk. Z. angusticollis colony demography results from the asynchronous development of termites which hatch during successive bouts of oviposition. We suggest that the demographic distribution of colony members produced by this overlap of generations reduces disease risk and is a previously unrecognized adaptive role of the caste distribution function. [ABSTRACT FROM AUTHOR]

Three experiments were conducted to explore the effects of severe food shortage on the control of two important and interrelated aspects of temporal division of labor in colonies of the honey bee ( Apis mellifera): the size and age distribution of a colony's foraging force. The experiments were conducted with single-cohort colonies, composed entirely of young bees, allowing us to quickly distinguish the development of new (precocious) foragers from increases in activity of bees already competent to forage. In experiment 1, colony food shortage caused an acceleration of behavioral development; a significantly greater proportion of bees from starved colonies than from fed colonies became precocious foragers, and at significantly younger ages. Temporal aspects of this starvation effect were further explored in experiment 2 by feeding colonies that we initially starved, and starving colonies that we initially fed. There was a significant decrease in the number of new foragers in starved colonies that were fed, detected 1 day after feeding. There also was a significant increase in the number of new foragers in fed colonies that were starved, but only after a 2-day lag. These results suggest that colony nutritional status does affect long-term behavioral development, rather than only modulate the activity of bees already competent to forage. In experiment 3, we uncoupled the nutritional status of a colony from that of the individual colony members. The behavior of fed individuals in starved colonies was indistinguishable from that of bees in fed colonies, but significantly different from that of bees in starved colonies, in terms of both the number and age distribution of foragers. These results demonstrate that effects of starvation on temporal polyethism are not mediated by the most obvious possible worker-nest interaction: a direct interaction with colony food stores. This is consistent with previous findings suggesting the importance of worker-worker interactions in the regulation of temporal polyethism in honey bees as well as other social insects. [ABSTRACT FROM AUTHOR]

Collective defense is one of the most ubiquitous behaviors performed by social groups. Because of its importance, complex societies may engage a set of defensive specialists, with physical and/or neurological attributes tuned for defense against specific invaders. These strategies must be balanced, however, with the need to flexibly respond to different threat levels and sources. Insect societies rely heavily on olfaction for detecting and communicating in the context of defense. We therefore asked whether threat detection via olfaction is specialized towards invader-specific cues and how this may be integrated into defense task specialization. Colonies of the stingless bee, Tetragonisca angustula, deploy a morphologically distinct sub-caste of larger-bodied workers (soldiers) for colony defense. These soldiers transition between two different guarding tasks as they age, progressing from guarding in a hovering position near the nest entrance to guarding in a standing position on the nest entrance tube. Hovering and standing guards intercept different types of invaders: primarily heterospecific versus conspecific, respectively. We asked whether hovering and standing guarding behaviors were modulated by differential sensitivity to invader-associated olfactory stimuli; then we compared their responses to these cues to those of smaller workers that perform predominantly non-defense tasks. We exposed bees under both field and lab conditions to citral, a kairomone produced by an obligate heterospecific nest robber, primarily intercepted by hovering guards. Consistent with their roles, hovering guards were more likely to move towards citral than were either standing guards or small-bodied bees within a Y-maze. We also presented guards at field nests with dummies of conspecific versus heterospecific invader types, varying whether they included citral odors. Standing guards were more responsive to conspecific intruder scenarios than hovering guards, but heterospecific response differed by presence of citral. Standing and hovering guards responded in similar proportions when citral was absent, but the addition of citral produced a marginally non-significant reduction in standing guard participation. Our results potentially demonstrate differentiated cue-specific responses that correspond to morphological task specialization and age polyethism in these eusocial societies. Significance statement: Group defense is a ubiquitous function of any society, but threats are often diverse. Though defense versus non-defense task specialization has been well studied, when and how individuals sub-specialize on particular threats is less understood. We asked how age-differentiated soldier sub-types in a stingless bee differ in their innate responsiveness to olfactory cues associated with nest invader type. Consistent with behavioral roles, younger soldiers were more innately reactive to odors of an obligate heterospecific parasite, and older soldiers were more reactive to odors of conspecific intruders. This suggests that either transitions in learning or discrete cue sensitivity mediate defensive sub-specialization. This is the first study to compare behavioral responsiveness to olfactory stimuli across age-specialized soldier sub-types. Results suggest benefits of flexible allocation and prompt further studies exploring the topic of defensive sub-specialization. [ABSTRACT FROM AUTHOR]

