Worker reproductive parasitism and drift in the western honeybee Apis mellifera

When a honeybee (Apis spp.) colony loses its queen and is unable to rear a new one, some of the workers activate their ovaries and produce eggs. When a colony has a queen (i.e., it is queenright) almost all worker-laid eggs are eaten, but when hopelessly queenless, the workers become more tolerant of worker-laid eggs and rear some of them to adult drones. This increased tolerance renders a queenless colony vulnerable to worker reproductive parasitism, wherein unrelated workers enter the colony and lay eggs. Here, we show that the proportion of unrelated (non-natal) workers significantly decreases after an Apis mellifera colony becomes queenless. The remaining non-natal workers are as likely to have activated ovaries as natal workers, yet they produce more eggs than natal workers, resulting in significantly higher reproductive success for non-natal workers. In a second experiment, we provided queenless and queenright workers with a choice to remain in their own colony or to join a queenless or queenright colony nearby. The experiment was set up such that worker movement was unlikely to be due to simple orientation errors. Very few workers joined another colony, and there was no preference for workers to drift into or out of queenless or queenright colonies, in accordance with the proportion of non-natal workers declining significantly after becoming queenless in the first experiment.     

Social parasitism of queens and workers in the Cape honeybee (<Emphasis Type="Italic">Apis mellifera capensis</Emphasis>)

Workers of a queenless honeybee colony can requeen the colony by raising a new queen from a young worker brood laid by the old queen. If this process fails, the colony becomes hopelessly queenless and workers activate their ovaries to lay eggs themselves. Laying Cape honeybee workers (Apis mellifera capensis) produce female offspring as an additional pathway for requeening. We tested the frequency of successful requeening in ten hopelessly queenless colonies. DNA genotyping revealed that only 8% of all queens reared in hopelessly queenless colonies were the offspring of native laying worker offspring. The vast majority of queens resulted from parasitic takeovers by foreign queens (27%) and invading parasitic workers (19%). This shows that hopelessly queenless colonies typically die due to parasitic takeovers and that the parasitic laying workers are an important life history strategy more frequently used than in providing a native queen to rescue the colony. Parasitism by foreign queens, which might enter colonies alone or accompanied by only a small worker force is much more frequent than previously considered and constitutes an additional life history strategy in Cape honeybees.     

Queen primer pheromone affects conspecific fire ant (<Emphasis Type="Italic">Solenopsis invicta</Emphasis>) aggression

Monogyne fire ant, Solenopsis invicta, colony workers are territorial and are aggressive toward members of other fire ant colonies. In contrast, polygyne colony workers are not aggressive toward non-nestmates, presumably due to broader exposure to heritable and environmentally derived nestmate recognition cues (broad template). Workers from both monogyne and polygyne fire ant colonies execute newly mated queens after mating flights. We discovered that monogyne and polygyne queens have a remarkable effect on conspecific recognition. After removal of their colony queen, monogyne worker aggression toward non-nestmate conspecifics quickly drops to merely investigative levels; however, heterospecific recognition/aggression remains high. Queenless monogyne or polygyne worker groups were also not aggressive toward newly mated queens. Queenless worker groups of both forms that adopted a monogyne-derived newly mated queen became aggressive toward non-nestmate workers and newly mated queens. We propose that the powerful effect of fire ant queens on conspecific nestmate recognition is caused by a queen-produced recognition primer pheromone that increases the sensitivity of workers to subtle quantitative differences in nestmate recognition cues. This primer pheromone prevents the adoption of newly mated queens (regulation of reproductive competition) in S. invicta and when absent allows queenless workers to adopt a new queen readily. This extraordinary discovery has broad implications regarding monogyne and polygyne colony and population dynamics.     

The kin recognition system of carpenter ants (Camponotus spp.)

Summary Hamilton's (1964) hypothesis linking haplodiploidy and eusociality in the Hymenoptera could be reconciled with the occurrence of polygyny and multiple insemination if workers are able to distinguish full (3/4 related) sisters from other familiar matri- and patrilines within the colony, and direct altruistic behavior toward them preferentially. We examined this possibility in small genetically mixed nests of the carpenter ant Camponotus floridanus, formed by the transfer of worker pupae from two unrelated source colonies. In 120 h of observation on 12 queenright and 12 queenless nests, more than 15,000 behavioral interactions were recorded. Workers antennated familiar nonkin significantly more frequently than familiar sisters. However, they failed to discriminate consistently between kin and non-kin in food exchanges and grooming. Aggressive behavior was occasionally observed in some queenless nests, but almost never in the presence of a queen. When aggression did occur, it was directed significantly more often toward non-kin. Though related adult workers did not cooperate preferentially, the biases in antennation and aggression do indicate an ability to discriminate familiar kin from familiar nonkin, which may be employed in other contexts such as the rearing of reproductive brood.     

