Regulation Of Worker Reproduction Research Articles

Dietary dopamine supplementation has no effect on ovary activity in queen-less or queen-right honeybee (Apis mellifera) workers

Eusociality in honeybees (Apis mellifera) is characterised by a reproductive division of labour, where the queen monopolises reproduction while worker reproduction is constrained. This constraint is mediated by queen mandibular pheromone (QMP), which inhibits worker ovary development through Notch signalling and possibly oocyte apoptosis. Dopamine has been implicated in regulating reproduction in worker honeybees, with prior studies suggesting that dietary dopamine enhances ovary activity in queen-less workers. This study aimed to test whether dopamine supplementation could overcome QMP-mediated reproductive constraint in worker honeybees. Using caged honeybee experiments, we administered dopamine and its precursor L-dopa at a range of concentrations, both in the presence and absence of QMP. Results showed that neither dopamine nor L-dopa supplementation affected ovary development, survival rates, or food intake, which contrasts with a previous study. These findings suggest that dopamine may not be a major factor in QMP-mediated reproductive inhibition. Instead, we suggest that the multifaceted nature of QMP’s components together with the complexity of neuroendocrine signalling makes it likely that multiple redundant mechanisms regulate worker reproduction. Future research should investigate the interplay between nutrition, dopamine and QMP components to fully understand the regulation of ovary activation in honeybee workers.

The Evolution of Eusociality: Insights From Comparing Two Indian Paper Wasp Species

Eusocial species live in colonies with a reproductive division of labour into fertile reproductive castes and sterile non-reproductive castes, an overlap of generations and cooperative brood care. A further distinction can be usefully made between primitively eusocial species which do not have morphological caste differentiation and highly eusocial species which do. Ropalidia marginata is a tropical primitively eusocial wasp that has been extensively studied, especially compared to other tropical social wasps. R. marginata has several distinct traits, such as a docile queen, well-developed age polyethism, and decentralized work regulation, which makes it different from other primitively eusocial wasps and reminiscent of highly eusocial species. since tropical wasps, especially those belonging to the genus Ropalidia have been poorly studied, we cannot be sure whether R. marginata is unique or its traits are more common among tropical Ropalidia species. to begin to overcome this problem, we have extended our research to the congeneric and sympatric Ropalidia cyathiformis. Here, we compare and contrast what we now know about these two species, especially concerning their reproductive and non-reproductive division of labour. We find that R. cyathiformis, unlike R. marginata, has a behaviourally dominant queen, weak and rigid age polyethism, likely uses behavioural dominance to regulate worker reproduction and individual workers self-regulate their own non-reproductive activities. We, therefore, conclude that R. marginata is indeed unique and argue that R. marginata is intermediate between primitively and highly eusocial wasps.

Bumble bee queen pheromones are context-dependent

Queen pheromones have long been studied as a major factor regulating reproductive division of labor in social insects. Hitherto, only a handful of queen pheromones were identified and their effects on workers have mostly been studied in isolation from the social context in which they operate. Our study examined the importance of behavioral and social context for the perception of queen semiochemicals by bumble bee workers. Our results indicate that a mature queen’s cuticular semiochemicals are capable of inhibiting worker reproduction only when accompanied by the queen’s visual presence and the offspring she produces, thus, when presented in realistic context. Queen’s chemistry, queen’s visual presence and presence of offspring all act to regulate worker reproduction, but none of these elements produces an inhibitory effect on its own. Our findings highlight the necessity to reconsider what constitutes a queen pheromone and suggest a new approach to the study of chemical ecology in social insects.

A small family business: synergistic and additive effects of the queen and the brood on worker reproduction in a primitively eusocial bee.

