Worker reproduction in the ant Formica fusca

We studied the kin conflict over male parentage in the ant Formica fusca. The conflict arises because each worker and queen is most related to her own sons and is thus predicted to lay eggs. Microsatellite analysis of eggs revealed that workers laid eggs in more than half the queenright experimental nests. Nevertheless, almost exclusively diploid offspring were reared in the presence of a queen. This also occurred when worker-laid haploid male eggs were experimentally introduced in to the nests. Because our experimental setup allowed us to exclude the possibility of queen policing, we conclude that worker laid eggs are removed by other workers, either as a response to their parentage or gender. Our results suggest that worker reproduction in F. fusca is ultimately an interplay of conflicts over male parentage and sex allocation and that both worker and self policing have roles as proximate mechanisms of resolution.     

The evolution of queen control over worker reproduction in the social Hymenoptera

A trademark of eusocial insect species is reproductive division of labor, in which workers forego their own reproduction while the queen produces almost all offspring. The presence of the queen is key for maintaining social harmony, but the specific role of the queen in the evolution of eusociality remains unclear. A long‐discussed scenario is that a queen either behaviorally or chemically sterilizes her workers. However, the demographic and ecological conditions that enable such manipulation are still debated. We study a simple model of evolutionary dynamics based on haplodiploid genetics. Our model is set in the commonly observed case where workers have lost the ability to lay female (diploid) eggs by mating, but retain the ability to lay male (haploid) eggs. We consider a mutation that acts in a queen, causing her to control the reproductive behavior of her workers. Our mathematical analysis yields precise conditions for the evolutionary emergence and stability of queen‐induced worker sterility. These conditions do not depend on the queen's mating frequency. We find that queen control is always established if it increases colony reproductive efficiency, but can evolve even if it decreases colony efficiency. We further derive the conditions under which queen control is evolutionarily stable against invasion by mutant workers who have recovered the ability to lay male eggs.     

Kin-selected conflict in the bumble-bee Bombus terrestris (Hymenoptera: Apidae)

Kin selection theory predicts conflict in social Hymenoptera between the queen and workers over male parentage because each party is more closely related to its own male offspring. Some aspects of the reproductive biology of the bumble-bee Bombus terrestris support kin selection theory but others arguably do not. We present a novel hypothesis for how conflict over male parentage should unfold in B. terrestris colonies. We propose that workers delay laying eggs until they possess information showing that egg laying suits their kin-selected interests. In colonies where queens start to lay haploid eggs early, we hypothesize that this occurs when workers detect the presence of queen-produced male brood in the brood's larval stage. In colonies where queens start to lay haploid eggs late, we hypothesize that it occurs when workers detect a signal from the queen to female larvae to commence development as queens. Our hypothesis accounts for previously unexplained aspects of the timing of reproductive events in B. terrestris, provides ultimate explanations for the results of a recent study of mechanisms underlying queen-worker conflict and helps explain this species' characteristic bimodal (split) sex ratios. Therefore, kin selection theory potentially provides a good explanation for reproductive patterns in B. terrestris.     