The reproductive dilemmas of queenless red dwarf honeybee (Apis florea) workers

Honeybee (Apis) workers cannot mate, but retain functional ovaries. When colonies have lost their queen, many young workers begin to activate their ovaries and lay eggs. Some of these eggs are reared, but most are not and are presumably eaten by other workers (worker policing). Here we explore some of the factors affecting the reproductive success of queenless workers of the red dwarf honeybee Apis florea. Over a 2-year period we collected 40 wild colonies and removed their queens. Only two colonies remained at their translocated site long enough to rear males to pupation while all the others absconded. Absconding usually occurred after worker policing had ceased, as evidenced by the appearance of larvae. Dissections of workers from eight colonies showed that in A. florea, 6% of workers have activated ovaries after 4 days of queenlessness, and that 33% of workers have activated ovaries after 3 weeks. Worker-laid eggs may appear in nests within 4 days and larvae soon after, but this is highly variable. As with Apis mellifera, we found evidence of unequal reproductive success among queenless workers of A. florea. In the two colonies that reared males to pupation and which we studied with microsatellites, some subfamilies had much higher proportions of workers with activated ovaries than others. The significance of absconding and internest reproductive parasitism to the alternative reproductive strategies of queenless A. florea workers is discussed.     

Social regulation of ovary activation in ’anarchistic’ honey-bees (Apis mellifera)

Honey-bee (Apis mellifera) colonies exhibit extreme reproductive division of labour. Workers almost always have inactive ovaries and the queen monopolises egg laying. Although extremely rare, ’anarchistic’ colonies exist in which workers produce male offspring despite the presence of the queen. By comparing the rates of ovary activation in anarchistic and wild-type bees fostered to host colonies of different genotype (i.e. anarchist and non-anarchist) and queen status (i.e. queenless and queenright), we investigated the factors involved in inhibiting ovary activation. Fostered anarchist workers always had a higher level of ovary development than fostered wild-type bees in both anarchist and non-anarchist host colonies. Fostered workers of both genotypes had more active ovaries in anarchistic than in wild-type hosts. Fostered workers of both strains also had more active ovaries in queenless than in queenright hosts. The results suggest that selection for worker reproduction in the anarchistic line has both reduced the effects of brood and queen pheromones on worker ovary inhibition and increased the likelihood that workers of the anarchistic line will develop ovaries compared to wild-type workers. Received: 14 June 2000 / Revised: 26 September 2000 / Accepted: 7 October 2000     

Worker policing and worker reproduction in Apis cerana

Workers of the Asian hive bee, Apis cerana, are shown to have relatively high rates of worker ovary activation. In colonies with an active queen and brood nest, 1-5% of workers have eggs in their ovarioles. When A. cerana colonies are dequeened, workers rapidly activate their ovaries. After 4 days 15% have activated ovaries and after 6 days, 40%. A cerana police worker-laid eggs in the same way that A. florea and A. mellifera do, but are perhaps slightly more tolerant of worker-laid eggs than the other species. Nevertheless, no worker's sons were detected in a sample of 652 pupal males sampled from 4 queenright colonies. A cerana continue to police worker-laid eggs, even after worker oviposition has commenced in a queenless colony.     

Colony level and within colony level selection in honeybees

Summary Although honeybee workers are usually infertile, in queenless colonies some workers can develop ovaries and produce offspring. Therefore the classical Darwinian fitness of workers is not zero. Experimental studies in the Cape honey bee (Apis mellifera capensis) reveal a huge genetic variation for individual fitness of workers. The present study with a one locus, two allele model for reproductive dominance of workers shows that a balanced system between colony level and individual within colony selection plausibly explains the phenomenon of a high genetic variance of worker fitness. In particular, a frequent occurrence of queenless colonies in the population leads to stable polymorphic equilibria. Also the multiple mating system of the honey bee queen supports the propagation of alleles causing reproductive dominance of workers.     