The mechanisms that maintain reproductive division of labor in social insects are still incompletely understood. Most studies focus on the relationship between adults, overlooking another important stakeholder - the juveniles. Recent studies show that not only the queen but also the brood regulate worker reproduction. However, how the two coordinate to maintain reproductive monopoly remained unexplored. Here, we disentangled the roles of the brood and the queen in primitively eusocial bees (Bombus impatiens) by examining their separated and combined effects on worker behavioral, physiological and brain gene expression. We found that young larvae produce a releaser effect on workers, decreasing oviposition and aggression, while the queen produces both releaser and primer effects, modifying worker behavior and reproductive physiology. The expression of reproduction- and aggression-related genes was altered in the presence of both queen and brood but was stronger or the same in the presence of the queen. We identified two types of interactions between the queen and the brood in regulating worker reproduction: (1) synergistic interactions regulating worker physiology, where the combined effect of the queen and the brood on worker physiology was greater than their separate effects; (2) additive interactions, where the combined effect of the queen and the brood on worker behavior was similar to the sum of their separate effects. Our results suggest that the queen and the brood interact synergistically and additively to regulate worker behavior and reproduction, and this interaction exists at multiple regulatory levels.

The road to sociality: brood regulation of worker reproduction in the simple eusocial bee Bombus impatiens

Eusocial societies, in which egg laying is monopolized by one or a few females, have evolved multiple times during the evolution of insects but were always rooted in a simple family structure. Female reproduction in such families is often characterized by a trade-off between reproduction and brood care, yet most work on the regulation of reproduction in social insects has focused on signals and traits exhibited by adults: particularly on the behaviour and chemical signals produced by the queen and nestmate workers. Here we examined the role of brood in regulating worker reproduction in Bombus impatiens , an annual eusocial species whose reproduction is monopolized by the queen via an unknown mechanism. We found that the presence of young larvae reduced workers' egg laying, whereas the presence of pupae stimulated egg laying. The effect of young larvae was quantity dependent, with nearly complete suppression of egg laying in cages containing a pair of workers and more than 10 young larvae, and replicable regardless of worker age, relatedness to brood or brood parentage/sex. The findings that any larvae can regulate worker reproduction in this simple, yet eusocial, species highlight the role of brood in the evolution of advanced eusocial insects as a mechanism for regulating worker sterility. These findings also provide the first holistic explanation for the regulation of worker reproduction in B. impatiens , suggesting that the queen inhibits worker reproduction through her brood. • Presence of young larvae inhibited worker egg laying in B. impatiens . • Presence of pupae stimulated worker egg laying. • Larval effects were independent of relatedness, brood parentage or its sex. • Larval effect was quantity dependent. • Brood care plays an important role in the evolution of sociality.

Reproductive parasitism by worker honey bees suppressed by queens through regulation of worker mandibular secretions

Social cohesion in social insect colonies can be achieved through the use of chemical signals whose production is caste-specific and regulated by social contexts. In honey bees, queen mandibular gland pheromones (QMP) maintain reproductive dominance by inhibiting ovary activation and production of queen-like mandibular gland signals in workers. We investigated whether honey bee queens can control reproductively active workers of the intraspecific social parasite Apis mellifera capensis, parasitising A. m. scutellata host colonies. Our results show that the queen’s QMP suppresses ovarian activation and inhibits the production of QMP pheromone signals by the parasitic workers, achieved through differential expression of enzymes involved in the biosynthesis of these pheromones at two points in the biosynthetic pathway. This is the first report showing that honey bee queens can regulate reproduction in intraspecific social parasites and deepens our understanding of the molecular mechanisms involved in the regulation of worker reproduction in social insects.

Cuticular hydrocarbons correlate with queen reproductive status in native and invasive Argentine ants (Linepithema humile, Mayr)

In insect societies, chemical communication plays an important role in colony reproduction and individual social status. Many studies have indicated that cuticular hydrocarbons (CHCs) are the main chemical compounds encoding reproductive status. However, these studies have largely focused on queenless or monogynous species whose workers are capable of egg laying and have mainly explored the mechanisms underlying queen-worker or worker-worker reproductive conflicts. Less is known about what occurs in highly polygynous ant species with permanently sterile workers. Here, we used the Argentine ant as a model to examine the role of CHCs in communicating reproductive information in such insect societies. The Argentine ant is unicolonial, highly polygynous, and polydomous. We identified several CHCs whose presence and levels were correlated with queen age, reproductive status, and fertility. Our results also provide new insights into queen executions in the Argentine ant, a distinctive feature displayed by this species in its introduced range. Each spring, just before new sexuals appear, workers eliminate up to 90% of the mated queens in their colonies. We discovered that queens that survived execution had different CHC profiles from queens present before and during execution. More specifically, levels of some CHCs were higher in the survivors, suggesting that workers could eliminate queens based on their chemical profiles. In addition, queen CHC profiles differed based on season and species range (native vs. introduced). Overall, the results of this study provide new evidence that CHCs serve as queen signals and do more than just regulate worker reproduction.

