Ontogeny of queen attraction to workers in the antCataglyphis cursor (Hymenoptera: Formicidae)

Summary The behaviour ofCataglyphis cursor workers towards queens at 15 days, one month or two months after worker emergence was tested. Workers reared entirely with their own maternal queen were tested with this queen or with an unfamiliar alien queen. Workers transferred within 48 h of emerging to a new definitive nest with an alien queen were tested with this queen or with the original maternal queen. The degree of attraction to each of these queens and the workers' behavioural repertoire were measured and analysed. The results showed the following: 1) The attractiveness of queens and the workers' queen recognition behaviour were linked. 2) Although unfamiliar alien queens hardly attract workers, familiar alien queens were as attractive as maternal queens, and induced the same strongly marked and unique worker response, indicating that workers learn queen attractant cues in the days immediately after emergence. 3) Agonistic reactions were observed, but workers continued to be attracted to their maternal queen even after developing an attraction response to an alien queen with which they had been reared. These results agree with the proposal that queens produce two kinds of pheromones, those that attract workers and those that mediate recognition of queens by workers. These results show the ability of workers to discriminate between queens. Workers are attracted to any queen, but recognize as nestmates only maternal or alien queens with which they have been maintained. 4) The differential in worker attraction and recognition from 15 days to 2 months and its modifications by post-imaginal experience illustrate worker behavioural ontogeny, which is a basis of social discrimination.     

Age and Behavior of Honey Bees,Apis mellifera (Hymenoptera: Apidae), that Perform Vibration Signals on Queens and Queen Cells

The vibration signal of the honey bee (Apis mellifera) may play a central role in the regulation of queen behavior during reproductive swarming and supersedure. We examined honey bee workers that performed vibration signals on queens and developing queen cells in three observation hives, each containing a population of marked bees of known age. In all three colonies, workers of all ages greater than 2 d old could perform vibration signals on queens and queen cells. However, most signals were performed by a small proportion of the bees of greater than 10 d of age. Relatively few workers less than 10 d old vibrated queens and queen cells, even though this age-group is typically associated with queen care. Thus, the regulation of queen behavior by the vibration signal may occur primarily through a relatively small subset of older workers that, under most circumstances, have only limited involvement with queens. It is unclear what triggers the vibrating of queens. Workers producing vibration signals did not differ from same-age non-vibrating controls in rate of locomotion in the hive or in task performance, and they rarely engaged in foraging, even though the majority of observed bees were of foraging age; vibrators also did not spend more time with queens and queen cells compared with controls. Vibration signals performed on queens and queen cells therefore do not appear to be influenced by task performance or increased contact with queens.     

Cheaters sometimes prosper: targeted worker reproduction in honeybee (Apis mellifera) colonies during swarming

Kin selection theory predicts that honeybee (Apis mellifera) workers should largely refrain from producing their own offspring, as the workers collectively have higher inclusive fitness if they rear the sons of their mother, the queen. Studies that have quantified levels of ovary activation and reproduction among workers have largely supported this prediction. We sampled pre‐emergent male pupae and adult workers from seven colonies at regular intervals throughout the reproductive part of the season. We show that the overall contribution of workers to male (drone) production is 4.2%, nearly 40 times higher than is generally reported, and is highest during reproductive swarming, when an average of 6.2% of the males genotyped are worker‐produced. Similarly, workers in our samples were 100 times more likely to have active ovaries than previously assumed. Worker reproduction is seasonally influenced and peaks when colonies are rearing new queens. Not all worker subfamilies contribute equally to reproduction. Instead, certain subfamilies are massively over‐represented in drone brood. By laying eggs within the period in which many colonies produce virgin queens, these rare worker subfamilies increase their direct fitness via their well‐timed sons.     