Sex ratio conflict and worker production in eusocial hymenoptera

The best known of the conflicts occurring in eusocial Hymenoptera is queen-worker conflict over sex ratio. So far, sex ratio theory has mostly focused on optimal investment in the production of male versus female sexuals, neglecting the investment in workers. Increased investment in workers decreases immediate sexual productivity but increases expected future colony productivity. Thus, an important issue is to determine the queen's and workers' optimal investment in each of the three castes (workers, female sexuals, and male sexuals), taking into account a possible trade-off between production of female sexuals and workers (both castes developing from diploid female eggs). Here, we construct a simple and general kin selection model that allows us to calculate the evolutionarily stable investments in the three castes, while varying the identity of the party controlling resource allocation (relative investment in workers, female sexuals, and male sexuals). Our model shows that queens and workers favor the investment in workers that maximizes lifetime colony productivity of sexual males and females, whatever the colony kin structure. However, worker production is predicted to be at this optimum only if one of the two parties has complete control over resource allocation, a situation that is evolutionarily unstable because it strongly selects the other party to manipulate sex allocation in its favor. Queens are selected to force workers to raise all the males by limiting the number of eggs they lay, whereas workers should respond to egg limitation by raising a greater proportion of the female eggs into sexual females rather than workers as a means to attain a more female-biased sex allocation. This tug-of-war between queens and workers leads to a stable equilibrium where sex allocation is between the queen and worker optima and the investment in workers is below both parties' optimum. Our model further shows that, under most conditions, female larvae are in strong conflict with queens and workers over their developmental fate because they value their own reproduction more than that of siblings. With the help of our model, we also investigate how variation in queen number and number of matings per queen affect the level of conflict between queens, workers, and larvae and ultimately the allocation of resource in the three castes. Finally, we make predictions that allow us to test which party is in control of sex allocation and caste determination.     

Queens, not workers, produce the males in the stingless bee Schwarziana quadripunctata quadripunctata

Most stingless bee colonies have one singly mated queen, resulting in a potential conflict between workers and queen over male production, because workers are more closely related to the sons of other workers than they are to the queen's sons. Furthermore, workers in the majority of stingless bee species have ovarian development, can produce haploid eggs, and show apparently agonistic behaviour towards their queen, suggesting a real conflict. We investigated whether genetic conflict over male production resulted in reproductive and behavioural conflict in Schwarziana q. quadripunctata. DNA microsatellite loci showed that, even though workers are more related to other workers' sons than to queen's sons, it is the queen who produces the males. Behavioural interactions between workers and their queen were not uniformly more aggressive during male production than at times with only worker production, although some differences might have been obscured by the fact that food supply was greater during male production. The potential conflict over male production inS. q. quadripunctata seems not to lead to an observable conflict between the workers and their queen. Workers might refrain from reproduction because of the costs involved for the colony or because of queen control.     

The honeybee queen influences the regulation of colony drone production

Social insect colonies invest in reproduction and growth, buthow colonies achieve an adaptive allocation to these life-historycharacters remains an open question in social insect biology.Attempts to understand how a colony's investment in reproductionis shaped by the queen and the workers have proved complicatedbecause of the potential for queen–worker conflict overthe colony's investment in males versus females. Honeybees,in which this conflict is expected to be minimal or absent,provide an opportunity to more clearly study how the actionsand interactions of individuals influence the colony's productionand regulation of males (drones). We examined whether honeybeequeens can influence drone regulation by either allowing orpreventing them from laying drone eggs for a period of timeand then examining their subsequent tendency to lay drone andworker eggs. Queens who initially laid drone eggs subsequentlylaid fewer drone eggs than the queens who were initially preventedfrom producing drone eggs. This indicates that a colony's regulationof drones may be achieved not only by the workers, who buildwax cells for drones and feed the larvae, but also by the queen,who can modify her production of drone eggs. In order to betterunderstand how the queen and workers contribute to social insectcolony decisions, future work should attempt to distinguishbetween actions that reflect conflict over sex allocation andthose that reflect cooperation and shared control over the colony'sinvestment in reproduction.     

No evidence that reproductive bumblebee workers reduce the production of new queens

Kin selection theory predicts potential conflict between queen and workers over male parentage in hymenopteran societies headed by one, singly mated queen, because each party is more closely related to its own male offspring. In ‘late-switching’ colonies of the bumblebee Bombus terrestris, i.e. colonies whose queens lay haploid eggs relatively late in the colony cycle, workers start to lay male eggs shortly after the queen lays the female eggs that will develop into new queens. It has been hypothesized that this occurs because workers recognize, via a signal given by the queen instructing female larvae to commence development as queens, that egg laying is now in their kin-selected interest. This hypothesis assumes that aggressive behaviour in egg-laying workers does not substantially reduce the production of new queens, which would decrease the workers' fitness payoff from producing males. We tested the hypothesis that reproductive activity inB. terrestris workers does not reduce the production of new queens. We used microsatellite genotyping to sex eggs and hence to select eight size-matched pairs of ‘late-switching’ colonies from a set of commercial colonies. From one colony of each pair we removed every egg-laying or aggressive worker observed. From the other colony, we simultaneously removed a nonegg-laying, nonaggressive worker. Removed workers were replaced with young workers from separate colonies at equal frequencies within the pair. There was no significant difference in queen productivity between colonies with reduced or normal levels of egg-laying or aggressive workers. Therefore, as predicted, reproductive B. terrestris workers did not significantly reduce the production of new queens.     