Turning workers into false queens: the role of exogenous pheromones in regulating reproduction in worker honey bees.

One of the responses that honey bee workers can make in the event of queen loss is to develop into false queens. False queens are workers that exhibit both behavioural and physiological traits similar to those of a true queen. However, the presence of more than one false queen in a colony distorts the established hierarchies. As transformation into a false queen occurs after emergence as an adult, we tested the effect of worker mobile pheromone carriers (PCs) treated with exogenously supplied pheromones on their nestmates. The PCs carried either synthetic mandibular gland pheromones or pheromones extracted from Apis melliferacapensis parasitic workers. Only the PCs attracted retinues of workers, increased pheromone production and activated their ovaries, becoming false queens. Pheromones from A. m.capensis workers were more effective than extracts of commercially available synthetic queen pheromones in eliciting these effects. Using this simple mobile pheromone delivery system, we have shown that carrying amounts of exogenous pheromone can induce pheromone production in the carrier, resulting in the production of false queens within experimental groups. Possible implications of using this technique to modify and regulate worker reproduction in colonies are discussed.

Do Bumble Bee, Bombus impatiens, Queens Signal their Reproductive and Mating Status to their Workers?

Reproduction in social insect societies reflects a delicate balance between cooperation and conflict over offspring production, and worker reproduction is widespread even in species showing strong reproductive skew in favor of the queen. To navigate these conflicts, workers are predicted to develop the means to estimate the queen's fecundity - potentially through behavioral and/or chemical cues - and to adjust their reproduction to maximize their fitness. Here, we introduced bumble bee, Bombus impatiens, workers to queens of different mating and reproductive status and examined worker reproduction and expression levels of two genes which were previously shown to be sensitive to the presence of the queen, vitellogenin and Krüppel-homolog 1. We further explored whether the queen's chemical secretion alone is sufficient to regulate worker reproduction, aggression and gene expression. We found that worker ovary activation was inhibited only in the presence of egg-laying queens, regardless of their mating status. Workers reared in the presence of newly-mated queens showed intermediate vitellogenin expression levels relative to workers reared with mated egg-laying and virgin queens. However, none of the whole-body chemical extracts of any of the queen treatment groups affected ovary activation, aggressive behavior, or gene expression in workers. Our findings indicate that only the presence of a freely-behaving, egg-laying queen can fully inhibit worker reproduction. It remains to be determined if workers detect differences in queen mating status and fecundity through differences in the queens' behavior alone or through the queen's behavior in concert with fertility signals.

Larval regulation of worker reproduction in the polydomous ant Novomessor cockerelli.

Although workers in many ant species are capable of producing their own offspring, they generally rear the queen's offspring instead. There are various mechanisms that regulate worker reproduction including inhibitory effects of ant brood. Colonies of the ant Novomessor cockerelli are monogynous and polydomous resulting in a large portion of nest workers being physically isolated from the queen for extended periods of time. Some workers experimentally isolated from the queen in laboratory nests lay viable eggs, which develop into males. We investigate the mechanism that regulates worker fertility in subnests separated from the queen by giving queenless worker groups queen-produced larvae, queen-produced eggs, or no brood. Our findings show that larvae delay the time to worker egg-laying, but eggs have no effect. Larval inhibition is a likely mechanism that contributes to the regulation of worker reproduction in N. cockerellli because larvae are easily transported to subnests that do not contain a queen.

A conserved class of queen pheromones? Re-evaluating the evidence in bumblebees (Bombus impatiens).