The appeasement effect of sterility signaling in dominance contests among Bombus terrestris workers

The establishment of dominance hierarchies through aggressive interactions is very common in insect societies. In many cases, it is also mediated through pheromone emissions that enable individuals to evaluate the reproductive quality and level of aggressiveness of the dominant individual, thereby reducing the number and intensity of costly fights. Here, we studied these processes in the primitively eusocial bee Bombus terrestris, using a paired bee system. Specifically, we investigated the behavioral, reproductive, and pheromonal correlates of dominance establishment. Workers were shown to establish dominance hierarchies using overt aggression within 3–4 days. Thereafter, the aggression drastically decreased, and dominance was maintained mostly by ritualized agonistic behavior. The behaviorally dominant bee lost the ester compounds that workers produce in their Dufour's gland (the so-called “sterility signal”) concomitantly with the development of her ovaries. The other bee announced as subordinate by continuously producing high amounts of those esters. The hypothesis that sterility signaling serves as an appeasement signal to pacify the dominant bees is supported by the negative correlation found between the proportion of these esters and the level of aggression that the subordinate received from the dominant worker. Physical interactions, and presumably also the ensuing overt aggression between the bees, were essential for the above pheromonal change to take place and enabled the dominant workers to develop their ovaries and to lay eggs. The subordinate bee’s signaling of non-reproductive status may minimize energy expenditure in costly fights and help stabilize the reproductive division of labor among workers.     

Dufour’s gland pheromone as a reliable fertility signal among honeybee (Apis mellifera) workers

When a colony becomes queenless and without the possibility of requeening, honeybee workers initiate reproduction and lay male eggs about a week later. Assays in which two bees were confined in a small arena revealed that they establish a reproductive dominance hierarchy, i.e., one worker demonstrates greater ovarian development than her paired bee. Reproductive dominance is independent of relatedness, and can be established between full sisters, cousins, or random nestmates. A social environment, however, is obligatory, as singly housed bees fail to develop ovaries on the same time scale. Allowing varying degrees of social interactions between the paired bees revealed that olfaction of volatile bee compounds, as well as tactile communication, seem to provide the necessary social environment. Ovarian development was accompanied by the production of queen-like Dufours gland secretion in these workers. Especially notable was the increase in the queen-like esters. This increase was tightly linked to ovarian development and not necessarily to the dominance status of the bees in the pair. Thus, the occurrence of queen-like esters can serve as a reliable fertility signal. Advertising ovarian status may recruit helper workers with less developed ovaries (and which are less likely to successfully reproduce before colony breakdown) to assist their nestmates and thereby gain inclusive fitness. Revealing the role of Dufours gland secretion as a fertility signal adds another dimension to our understanding of how queen pheromones operate. The mandibular-gland secretion is a good predictor of dominance hierarchy, being correlated with false-queen characteristics but not fertility, whereas Dufours gland secretion is a good predictor of fertility but not dominance hierarchy.Communicated by R.F.A. Moritz     

The kin recognition system of carpenter ants (Camponotus spp.)

Summary The phenotypic cues that provide for rejection of non-nestmates by workers of the ant genus Camponotus could derive from any or all of four sources: (1) environmental odors; (2) the individual's own genetically-determined recognition pheromones or discriminators; (3) a gestalt or mixture of transferable discriminators, produced by each nestmate and absorbed by all; and/or (4) the discriminators of the queen applied to all nestmates. To test these hypotheses, four series of small experimental colonies were created: inter- and intraspecific mixed colonies containing queens, queenless worker groups, and pairs of worker groups between which a single queen was repeatedly switched. Intraspecific mixed colonies and queenless groups were further divided into groups receiving different diets. Aggression of workers in 165 experimental colonies was assayed in a total of 4064 neutral arena tests. Workers adopted into inter- and intraspecific mixed colonies with queens were highly aggressive to unfamiliar kin from pure colonies, independent of diet and of the proportion of different kin groups in the colony. However, queenless workers exhibited less aggression to unfamiliar kin than to non-kin, demonstrating the existence of worker discriminators. Diet differences slightly enhanced aggression among unfamiliar queenless kin. Non-kin sharing a switched queen were as unaggressive to one another as were sisters. The ability to adopt queenless workers between colonies gradually declined over 1–2 wks following their emergence from pupae. We propose a hierarchy of importance of cue sources in determining nestmate discrimination in small Camponotus colonies: Queen discriminators> worker discriminators>environmental cues. A flow-diagram model of social insect kin recognition, based on the phenotype matching concept of Holmes and Sherman (1983), is discussed.     