Kin structure and queen execution in the Argentine ant Linepithema humile

Every spring, workers of the Argentine Ant Linepithema humile kill a large proportion of queens within their nests. Although this behaviour inflicts a high energetic cost on the colonies, its biological significance has remained elusive so far. An earlier study showed that the probability of a queen being executed is not related to her weight, fecundity, or age. Here we test the hypothesis that workers collectively eliminate queens to which they are less related, thereby increasing their inclusive fitness. We found no evidence for this hypothesis. Workers of a nest were on average not significantly less related to executed queens than to surviving ones. Moreover, a population genetic analysis revealed that workers were not genetically differentiated between nests. This means that workers of a given nest are equally related to any queen in the population and that there can be no increase in average worker–queen relatedness by selective elimination of queens. Finally, our genetic analyses also showed that, in contrast to workers, queens were significantly genetically differentiated between nests and that there was significant isolation by distance for queens.     

The Behavior of Honey Bees (Apis mellifera ligustica) during Queen Duels

Conflict is rare among the members of a highly cooperative society such as a honey bee colony. However, conflict within a colony increases drastically during colony reproduction ('swarming') when newly produced queens fight each other until only one queen remains in the nest. This study describes the behavior of queens and workers during naturally occurring queen combat. The duels of five pairs of queens were observed in three observation colonies. A typical duel is described qualitatively and the events of all five duels are described quantitatively. Several aspects of duels that are of particular interest are examined in detail, including the behavior of queens near capped queen cells, worker aggression toward queens, queen tooting, and the relation of queen and worker behavior to the outcome of the duel. The results of this investigation serve as a foundation for rigorous tests of hypotheses regarding the adaptive significance of queen and worker behavior during queen combat. The results presented suggest that: young queens patrol queen cells to kill rival queens while they are vulnerable; workers aggress queens to prevent them from destroying queen cells; queens toot to inhibit worker aggression; workers immobilize queens to make them easy targets for rival queens; and queens eject hind-gut contents to cause their rival to be immobilized by the workers.     

Maternity of emergency queens in the Cape honey bee,Apis mellifera capensis

During reproductive swarming, some workers of the Cape honey bee, Apis mellifera capensis, lay eggs in queen cells, many of which are reared to maturity. However, it is unknown if workers are able to lay in queen cells immediately after queen loss during an episode of emergency queen rearing. In this study we experimentally de‐queened colonies and determined the maternity of larvae and pupae that were reared as queens. This allowed us to determine how soon after queen loss workers contribute to the production of new queens. We were further interested to see if workers would preferentially raise new queens from queen‐laid brood if this was introduced later. We performed our manipulations in two different settings: an apiary setting where colonies were situated close together and a more natural situation in which the colonies were well separated. This allowed us to determine how the vicinity of other colonies affects the presence of parasites. We found that workers do indeed contribute to queen cell production immediately after the loss of their queen, thus demonstrating that some workers either have activated ovaries even when their colony has a queen or are able to activate their ovaries extremely rapidly. Queen‐laid brood introduced days after queen loss was ignored, showing that workers do not prefer to raise new queens from queen brood when given a choice. We also detected non‐natal parasitism of queen cells in both settings. We therefore conclude that some A. m. capensis genotypes specialize in parasitizing queen cells.     

Attraction and Repellence of Workers by the Honeybee Queen (Apis mellifera L.)

The spatial distribution of worker honeybees in colonies of two African subspecies ( Apis mellifera capensis and Apis mellifera scutellata ), as well as their natural hybrids, was determined in five observation colonies, each containing one frame. The queens were allowed to roam freely throughout the hive during the initial phase of the experiment, and were observed on both sides of the frame in all colonies. In the second phase of the experiment the queen was caged on one side of the frame in three of the observation colonies, the other two colonies serving as controls. Queen caging significantly affected the distribution of worker bees, with more A. m. scutellata workers being attracted to the queen and more A. m. capensis worker bees being repelled by the presence of the queen. The hybrid workers were also repelled, but to a lesser extent. Queens thus not only attract workers to form a retinue or during swarming but also repel workers in the nest. Evasion of the reproductive suppression by the queen pheromones may be a typical behavior for workers with a high reproductive potential.     