Within-colony relatedness asymmetry and social conflicts in ants

The haplodiplo?d sex-determining system of Hymenoptera, whereby males usually develop from unfertilized eggs and females from fertilised eggs, results in relatedness coefficients that are not uniform among colony members. These asymmetries in relatedness are directly affected by the genetic architecture of the colony, which in turn depends on various factors such as queen number or queen mating frequency. Relatedness asymmetries induce different fitness returns per unit investment and, as a result, conflicts over brood composition may arise among colony members. Conflicts between the queen(s) and the workers over sex ratio represent one of the most frequent conflicts in eusocial Hymenoptera. Arrhenotoky allows queens great flexibility to control the sex of their progeny, by fertilizing or not the eggs; however because workers take care of the brood, they may influence the sex ratio by preferentially rearing one sex. Another salient conflict concerns the females over reproduction. In species where workers can mate and reproduce, physical aggressions or chemical communication may lead to dominance hierarchies for access to reproduction.     

Sex ratio determination by queens and workers in the ant Pheidole desertorum

Because workers in colonies of eusocial Hymenoptera are more closely related to sisters than to brothers, theory predicts workers should bias investment in reproductive broods to favour reproductive females over males. However, conflict between queens and workers is predicted. Queens are equally related to daughters and sons, and should act to prevent workers from biasing investment. Previous study of the ant Pheidole desertorum showed that workers are nearly three times more closely related to reproductive females than males; however, the investment sex ratio is very near equal, consistent with substantial queen control of workers. Near-equal investment is produced by an equal frequency of colonies whose reproductive broods consist of only females (female specialists) and colonies whose reproductive broods consist of only males or whose sex ratios are extremely male biased (male specialists). Because natural selection should act on P. desertorum workers to bias investment in favour of reproductive females, why do workers in male-specialist colonies rear only (or mostly) males? We tested the hypothesis that queens prevent workers from rearing reproductive females by experimentally providing workers with immature reproductive broods of both sexes. Workers reared available reproductive females, while failing to rear available males. Worker preference for rearing reproductive females is consistent with queens preventing their occurrence in colonies of male specialists. These results provide evidence that queens and workers will act in opposition to determine the sex ratio, a fundamental prediction of queen-worker conflict theory. Copyright 2000 The Association for the Study of Animal Behaviour.     

Queen-worker conflicts over male production and sex allocation in a primitively eusocial wasp

Abstract In a colony headed by a single monandrous foundress, theories predict that conflicts between a queen and her workers over both sex ratio and male production should be intense. If production of males by workers is a function of colony size, this should affect sex ratios, but few studies have examined how queens and workers resolve both conflicts simultaneously. We conducted field and laboratory studies to test whether sex-ratio variation can be explained by conflict over male production between queen and workers in the primitively eusocial wasp Polistes chinensis antennalis.
Worker oviposition rate increased more rapidly with colony size than did queen oviposition. Allozyme and micro-satellite markers revealed that the mean frequency of workers' sons among male adults in queen-right colonies was 0.39 ± 0.08 SE (n = 22). Genetic relatedness among female nestmates was high (0.654–0.796), showing that colonies usually had a single, monandrous queen. The mean sex allocation ratio (male investment/male and gyne investments) of 46 queen-right colonies was 0.47 ± 0.02, and for 25 orphaned colonies was 0.86 ± 0.04. The observed sex allocation ratio was likely to be under queen control. For queen-right colonies, the larger colonies invested more in males and produced reproductives protandrously and/or simultaneously, whereas the smaller colonies invested more in females and produced reproductives protogynously. Instead of positive relationships between colony size and worker oviposition rate, the frequency of workers' sons within queen-right colonies did not increase with colony size. These results suggest that queens control colony investment, even though they allow worker oviposition in queen-right colonies. Eggs laid by workers may be policed by the queen and/or fellow workers. Worker oviposition did not influence the outcome of sex allocation ratio as a straightforward function of colony size.     