Queen acceptance and the complexity of nestmate discrimination in the Argentine ant

In most social insect species, individuals recognize and behave aggressively towards non-nestmate conspecifics to maintain colony integrity. However, introduced populations of the invasive Argentine ant, Linepithema humile, exhibit pronounced variation in intraspecific aggression denoting diversity in nestmate recognition behavior, which possibly shapes their social structure and the varying levels of unicoloniality observed among these populations. One approach to better understand differential aggression behaviors towards conspecifics and recognition cue perception and response in L. humile is to examine variation in nestmate discrimination capability among genetically distinct colonies under different social contexts. Consequently, we investigated the dynamics of queen and worker recognition in southeastern US L. humile queenless and queenright colonies by measuring rates of non-nestmate worker and queen adoption and intercolony genetic similarity. Aggression levels between colony pairs differed and were associated with non-nestmate worker, but not queen adoption. Adoption of queens and workers was a function of host colony origin, while colony queen number affected adoption of queens, but not workers, with queens more readily accepted by queenless hosts. Fecundity of adopted non-nestmate queens was comparable to that of rejected non-nestmate and host colony queens, suggesting that queen fecundity did not affect adoption decisions. Genetic similarity between colonies ranged from 30 to 77% alleles shared, with more genetically similar colonies showing lower levels of intraspecific aggression. Non-nestmate queens and workers that were more genetically similar to host colony workers were more likely to be adopted. We provide the first evidence for the role of L. humile colony queen number on queen discrimination and suggest an effect of resident queens on worker conspecific acceptance thresholds. Our findings indicate a role for genetically based cues in L. humile nestmate recognition. However, subtle discrimination capability seems to be influenced by the social context, as demonstrated by more frequent recognition errors in queenless colonies.     

Individual responsiveness to shock and colony-level aggression in honey bees: evidence for a genetic component

The phenotype of the social group is related to phenotypes of individuals that form that society. We examined how honey bee colony aggressiveness relates to individual response of male drones and foraging workers. Although the natural focus in colony aggression has been on the worker caste, the sterile females engaged in colony maintenance and defense, males carry the same genes. We measured aggressiveness scores of colonies and examined components of individual aggressive behavior in workers and haploid sons of workers from the same colony. We describe for the first time, that males, although they have no stinger, do bend their abdomen (abdominal flexion) in a posture similar to stinging behavior of workers in response to electric shock. Individual worker sting response and movement rates in response to shock were significantly correlated with colony scores. In the case of drones, sons of workers from the same colonies, abdominal flexion significantly correlated but their movement rates did not correlate with colony aggressiveness. Furthermore, the number of workers responding at increasing levels of voltage exhibits a threshold-like response, whereas the drones respond in increasing proportion to shock. We conclude that there are common and caste-specific components to aggressive behavior in honey bees. We discuss implications of these results on social and behavioral regulation and genetics of aggressive response.     

Reproductive competition in queenless honey bee colonies (Apis mellifera L.)

Previously we reported that there are subfamily differences in drone production in queenless honey bee colonies, but these biases are not always explained by subfamily differences in oviposition behavior. Here we determine whether these puzzling results are best explained by either inadequate sampling of the laying worker population or reproductive conflict among workers resulting in differential treatment of eggs and larvae. Using colonies composed of workers from electrophoretically distinct subfamilies, we collected samples of adult bees engaged in the following behavior: true egg laying, false egg laying, indeterminate egg laying, egg cannibalism, or nursing (contact with larvae). We also collected samples of drone brood at four different ages: 0 to 2.5-h-old eggs, 0 to 24-h-old eggs, 3 to 8-day-old larvae, and 9 to 14-day-old larvae and pupae. Allozyme analyses revealed significant subfamily differences in the likelihood of exhibiting egg laying, egg cannibalism, and nursing behavior, as well as significant subfamily differences in drone production. There were no subfamily differences among the different types of laying workers collected from each colony, suggesting that discrepancies between subfamily biases in egg-laying behavior and drone production are not due to inadequate sampling of the laying worker population. Subfamily biases in drone brood production within a colony changed significantly with brood age. Laying workers had significantly more developed ovaries than either egg cannibals or nurses, establishing a physiological correlate for the observed behavioral genetic differences. These results suggest there is reproductive conflict among subfamilies and individuals within queenless colonies of honey bees. The implications of these results for the evolution of reproductive conflict, in both queenright and queenless contexts, are discussed.     