Queen replacement in African and European honey bee colonies with and without afterswarms

We examined the dynamics of the queen replacement process in African and European colonies that did and did not produce afterswarms. In colonies without afterswarms, the queen replacement process was completed in 24–48 hours, the first-emerging virgin queen (VQ) typically inherited the natal nest even if multiple queens emerged, workers performed few vibration signals on emerged queens, and all signaling activity was directed toward early emerging VQs. In contrast, if colonies did produce afterswarms, the queen replacement process required 5–6 days, there was no advantage for first-emerging queens, vibration rates on emerged queens were 25 times greater, and signaling activity was directed toward all VQs. Although vibration signal activity was more pronounced in colonies with afterswarms, the signal was consistently associated with increased VQ survival under all conditions. These trends were exhibited similarly in the African and European colonies, suggesting that they have broad applicability to queen-replacement decisions over a range of environmental and racial conditions. However, the African and European colonies differed in the total number of queens involved in the elimination process and the relative importance of queen duels and pre-emergence destruction under the different reproductive strategies. Taken together, our results suggest that worker behavior is a major determinant for the outcome of queen replacement, either through reduced interactions that allow first-emerged queens to rapidly eliminate rivals, or through increased use of interactions such as the vibration signal, which may allow workers to influence the ultimate fate of each emerged VQ. We discuss the possibility that these behavior patterns may reflect the roles of cooperation and conflict in shaping honey bee reproductive decisions. Received 8 May 2007; revised 7 November 2007; accepted 20 November 2007.     

The sensitization of young workers to queens in the ant Myrmica rubra L.

The effect of workers, born into a queen-containing society, upon their subsequent broodrearing behaviour, was tested in the polygynous ant Myrmica rubra L., using small summer and large overwintered larvae. Workers, reared from the point of emergence in the presence of queens, had more control over larval growth compared with workers reared without queens. The current presence of queens had little influence. A critical period exists when young workers become sensitized and perhaps imprinted by the presence of queens. The character of the workers, size of the colony and the queen/worker ratio influence the degree of worker response towards queens and are discussed.     

Stay or drift? Queen acceptance in the ant <Emphasis Type="Italic">Formica paralugubris</Emphasis>

The acceptance of new queens in ant colonies has profound effects on colony kin structure and inclusive fitness of workers. Therefore, it is important to study the recognition and discrimination behaviour of workers towards reproductive individuals entering established colonies. We examined the acceptance rate of queens in populations of the highly polygynous ant F. paralugubris, where the genetic differentiation among nests and discrimination ability among workers suggest that workers might reject foreign queens. We experimentally introduced young queens in their natal nest and in foreign nests. Surprisingly, the survival rate of mated queens did not differ significantly when introduced in a foreign male-producing nest, a foreign female-producing nest, or the natal nest. Moreover, the survival of virgin queens in their natal nest was twice the one of mated queens, suggesting that mating status plays an important role for acceptance. The results indicate that other factors than queen discrimination by workers are implicated in the limited longdistance gene flow between nests in these populations. Received 8 April 2008; revised 16 June 2008; accepted 1 July 2008.     

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.     

Absence of nepotism toward imprisoned young queens during swarming in the honey bee

Nepotism is an important potential conflict in animal societies.However, clear evidence of nepotism in the rearing of queensin social insects is limited and controversial. In the honeybee, Apis mellifera, multiple mating by queens leads to thepresence of many patrilines within each colony. When the coloniesreproduce through swarming, workers rear a number of new queens,only a few of which will ultimately head a colony. Workers canpotentially increase their inclusive fitness by nepotisticallyfavoring full-sister over half-sister queens during the queenrearing and elimination process. Most studies have focused oninteractions between workers and immature queens (eggs and larvae)or adult queens who have exited their queen cells. However,adult queens often remain in their queen cells for up to 1 weekafter emerging from their pupa. In this situation, workers preventthe queens from emerging, feed them, and protect them from otheremerged queens. This stage in queen rearing is therefore onein which nepotism could occur. The current study is the firstto investigate the kinship between workers and adult queenswho have not emerged from their queen cells. We observed thefull suite of behaviors expected during this phase of colonyreproduction. Although there was no evidence for nepotism inthe worker–queen interactions, there was a nonrandom distributionacross patrilines of the workers interacting with the queencells. In addition, in one colony we found differential treatmentof fostered (nonkin)-queen cells.     