Do hornets have zombie workers?

Colonies of the European hornet, Vespa crabro, are typically founded by a single queen mated to a single male. From the resulting colony relatedness pattern we predicted strong worker-queen conflict over male production where both the workers and the queen attempt to produce the colony's males. To test for this conflict, male production was studied in 15 hornet nests using a combination of DNA microsatellite analysis (282 males), worker ovary dissections (500 workers from eight nests) and 50 h of observation (four nests). In contrast to our prediction, the data show that hornet males are queens' sons, that workers never attempt to lay eggs, rarely have activated ovaries, and that there is no direct aggression between the queen and the workers. This contrasts with other data for vespine wasps, which support relatedness predictions. Dolichovespula arenaria has the same kin structure as V. crabro and workers produce males in many colonies. The similarity between these two species makes it difficult to explain why workers do not reproduce in V. crabro. Self-restraint is expected if worker reproduction significantly reduces colony productivity but there is no obvious reason why this should be important to V. crabro but not to D. arenaria. Alternatively, queen control may be important. The absence of expressed queen-worker conflict rules out physical control. Indirect pheromonal control is a possibility and is supported by the occurrence of royal courts and queen pheromone in Vespa but not Dolichovespula. Pheromonal queen control is considered evolutionarily unstable, but could result from a queen-worker arms race over reproductive control in which the queen is ahead. The genetic data also revealed diploid males in one colony, the first example in the vespine wasps, and two colonies with double matrilines, suggesting that occasional usurpation by spring queens occurs.     

Unequal partitioning of reproduction and investment between cooperating queens in the fire ant,Solenopsis invicta,as revealed by microsatellites

Social insects provide ideal systems for investigating how kinship and ecological factors affect cooperation and conflict. In many ant species, unrelated queens cooperate to initiate new colonies. However, fights between queens break out after the eclosion of the first workers, leading to the death of all but one queen. Queens within associations potentially face a trade-off. On one hand, a queen should restrain her investment in brood production and care if this helps her to maintain fighting ability. On the other hand, a queen may benefit by increasing her contribution to brood production if having more daughter workers than her cofoundresses enhances her chances of taking over the colony. Increased investment is also beneficial because a large brood enhances colony survival. Using microsatellites, we determined the maternity of workers (adults and larvae) at the time of queen execution in the fire ant, Solenopsis invicta. Differential mass loss by initially equal nestmates affected survival, with the queen losing less body mass being more likely to survive. Surprisingly, the queen which lost less body mass, that is the one which provided the lowest energy investment, was the one which achieved higher maternity. A control experiment indicated that interactions among queens are responsible for this differential partitioning of reproductive and investment tasks between nestmates. The finding that the queen most likely to win the fights is the one with above-average maternity may explain why workers apparently do not attempt to influence the outcome of fights.     

How queen and workers share in male production in the stingless bee Melipona subnitida Ducke (Apidae, Meliponini)