The regulation of reproductive division of labour is a key component in the evolution of social insects. Chemical signals are important mechanisms to regulate worker reproduction, either as queen-produced pheromones that coercively inhibit worker reproduction or as queen signals that honestly advertise her fecundity. A recent study suggested that a conserved class of hydrocarbons serve as queen pheromones across three independent origins of eusociality. In bumblebees (Bombus terrestris), pentacosane (C25) was suggested to serve as a queen pheromone. Here, we repeat these studies using a different species of bumblebee (Bombus impatiens) with a more controlled experimental design. Instead of dequeened colonies, we used same-aged, three-worker queenless groups comprising either experienced or naive workers (with/without adult exposure to queen pheromone). We quantified three hydrocarbons (C23, C25 and C27) on the cuticular surfaces of females and tested their effects on the two worker types. Our results indicate differences in responses of naive and experienced workers, genetic effects on worker reproduction, and general effects of hydrocarbons and duration of egg laying on ovary resorption rates. However, we found no evidence to support the theory that a conserved class of hydrocarbons serve as queen pheromones or queen signals in Bombus impatiens.

Social Context and Reproductive Potential Affect Worker Reproductive Decisions in a Eusocial Insect

Context-dependent decision-making conditions individual plasticity and is an integrant part of alternative reproductive strategies. In eusocial Hymenoptera (ants, bees and wasps), the discovery of worker reproductive parasitism recently challenged the view of workers as a homogeneous collective entity and stressed the need to consider them as autonomous units capable of elaborate choices which influence their fitness returns. The reproductive decisions of individual workers thus need to be investigated and taken into account to understand the regulation of reproduction in insect societies. However, we know virtually nothing about the proximate mechanisms at the basis of worker reproductive decisions. Here, we test the hypothesis that the capacity of workers to reproduce in foreign colonies lies in their ability to react differently according to the colonial context and whether this reaction is influenced by a particular internal state. Using the bumble bee Bombus terrestris, we show that workers exhibit an extremely high reproductive plasticity which is conditioned by the social context they experience. Fertile workers reintroduced into their mother colony reverted to sterility, as expected. On the contrary, a high level of ovary activity persisted in fertile workers introduced into a foreign nest, and this despite more frequent direct contacts with the queen and the brood than control workers. Foreign workers' reproductive decisions were not affected by the resident queen, their level of fertility being similar whether or not the queen was removed from the host colony. Workers' physiological state at the time of introduction is also of crucial importance, since infertile workers failed to develop a reproductive phenotype in a foreign nest. Therefore, both internal and environmental factors appear to condition individual reproductive strategies in this species, suggesting that more complex decision-making mechanisms are involved in the regulation of worker reproduction than previously thought.

DETERMINATION OF THE COST OF WORKER REPRODUCTION VIA DIMINISHED LIFE SPAN IN THE ANTDIACAMMASP.

Workers of social Hymenoptera can usually produce male offspring, but rarely do so in the presence of a queen despite the potential individual fitness benefit. Various mechanisms have been hypothesized to regulate worker reproduction, including avoiding the colony-level cost of worker reproduction. However, firm quantitative evidence is lacking to support that hypothesis. Here, we accurately quantified this cost by studying an ant species (Diacamma sp.) in which worker reproduction is rare in the presence of the gamergate (the functional queen). A series of experiments to manipulate worker-gamergate contact revealed that short-term brood-production efficiency is not changed by the presence of worker reproduction. However, when workers reproduce, their average life span is reduced to between 74% and 88% of that in the absence of reproduction, indicating a long-term cost to the colony. In theory, this cost can explain the policing of worker reproduction under a queen-single mating system, but the cost does not appear to be high enough to stop worker reproduction. When contact with the gamergate is lost, it is only the nonreproductive workers whose life span was reduced; the reproductive workers lived as long as nonorphaned workers. We suggest that an increased workload can account for the reduction in life span better than a trade-off between reproduction and longevity.

Regulation of Reproduction in the Primitively Eusocial Wasp Ropalidia marginata: on the Trail of the Queen Pheromone

Queens and workers are not morphologically differentiated in the primitively eusocial wasp, Ropalidia marginata. Upon removal of the queen, one of the workers becomes extremely aggressive, but immediately drops her aggression if the queen is returned. If the queen is not returned, this hyper-aggressive individual, the potential queen (PQ), will develop her ovaries, lose her hyper-aggression, and become the next colony queen. Because of the non-aggressive nature of the queen, and because the PQ loses her aggression by the time she starts laying eggs, we hypothesized that regulation of worker reproduction in R. marginata is mediated by pheromones rather than by physical aggression. Based on the immediate loss of aggression by the PQ upon return of the queen, we developed a bioassay to test whether the queen's Dufour's gland is, at least, one of the sources of the queen pheromone. Macerates of the queen's Dufour's gland, but not that of the worker's Dufour's gland, mimic the queen in making the PQ decrease her aggression. We also correctly distinguished queens and workers of R. marginata nests by a discriminant function analysis based on the chemical composition of their respective Dufour's glands.