Size and composition of swarming colonies in Provespa anomala (Hymenoptera, Vespidae), a nocturnal social wasp

Summary: Ninety-eight nests of various growing stages of Provespa anomala were found in the lowlands of Sumatra, Indonesia, from August to January. Its colony cycle is considered to be annual, with nests built throughout the year. There were two types of early nests before the emergence of workers, one with a worker number of less than 63 and the other of more than 231. The former were new nests, each containing a new queen and were built by reproductive swarming, whereas each of the latter was possibly re-built by an old queen and an absconding swarm. Ten swarming colonies were attracted by an oil-lamp light; these consisted of a copulated queen with immature oocytes in the ovary and 55 workers on average. No males, or workers stylopized by Xenos provesparum were observed either in colonies before worker emergence or in swarms coming flying into the light. Differences between swarming in Provespa, polygyny and nest relocation in Vespa, and those in swarm-founding Polistinae are discussed.     

A quantitative study of worker reproduction in queenright colonies of the Cape honey bee, Apis mellifera capensis

Reproduction by workers is rare in honey bee colonies that have an active queen. By not producing their own offspring and preventing other workers from producing theirs, workers are thought to increase their inclusive fitness due to their higher average relatedness towards queen-produced male offspring compared with worker-produced male offspring. But there is one exception. Workers of the Cape honey bee, Apis mellifera capensis, are able to produce diploid female offspring via thelytokous parthenogenesis and thus produce clones of themselves. As a result, worker reproduction and tolerance towards worker-produced offspring is expected to be more permissive than in arrhenotokous (sub)species where worker offspring are male. Here we quantify the extent to which A. m. capensis workers contribute to reproduction in queenright colonies using microsatellite analyses of pre-emergent brood. We show that workers produced 10.5% of workers and 0.48% of drones. Most of the workers' contribution towards the production of new workers coincided with the colonies producing new queens during reproductive swarming.     

Worker interests and male production in Polistes gallicus, a Mediterranean social wasp

The resolution of social conflict in colonies may accord with the interests of the most numerous party. In social insect colonies with single once-mated queens, workers are more closely related to the workers' sons than they are to the queens' sons. Therefore, they should prefer workers to produce males, against the queen's interests. Workers are capable of producing males as they arise from unfertilized eggs. We found Polistes gallicus to have colonies of single, once-mated queens, as determined by microsatellite genotyping of the workers, so worker interests predict worker male production. In colonies lacking queens, workers produced the males, but not in colonies with original queens. Thus worker interests were expressed only when the queen was gone. The high fraction of missing queens and early end to the colony cycle relative to climate so early in the season is surprising and may indicate a forceful elimination of the queen.     

Colony strength and queen replacement in Melipona marginata (Apidae: Meliponini).

Physogastric queens of Melipona marginata were removed from their colonies in order to verify the acceptance of a new queen by workers. Colony strength was evaluated according to queen oviposition rate and comb diameters. Replacement was observed seven times. Its occurrence and speed related positively to colony strength, independently of queen's age. In weak colonies, queen replacement was observed only once, following colony population increase that occurred after introduction of combs from another colony. Worker oviposition after queen removal was observed three times: in a strong colony with virgin queens and males, and in two of the weak colonies. In the first two or three days of new queen oviposition, during which most of the eggs were eaten by the queen, worker oviposition preceded almost all provisioning and oviposition processes (POPs). After this period, worker oviposition decreased until it reached around 25% of the POPs. Daily oviposition rate of young queens decreased or was even interrupted by hatching of their first brood.     

Mate number,kin selection and social conflicts in stingless bees and honeybees

Microsatellite genotyping of workers from 13 species (ten genera) of stingless bees shows that genetic relatedness is very high. Workers are usually daughters of a single, singly mated queen. This observation, coupled with the multiple mating of honeybee queens, permits kin selection theory to account for many differences in the social biology of the two taxa. First, in contrast to honeybees, where workers are predicted to and do police each other''s male production, stingless bee workers are predicted to compete directly with the queen for rights to produce males. This leads to behavioural and reproductive conflict during oviposition. Second, the risk that a daughter queen will attack the mother queen is higher in honeybees, as is the cost of such an attack to workers. This explains why stingless bees commonly have virgin queens in the nest, but honeybees do not. It also explains why in honeybees the mother queen leaves to found a new nest, while in stingless bees it is the daughter queen who leaves.     

