QUEEN SIGNALING IN SOCIAL WASPS

Social Hymenoptera are characterized by a reproductive division of labor, whereby queens perform most of the reproduction and workers help to raise her offspring. A long‐lasting debate is whether queens maintain this reproductive dominance by manipulating their daughter workers into remaining sterile (queen control), or if instead queens honestly signal their fertility and workers reproduce according to their own evolutionary incentives (queen signaling). Here, we test these competing hypotheses using data from Vespine wasps. We show that in natural colonies of the Saxon wasp, Dolichovespula saxonica, queens emit reliable chemical cues of their true fertility and that these putative queen signals decrease as the colony develops and worker reproduction increases. Moreover, these putative pheromones of D. saxonica show significant conservation with those of Vespula vulgaris and other Vespinae, thereby arguing against fast evolution of signals as a result of a queen–worker arms race ensuing from queen control. Lastly, levels of worker reproduction in these species correspond well with their average colony kin structures, as predicted by the queen signaling hypothesis but not the queen control hypothesis. Altogether, this correlative yet comprehensive analysis provides compelling evidence that honest signaling explains levels of reproductive division of labor in social wasps.     

The value of oviposition timing,queen presence and kinship in a social insect

Reproductive cooperation confers benefits, but simultaneously creates conflicts among cooperators. Queens in multi-queen colonies of ants share a nest and its resources, but reproductive competition among queens often results in unequal reproduction. Two mutually non-exclusive factors may produce such inequality in reproduction: worker intervention or queen traits. Workers may intervene by favouring some queens over others, owing to either kinship or queen signals. Queens may differ in their intrinsic fecundity at the onset of oviposition or in their timing of the onset of oviposition, leading to their unequal representation in the brood. Here, we test the role of queen kin value (relatedness) to workers, timing of the onset of oviposition and signals of presence by queens in determining the maternity of offspring. We show that queens of the ant Formica fusca gained a significantly higher proportion of sexuals in the brood when ovipositing early, and that the presence of a caged queen resulted in a significant increase in both her share of sexual brood and her overall reproductive share. Moreover, the lower the kin value of the queen, the more the workers invested in their own reproduction by producing males. Our results show that both kinship and breeding phenology influence the outcome of reproductive conflicts, and the balance of direct and indirect fitness benefits in the multi-queen colonies of F. fusca.     

Queen pheromone regulates egg production in a termite

In social insects, resource allocation is a key factor that influences colony survival and growth. Optimal allocation to queens and brood is essential for maximum colony productivity, requiring colony members to have information on the total reproductive power in colonies. However, the mechanisms regulating egg production relative to the current labour force for brood care remain poorly known. Recently, a volatile chemical was identified as a termite queen pheromone that inhibits the differentiation of new neotenic reproductives (secondary reproductives developed from nymphs or workers) in Reticulitermes speratus. The same volatile chemical is also emitted by eggs. This queen pheromone would therefore be expected to act as an honest message of the reproductive power about queens. In this study, we examined how the queen pheromone influences the reproductive rate of queens in R. speratus. We compared the number of eggs produced by each queen between groups with and without exposure to artificial queen pheromone. Exposure to the pheromone resulted in a significant decrease in egg production in both single-queen and multiple-queen groups. This is the first report supporting the role of queen pheromones as a signal regulating colony-level egg production, using synthetically derived compounds in a termite.     