Mechanisms of social regulation change across colony development in an ant

BackgroundMutual policing is an important mechanism for reducing conflict in cooperative groups. In societies of ants, bees, and wasps, mutual policing of worker reproduction can evolve when workers are more closely related to the queen's sons than to the sons of workers or when the costs of worker reproduction lower the inclusive fitness of workers. During colony growth, relatedness within the colony remains the same, but the costs of worker reproduction may change. The costs of worker reproduction are predicted to be greatest in incipient colonies. If the costs associated with worker reproduction outweigh the individual direct benefits to workers, policing mechanisms as found in larger colonies may be absent in incipient colonies.ResultsWe investigated policing behaviour across colony growth in the ant Camponotus floridanus. In large colonies of this species, worker reproduction is policed by the destruction of worker-laid eggs. We found workers from incipient colonies do not exhibit policing behaviour, and instead tolerate all conspecific eggs. The change in policing behaviour is consistent with changes in egg surface hydrocarbons, which provide the informational basis for policing; eggs laid by queens from incipient colonies lack the characteristic hydrocarbons on the surface of eggs laid by queens from large colonies, making them chemically indistinguishable from worker-laid eggs. We also tested the response to fertility information in the context of queen tolerance. Workers from incipient colonies attacked foreign queens from large colonies; whereas workers from large colonies tolerated such queens. Workers from both incipient and large colonies attacked foreign queens from incipient colonies.ConclusionsOur results provide novel insights into the regulation of worker reproduction in social insects at both the proximate and ultimate levels. At the proximate level, our results show that mechanisms of social regulation, such as the response to fertility signals, change dramatically over a colony's life cycle. At the ultimate level, our results emphasize the importance of factors besides relatedness in predicting the level of conflict within a colony. Our results also suggest policing may not be an important regulatory force at every stage of colony development. Changes relating to the life cycle of the colony are sufficient to account for major differences in social regulation in an insect colony. Mechanisms of conflict mediation observed in one phase of a social group's development cannot be generalized to all stages.

Reproductive hierarchies and status discrimination in orphaned colonies of Pachycondyla apicalis ants

In group-living animals where dominance hierarchies occur, aggression can be reduced if individuals are able to recognize each other. To do this, and to adapt their behaviour suitably when faced with a rival, individuals may rely on two nonmutually exclusive recognition means: they could recognize group members individually and/or their social status. Within insect societies, although conflicts over reproduction resulting in hierarchy establishment are widespread, relatively little is known about the cognitive abilities involved in the regulation of agonistic interactions. We tested whether low-ranking workers of Pachycondyla apicalis ants are able to discriminate each other individually and/or if they can discriminate the status of their nestmates. We found no evidence of individual discrimination among subordinates whereas they were able to discriminate their nestmates on the basis of their social and reproductive status. Such a skill may allow them to regulate worker reproduction in queenright colonies efficiently. By considering the structure of the hierarchy and the nature of the dominance relationships in P. apicalis societies, we discuss the existence of a more accurate recognition system among the high-ranking workers.

Regulation of worker reproduction in bumblebees (Bombus terrestris): workers eavesdrop on a queen signal

In the annual bumblebee Bombus terrestris, the onset of queen-worker conflict over male production is seasonally and socially constrained. Workers will do better if they start to reproduce (the so-called competition phase) only after ascertaining that larvae are committed to gyne development but before the season ends because they gain more by rearing sister-gynes than their own sons. Here, we tested two nonmutually exclusive hypotheses as to what triggers the onset of worker reproduction: Workers can directly monitor larval development and/or workers eavesdrop on the queen signal that directs gyne development. Exposing workers to gyne larvae through a double mesh did not advance the competition phase compared to control colonies. However, when workers, but not the queen, were allowed contact with gyne larvae, both the competition phase and gyne production were advanced. Thus, while larvae do not emit a volatile pheromone that discloses their developmental route, the physical contact of workers with such larvae triggers early competition phase. However, workers exclusively exposed to worker larvae (colonies prevented from producing gyne larvae) started to reproduce at the same time as control colonies. Replacing the resident queen with an older queen (from gyne-rearing colonies) advanced the competition phase, irrespective of worker age. The results are consistent with the hypothesis that workers eavesdrop on the queen pheromones. This is adaptive because it allows workers a broader time-window for reproduction and thus to gain fitness from rearing both sister-gynes and sons before the season ends without affecting colony development.