Summary. Potential conflict between the queen and workers over the production of males is expected in stingless bees as a result of the higher relatedness of workers with their sons than with their brothers. This conflict was studied in Melipona subnitida by observing how the queen and the workers share in male production. The oviposition of individual cells was observed in two colonies with individually marked workers for a period of 51 and 40 days respectively. The gender that developed from these cells was then determined. The results revealed that most male production was concentrated in a 2–3-week period, during which laying workers were present. During these weeks, the queens produced twice as many males as all laying workers together. Outside this distinct period, the queens produced an occasional male. A reproductive worker either oviposited before the queen did, in which case she immediately proceeded to close the cell and thus prevented the queen from oviposition, or oviposited and sealed the cell after the queen had laid an egg. When cell construction and oviposition occured on several combs simultaneously, the workers preferentially laid male eggs on the newest combs. We discuss the proximate mechanism and ultimate cause of the way in which queen-worker male production occurred. In conclusion, we argue that overt behavioural conflict, occasionally displayed by reproductive workers of this species, can be of great cost to the colony.Received 27 February 2004; revised 6 September 2004; accepted 1 October 2004.     

Queen execution in a monogynous ant

Workers in many species of social insects are capable of laying unfertilized eggs, which can develop into haploid males. This causes a conflict about male parentage between queens and workers. In a few species, this may result in matricide, that is, workers kill the colony''s queen. Queen killing has so far been observed mainly in multi‐queen colonies or in annual species, when the queen''s fecundity declines at the end of the reproductive period. Here, we report queen expulsion and matricide in a monogynous, monandrous ant with perennial societies. Workers were seen to aggressively expel both related and unrelated queens from their nest shortly after the end of hibernation. Queen expulsion and matricide led to a significant decrease in the number of workers and brood, but eventually increased the direct fitness of workers through significant male production. Long‐term observations revealed a short lifespan of queens, while workers in orphaned colonies survived and produced male offspring over several years.     

Sex allocation conflict between queens and workers in Formica pratensis wood ants predicts seasonal sex ratio variation

Sex allocation theory predicts parents should adjust their investment in male and female offspring in a way that increases parental fitness. This has been shown in several species and selective contexts. Yet, seasonal sex ratio variation within species and its underlying causes are poorly understood. Here, we study sex allocation variation in the wood ant Formica pratensis. This species displays conflict over colony sex ratio as workers and queens prefer different investment in male and female offspring, owing to haplodiploidy and relatedness asymmetries. It is unique among Formica ants because it produces two separate sexual offspring cohorts per season. We predict sex ratios to be closer to queen optimum in the early cohort but more female‐biased and closer to worker optimum in the later one. This is because the power of workers to manipulate colony sex ratio varies seasonally with the availability of diploid eggs. Consistently, more female‐biased sex ratios in the later offspring cohort over a three‐year sampling period from 93 colonies clearly support our prediction. The resulting seasonal alternation of sex ratios between queen and worker optima is a novel demonstration how understanding constraints of sex ratio adjustment increases our ability to predict sex ratio variation.     

Queen-worker conflict over sex ratio: A comparison of primary and secondary sex ratios in the Argentine ant,Iridomyrmex humilis

We compare the primary sex ratio (proportion of haploid eggs laid by queens) and the secondary sex ratio (proportion of male pupae produced) in the Argentine ant Iridomyrmex humilis with the aim of investigating whether workers control the secondary sex ratio by selectively eliminating male brood. The proportion of haploid eggs produced by queens was close to 0.5 in late winter, decreased to less than 0.3 in spring and summer, and increased again to a value close to 0.5 in fall. Laboratory experiments indicate that temperture is a proximate factor influencing the primary sex ratio with a higher proportion of haploid eggs being laid at colder temperatures. Production of queen pupae ceased in mid-June, about three weeks before that of male pupae. After this time only worker pupae were produced. During the period of production of sexuals, the proportion of male pupae ranged from 0.30 to 0.38. Outside this period no males were reared although haploid eggs were produced all the year round by queens. Workers thus exert a control on the secondary sex ratio by eliminating a proportion of the male brood during the period of sexual production and eliminating all the males during the remainder of the cycle. These data are consistent with workers preferring a more female-biased sex ratio than queens. The evolutionary significance of the production of male eggs by queens all the year round is as yet unclear. It may be a mechanism allowing queen replacement in the case of the death of the queens in the colony.     