Reproductive parameters vary with social and ecological factors in the polygynous ant Formica exsecta

Due to their haplo‐diploid sex determination system and the resulting conflict over optimal sex allocation between queens and workers, social Hymenoptera have become important model species to study variation in sex allocation. While many studies indeed reported sex allocation to be affected by social factors such as colony kin structure or queen number, others, however, found that sex allocation was impacted by ecological factors such as food availability. In this paper, we present one of the rare studies that simultaneously investigated the effects of social and ecological factors on social insect nest reproductive parameters (sex and reproductive allocation, nest productivity) across several years. We found that the sex ratio was extremely male biased in a polygynous (multiple queens per nest) population of the ant Formica exsecta. Nest‐level sex allocation followed the pattern predicted by the queen‐replenishment hypothesis, which holds that gynes (new queens) should only be produced and recruited in nests with low queen number (i.e. reduced local resource competition) to ensure nest survival. Accordingly, queen number (social factor) was the main determinant on whether a nest produced gynes or males. However, ecological factors had a large impact on nest productivity and therefore on a nest's resource pool, which determines the degree of local resource competition among co‐breeding queens and at what threshold in queen number nests should switch from male to gyne production. Additionally, our genetic data revealed that gynes are recruited back to their parental nests after mating. However, our genetic data are also consistent with some adult queens dispersing on foot from nests where they were produced to nests that never produced queens. As worker production is reduced in gyne‐producing nests, queen migration might be offset by workers moving in the other direction, leading to a nest network characterized by reproductive division of labour. Altogether our study shows that both, social and ecological factors can influence long‐term nest reproductive strategies in insect societies.     

Influence of queen weight and colony origin on worker response in Solenopsis geminata

Abstract. The influence of weight and colony origin of the queen of Solenopsis geminata (F.) (Hymenoptera: Formicidae) on worker attraction is studied under laboratory conditions. In the first experiment, worker response to individual queens of different weight from the same colony is evaluated. Heavier queens are more attractive than smaller queens to their own workers. In subsequent experiments, the colony origin effect is investigated and worker response to a pair of queens of the same weight from the same or different colonies is compared. When queens are from the same colony, workers do not show a significant preference between queens. However, when queens are from a different colony, workers are significantly more attracted to their own queen than to the foreign queen. Finally, the response of workers to queens of different weight from the same or different colonies is investigated. In both cases, workers are significantly more attracted to a heavier queen than a lighter queen, even if the lighter queen is their own queen. A putative pheromonal component (E)‐6‐(1‐pentenyl)‐2H‐2‐pyranone, is not positively correlated with queen weight.     

REPRODUCTIVE CONFLICT IN BUMBLEBEES AND THE EVOLUTION OF WORKER POLICING

Worker policing (mutual repression of reproduction) in the eusocial Hymenoptera represents a leading example of how coercion can facilitate cooperation. The occurrence of worker policing in “primitively” eusocial species with low mating frequencies, which lack relatedness differences conducive to policing, suggests that separate factors may underlie the origin and maintenance of worker policing. We tested this hypothesis by investigating conflict over male parentage in the primitively eusocial, monandrous bumblebee, Bombus terrestris. Using observations, experiments, and microsatellite genotyping, we found that: (a) worker‐ but not queen‐laid male eggs are nearly all eaten (by queens, reproductive, and nonreproductive workers) soon after being laid, so accounting for low observed frequencies of larval and adult worker‐produced males; (b) queen‐ and worker‐laid male eggs have equal viabilities; (c) workers discriminate between queen‐ and worker‐laid eggs using cues on eggs and egg cells that almost certainly originate from queens. The cooccurrence in B. terrestris of these three key elements of “classical” worker policing as found in the highly eusocial, polyandrous honeybees provides novel support for the hypothesis that worker policing can originate in the absence of relatedness differences maintaining it. Worker policing in B. terrestris almost certainly arose via reproductive competition among workers, that is, as “selfish” policing.