The mechanism of the queen signal in regulation of worker reproduction in the myrmicine ant Aphaenogaster smythiesi japonica

In ants, it is generally accepted that worker reproduction is regulated by a chemical signal informing workers of the queen's presence and stimulating workers to refrain from their own reproduction. This is known as the ‘queen signal’ — the mechanism for which is not well understood. In the myrmicine ant, Aphaenogaster smythiesi japonica, the queen signal mechanism was investigated by laboratory experiments. Firstly, in artificial nests where the nest chambers were separated by meshes, the workers were kept under queenright and queenless conditions in the laboratory. After 1 month in queenless conditions, a remarkable development of ovarioles with reproductive eggs was observed in a few queenless workers of each colony. Such development was not observed in queenright workers. This indicates that information of queen presence cannot be transmitted through meshes and that the chemical substances transmitting queen signal are not volatile. Secondly, in other artificial nests, the contact with the queen by workers was limited by attaching a piece of plastic string to their dorsal alitrunk and connecting nest chambers with small tubes. According to the limitation of contact, the workers were classified into three groups, queenright workers (Q+), queenless workers (Q–) and workers which could freely contact with the queen and all workers (FM). The development of ovaries with reproductive eggs was never observed in all workers of the three groups Q+, Q– and FM, indicating that their reproduction was regulated. This strongly suggests that A. s. japonica workers could recognize the queen's presence by direct contact with the queen and that the information could be transmitted via workers in the colony.

Surface hydrocarbons of queen eggs regulate worker reproduction in a social insect.

A hitherto largely unresolved problem in behavioral biology is how workers are prevented from reproducing in large insect societies with high relatedness. Signals of the queen are assumed to inform the nestmates about her presence in the colony, which leads to indirect fitness benefits for workers. In the ant Camponotus floridanus, we found such a signal located on queen-laid eggs. In groups of workers that were regularly provided with queen-laid eggs, larvae, and cocoons, with larvae and cocoons alone, or with no brood, only in the groups with queen-laid eggs did workers not lay eggs. Thus, the eggs seem to inform the nestmates about the queen's presence, which induces workers to refrain from reproducing. The signal on queen-laid eggs is presumably the same that enables workers to distinguish between queen- and worker-laid eggs. Despite their viability, the latter are destroyed by workers when given a choice between both types. Queen- and worker-laid eggs differ in their surface hydrocarbons in a way similar to the way fertile queens differ from workers in the composition of their cuticular hydrocarbons. When we transferred hydrocarbons from the queen cuticle to worker-laid eggs, the destruction of those eggs was significantly mitigated. We conclude that queen-derived hydrocarbon labels inform workers about the presence of a fertile queen and thereby regulate worker reproduction.

The energetic cost of reproductive conflicts in the ant Pachycondyla obscuricornis

In a variety of social animals, individuals can secure reproductive rights through aggressive dominance. Direct individual benefits of aggression are widely recognized, but underlying costs affecting group productivity, and thus indirect benefits, are less clear. Costs of aggressive regulation of reproduction are especially important in small social insect colonies, where individual workers could potentially dominate male production. We estimated the energetic costs associated with the regulation of worker reproduction in the ponerine ant Pachycondyla obscuricornis, using the total CO 2 emission of a colony as a measure. The level of CO 2 emission of 12 experimental colonies varied significantly during five periods with varying levels of aggression and egg-laying. Overall, CO 2 emission increased with the degree of fighting in a colony, but was not associated with differences in egg-laying. Aggressive regulation of reproduction and the formation of a dominance hierarchy thus pose an energetic cost to the colony. Furthermore, workers reduce their work-activities immediately after experimental orphaning, giving a further cost to the colony. These costs might influence the outcome of conflicts over male production in ants. This paper presents the first quantification of energetic costs of aggressive behavior regulating reproduction in ants.