In social insects, within-colony worker diversity has long been thought to improve colony fitness. Recent studies start to question this assertion in species with moderate diversity. However, demonstrating an absence of effect is difficult as this absence could be due to the measurement of only few life history traits or to artificial conditions. In order to circumvent these limitations, we experimentally decreased worker size diversity within colonies of the ant Temnothorax nylanderi, with or without affecting mean worker size and we reintroduced them in the field for 4 months (spring and early summer). We then thoroughly measured their fitness based on survival, growth, and reproductive success. Our results show that our manipulation did not affect colony fitness. In addition, colonies did not restore diversity to its initial level, further suggesting that worker size diversity is not a key parameter to them. We found the classically observed positive relationship between colony size, colony growth, and reproductive success. Overall, our results confirm that worker size diversity within colony is not necessarily adaptive in species where it is moderate. We discuss the alternative mechanisms that could explain the evolutionary persistence of moderate worker size diversity. Significance statement: Organisms that live in groups can greatly benefit from the emergence of novel group-level traits. For instance, social insects show significant variability in worker size within colonies. This size diversity increases the division of labor among workers and improves colony fitness. However, in species where size diversity is moderate, this relationship may not always be verified. Here, we manipulated both worker size diversity and mean worker size within colonies of the ant Temnothorax nylanderi, we reintroduced them in the field, and we extensively measured colony fitness after 4 months. We found no impact on colony survival, growth, and reproduction. We discuss how social life and its associated cooperation and conflicts could cause variation in worker size, without any positive effect on colony fitness. [ABSTRACT FROM AUTHOR]

The ecological success of social insects is often attributed to their complex social organization and division of labor. Much previous work has investigated the extent to which individual workers within colonies specialize on certain tasks, which presumably increases colony efficiency. Fewer studies have investigated the extent to which individual biases for multiple related tasks adaptively shape division of labor. Here, we focus on honey bee (Apis mellifera) workers that perform hygienic behavior, the detection and removal of diseased larvae in order to reduce pathogen transmission within the hive. We individually marked workers observed performing this rare task and tracked their behavior over three days to fully characterize their task repertoires. We then compared the task repertoires of workers who specialized on hygienic behavior to generalist workers who occasionally perform hygienic behavior to identify additional task biases in hygienic specialists. We show that workers specialized in hygienic behavior are much more likely to also specialize in removing dead adult bodies from the hive, a task that is also associated with colony defense against disease. Our results demonstrate that individual specialization in one task can predict specialization in another related task. We argue these associations represent a type of specialization in multiple tasks that may be an important aspect of how insect colonies adaptively allocate their workers. Significance statement: Any animal group that divides up work among individuals faces the challenge of figuring out the best way to allocate workers towards certain tasks. One mechanism by which large groups can increase their efficiency is by utilizing specialized workers dedicated to a single task. However, it has also been suggested that if multiple tasks require similar skills or are spatially associated with one another, then group efficiency can be further increased by using the same set of workers to perform those tasks as well. Here, we show that honey bee workers specialized in removing dead larvae from the brood zone of the hive are much more likely than bees of the same age to also specialize in removing dead adults from the bottom of the hive. We suggest that this task association has implications for colony fitness and exemplifies an understudied component of how social insect colonies allocate their workers. [ABSTRACT FROM AUTHOR]

Collective personalities refer to temporally consistent behavioral differences between distinct social groups. This phenomenon is a ubiquitous and key feature of social groups in nature, as virtually every study conducted to date has documented repeatable between-group differences in collective behavior, and has revealed ongoing selection on these traits in both the laboratory and field environments. Five years ago, foundational reviews by Bengston and Jandt pioneered this topic and delimited the present knowledge on collective personality. Here, we update these reviews by summarizing the recent works conducted in the field's most prominent model systems: social spiders and eusocial insects. After presenting how these recent works helped scientists to better understand the determinants of collective personality, we used a trait-by-trait format to compare and contrast the results and thematic trends obtained in these taxa on 10 major aspects of collective personality: division of labor, foraging, exploration, boldness, defensive behavior, aggressiveness, decision-making, cognition, learning, and nest construction. We then discuss why similarities and dissimilarities in these results open the door to applying numerous theories developed in evolutionary behavioral ecology for individual traits (e.g., life history theory, game theory, optimal foraging theory) at the colony level, and close by providing examples of unexamined questions in this field that are ripe for new inquiries. We conclude that collective personality, as a framework, has the potential to improve our general understanding of how selection acts on intraspecific variation in collective phenotypes that are of key importance across arthropod societies and beyond. [ABSTRACT FROM AUTHOR]