Division of labor between undertaker specialists and other middle-aged workers in honey bee colonies

A primary determinant of colony organization in temporally polyethic insect societies is inter-individual variation in behavior that is independent of worker age. We examined behavioral repertoires, behavioral correlates of adult development, and spatial distributions within the hive to explore the mechanisms that produce behavioral variation among middle-age honey bees (Apis mellifera). Individually labeled undertakers, guards, food storers, and wax workers exhibited a broad range of task-related behavior, but bees tagged as undertakers were more likely to subsequently remove a corpse from the hive and handle a corpse compared to other middle-aged bees. The activity level of undertakers was similar to other task groups, suggesting that undertaking specialists were neither hyper-active “elites” nor quiescent “reserves” that become active only when a dead bee stimulus is present. Undertakers also were more likely to remove debris and to remain in the lower region of the hive or near the entrance, even when not engaged in corpse removal; both preferences may promote colony efficiency by reducing inter-task travel times. Guards and undertakers were less likely to perform behavior normally associated with young bees compared to food storers and wax workers. Undertakers and guards also initiated foraging at earlier ages than the other task groups. These results suggest that undertakers and guards may be slightly developmentally advanced compared to food storers and wax workers. There also was evidence for lifetime differences in behavioral preferences which could not be explained by differences in adult development. Bees tagged as undertakers were more likely to subsequently remove a dead bee during their entire pre-foraging career compared to other task groups or members of their general age cohort. Differences in both the rate of adult development and individual behavioral preferences, both of which may be subject to genetic and environmental influences, are important determinants of inter-individual variation among honey bees of middle age. Received: 5 February 1997 / Accepted after revision: 27 May 1997     

Regulation of ovary activation in worker honey-bees (Apis mellifera): larval signal production and adult response thresholds differ between anarchistic and wild-type bees

One-day-old anarchistic (selected for successful worker reproduction) and wild-type honey-bee workers were introduced into queenright colonies of honey-bees of two treatments. In treatment 1, all eggs and larvae were offspring of queens from an anarchistic line. In treatment 2, all eggs and larvae were offspring of wild-type queens. In both treatments, adult workers were wild type. This experimental arrangement was used to test the importance of larval genotype on ovary activation in young adult workers. After 12 days, the introduced bees were dissected to determine the frequency of ovary activation. In those colonies provided with wild-type brood, 0% of introduced wild-type bees and 16% of anarchistic bees had activated ovaries. In those colonies provided with anarchistic brood, 13% of introduced wild-type bees and 41% of anarchistic bees had activated ovaries. These results strongly support the hypothesis that selection for high levels of worker reproduction in anarchistic stocks has reduced the amount or composition of brood pheromones produced by larvae that normally signal workers to refrain from reproduction. They also suggest that anarchistic workers have a higher threshold for these signals than wild-type bees.     

Differential reproductive success among subfamilies in queenless honeybee (<Emphasis Type="Italic">Apis mellifera</Emphasis> L.) colonies

With very rare exceptions, queenright worker honeybees (Apis mellifera L.) forego personal reproduction and suppress reproduction by other workers, preferring to rear the queens sons. This is in stark contrast to colonies that have lost their queen and have failed to rear a replacement. Under these conditions workers activate their ovaries and lay many eggs that develop parthenogenetically into a final brood of males (drones) before the colony perishes. Interestingly, not all workers contribute equally to this final generation of drones in queenless colonies. Some subfamilies (workers that share the same father) contribute a disproportionately greater number of offspring than other subfamilies. Here we explore some of the mechanisms behind this reproductive competition among subfamilies. We determined the relative contribution of different subfamilies present in colonies to laying workers, eggs, larvae and pupae by genotyping samples of all life stages using a total of eight microsatellite loci. Our colonies were headed by free-mated queens and comprised 8–17 subfamilies and therefore differed significantly from colonies used in an earlier study investigating the same phenomena where colonies comprised an artificially low number of subfamilies. We show that, first, subfamilies vary in the speed with which they activate their ovaries after queen-loss and, second, that the survival of eggs to the larval stage is unequal among subfamilies suggesting that some subfamilies lay eggs that are more acceptable than others. However, there is no statistically significant difference among subfamilies in the survival of larvae to pupae, indicating that ovary activation and egg survival are the critical components to reproductive competition among subfamilies of queenless honeybee workers.Communicated by R. Page     