A Route to Direct Fitness: Natural and Experimentally Induced Queen Succession in the Tropical Primitively Eusocial Wasp <Emphasis Type="Italic">Ropalidia marginata</Emphasis>

Insect societies are hallmarks of cooperation because one or a few queens monopolize reproduction and several non-reproductive workers cooperatively raise brood. However, the loss of the queen exposes a colony to potential reproductive conflict, which is resolved only after a new queen takes over. We studied queen succession in natural and experimental colonies of the primitively eusocial wasp Ropalidia marginata to understand the proximate behavioral strategies involved in the resolution of this conflict. Previous work has shown that in this species, experimental queen removal always results in only one worker becoming hyper-aggressive and taking over the colony as its next queen, without ever being challenged. Here we show that even during natural queen turnover, one and only one worker becomes hyper-aggressive and takes over as the next queen, without being challenged. During natural queen turn-over, aggression of the successor may sometimes begin before the loss of the old queen and may sometimes decline more rapidly, unlike in the case of experimental queen removal. The successor begins to lay eggs sooner after a natural queen turn-over as compared to experimental queen removal. This is expected because workers might detect the gradual decline of the queen preceding her disappearance. Because queen succession is expected to be more prevalent in tropical perennial species, we expect natural selection to have favored such an orderly queen succession so that a route to direct fitness is available without significant reduction in cooperation.     

Conflict over male parentage in stingless bees

Summary Stingless bees usually have one, singly-mated queen. This can lead to a genetic conflict of interest between the queen and the non-laying workers over who should produce the males. In many stingless bee species workers have developed ovaries and can produce male-destined eggs. In this study we compile the available data on who produces the males in stingless bees. Worker reproduction is common but less frequent than expected from predictions built on relatedness-based preferences of non-laying workers. We tested whether the pattern in worker reproduction can be explained best by queen control, by an arms race between workers and their queen, by the costs of losing workers to reproductive competition, or by phylogenetic constraints. The data are consistent with the view that there is ongoing conflict over male production that is resolved differently depending on the specific dynamics of costs and benefits of worker reproduction. There was also a role for phylogeny; Melipona workers often reproduced while Plebeia and Australian stingless bee workers seldom or never did. The high worker reproduction in Melipona may reflect low costs, because many of the replaced queen-laid eggs would become excess queens.Received 17 April 2003; revised 2 September 2003; accepted 5 September 2003.     

Male parentage in army ants

In most social insects workers do not mate, but have retained the ability to produce haploid eggs that can develop into viable male offspring. Under what circumstances this reproductive potential is realized and how the ensuing worker-queen conflict over male production is resolved, is an area of active research in insect sociobiology. Here we present microsatellite data for 176 males from eight colonies of the African army ant Dorylus (Anomma) molestus. Comparison with worker genotypes and inferred queen genotypes from the same colonies show that workers do not or at best very rarely reproduce in the presence of the queen. Queens of D. (A.) molestus are known to be highly multiply mated. This implies that workers are on average more closely related to queen sons than to other workers' sons, so that our results are consistent with predictions from inclusive fitness theory. It remains unknown, however, whether worker sterility is maintained by active worker policing or by self-restraint.     

Worker policing persists in a hopelessly queenless honey bee colony (<Emphasis Type="Italic">Apis mellifera</Emphasis>)

Summary In queenright colonies of Apis mellifera, worker policing normally eliminates worker-laid eggs thereby preventing worker reproduction. However, in queenless colonies that have failed to rear a replacement queen, worker reproduction is normal. Worker policing is switched off, many workers have active ovaries and lay eggs, and the colony rears a last batch of male brood before dying out. Here we report a colony which, when hopelessly queenless, did not stop policing although a high proportion of workers had active ovaries (12.6%) and many eggs were laid. However, all these eggs and also worker-laid eggs transferred from another colony were policed. This unusual pattern was repeated eight weeks later by a second queenless colony made using worker bees from the same mother colony, which strongly suggests genetic determination.Received 19 May 2003; revised 11 September 2003; accepted 23 September 2003.