“Selfish worker policing” controls reproduction in a Temnothorax ant

Animal societies, including those of humans, are under constant threat by selfish individuals, who attempt to enforce their own interests at the cost of the group. In the societies of bees, wasps, and ants, such individual selfishness can be prevented by “policing,” whereby workers or queens impede the reproduction of other individuals by aggression, immobilization, or egg eating. In this study, we report on a particular kind of reproduction control in the ant Temnothorax unifasciatus, which can be considered as a selfish act itself. We experimentally induced workers to lay eggs by dividing several colonies into two halves, one with and one without a queen. In queenless colonies, workers established rank orders by aggression and several top-ranking workers started to reproduce. Upon reunification, egg-laying workers mostly stopped behaving aggressively. They were neither attacked by the queen nor by random workers, but instead received infrequent, nondestructive, targeted aggression from a few workers, most of which became fertile when the queen was later removed. The introduction of differentially stained worker-laid and queen-laid eggs in queenright fragments did not lead to a selective removal of worker-laid eggs. Hence, there appears to be no collective worker policing in T. unifasciatus. Instead, reproduction appears to be controlled mostly through a few attacks from high-ranking workers, which, in this way, might attempt to selfishly increase their chances of future reproduction.     

Chemical camouflage of the slave-making ant Polyergus samurai queen in the process of the host colony usurpation (Hymenoptera: Formicidae)

Founding queens of the obligatory social parasite ant Polyergus samurai usurp the host ant Formica japonica colony. The aggressive behaviors of F. japonica workers on the parasite queen disappear after the parasite queen kills the resident queen. To determine whether the parasite queen chemically mimics the host ants, we examined the aggressive behavior of F. japonica workers toward glass dummies applied with various extracts of the parasite queen and host workers. The crude extracts and hydrocarbon fraction reproduced the host workers’ behavior to the live ants. The extracts of the post-adoption parasite queen, as well as the nestmate extracts of F. japonica, did not elicit the aggressive behavior, but the extract of the pre-adoption parasite queen triggered attacks by the host workers. The nestmate recognition of host workers did not change, regardless of contact with the parasite. The gas chromatography and gas chromatography–mass spectrometry analyses indicated that the cuticular hydrocarbon (CHC) profile of the parasite queen drastically changed during the process of usurpation. Discriminant analysis showed the successfully usurped P. samurai queen had colony-specific CHC profiles. CHC profiles of the P. samurai queen who killed the host queen were more similar to those of the host queen than the workers, while the P. samurai queen who usurped the queenless colony had a profile similar to those of host workers. These results suggest that the P. samurai queen usually acquires the CHCs from the host queen during the fight, but from host wokers in queenless host colonies.     

Regulation of honey bee age polyethism by juvenile hormone

Summary Previous studies suggested that juvenile hormone (JH) is involved in the regulation of physiological processes that are associated with division of labor in honey bees but the effects of JH on behavior were not clear. The hypothesis that JH affects worker age polyethism was tested by observing individually marked bees topically treated with different doses of the JH analog methoprene. Methoprene caused dose-dependent changes in the timing and frequency of occurrence of four important age-dependent tasks: brood and queen care, food storage, nest maintenance, and foraging. Weak or no effects were observed for social interactions, self-grooming, and other non-task behaviors that were not performed in an age-dependent manner. These results support the hypothesis that JH is involved in the control of age polyethism. A model is presented that explains the role of JH in regulating division of labor. JH may regulate the colony's allocation of labor by altering the probabilities of response to tasks. According to this model, hormone titers increase with age according to a genetically determined pattern of development, but this rise may be modulated by environmental and colony factors such as food availability and population structure. Extrinsic regulation of JH may be a mechanism underlying the ability of workers to respond to changing colony needs.