Proximate Determinants of Reproductive Skew in Polygyne Colonies of the Ant Formica fusca

Understanding the determinants of reproductive skew (the partitioning of reproduction among co‐breeding individuals) is one of the major questions in social evolution. In ants, multiple‐queen nests are common and reproductive skew among queens has been shown to vary tremendously both within and between species. Proximate determinants of skew may be related to both queen and worker behaviour. Queens may attempt to change their reproductive share through dominance interactions, egg eating and by changing individual fecundity. Conversely, workers are in a position to regulate the reproductive output of queens when rearing the brood. This paper investigates queen behaviour at the onset of egg laying and the effect of queen fecundity and worker behaviour on brood development and reproductive shares of multiple queens in the ant Formica fusca. The study was conducted in two‐queen laboratory colonies where the queens produced only worker offspring. The results show that in this species reproductive apportionment among queens is not based on dominance behaviour and aggression, but rather on differences in queen fecundity. We also show that, although the queen fecundity at the onset of brood rearing is a good indicator of her final reproductive output, changes in brood composition occur during brood development. Our results highlight the importance of queen fecundity as a major determinant of her reproductive success. They furthermore suggest that in highly derived polygyne species, such as the Formica ants, direct interactions as a means for gaining reproductive dominance have lost their importance.     

Virgin queens selectively destroy fully matured queen cells in the honeybee <Emphasis Type="Italic">Apis mellifera</Emphasis> L.

Summary Experiments were carried out to determine how newly emerged virgin queens destroy queen cells with broods which will be competitors for the succession of the colony. When queen cells with older, 13-day-old broods set to emerge within 1 day were presented together with those of younger broods to workers and newly emerged queens in the colony, we found that the older queen cells were preferentially destroyed. It was also shown that a virgin queen destroyed the queen cells with older brood (12–13 days old) first when they were presented together with cells with younger broods (9–10 days old) simultaneously in the experimental cage. However, no significant preference was detected in the destruction between queen cells with 10- and 7-day-old broods. We concluded that virgin queens selectively destroy the queen cells housing broods which will emerge shortly. The possibility that by the selective destruction of older queen cells, newly emerged queens can reduce their risks including death that might otherwise be caused by fights with competitors was discussed.Received 10 June 2003; revised 22 December 2003; accepted 15 January 2004.     

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.     

Semi-claustral colony founding in the seed-harvester ant Pogonomyrmex californicus: a comparative analysis of colony founding strategies

The evolution of queens that rear their first brood solely using body reserves, i.e. fully claustral, is viewed as a major advance for higher ants because it eliminated the need for queens to leave the nest to forage. In an apparently unusual secondary modification, the seed-harvester ant Pogonomyrmex californicus displays obligate queen foraging, i.e. queens must forage to garner the resources necessary to survive and successfully rear their first brood. I examined the potential benefits of queen foraging by comparing ecological and physiological traits between P. californicus and several congeners in which the queen can rear brood using only body reserves. The primary advantage of foraging appears to lie in providing the queens of P. californicus with the energy to raise significantly more brood than possible by congeners that use only body reserves; the workers reared in the first brood were also heavier in mass than that predicted by their head width. Other correlates of queen foraging in P. californicus relative to tested congeners included a significantly lower total fat content for alate queens, a small queen body size, and a low queen to worker body mass ratio. Queens also forage in several other well-studied species of Pogonomyrmex, suggesting the possibility that queen foraging may be more common than previously thought in higher ants.     

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.     

Competition over workers: fertility signalling in wingless queens of <Emphasis Type="Italic">Hypoponera opacior</Emphasis>

The ant Hypoponera opacior exhibits alternative reproductive morphs associated with distinct sexual behaviours. Wingless, worker-like gynes mate in fall in their mother nest. Subsequently, these polygynous nests divide and wingless queens disperse on foot accompanied by workers, which help during nest foundation. Local resource competition amongst wingless queens was indicated by male-biased sex ratios. Queens compete over access to workers, and this competition manifests in dominance interactions. We colour-marked queens and workers to study this behaviour. Marked queens were treated aggressively and frequently killed by nestmates, whilst similarly labelled workers were readopted. We hypothesise that mated wingless queens—although they resemble workers in external morphology—differ chemically and that fertile queens with divergent odours are not tolerated. Thereby, sterile H. opacior workers avoid the risk to raise offsprings of unrelated queens. However, when nests split, workers should base their decision which queen to follow not only on relatedness, but also on queen fertility. Cuticular hydrocarbon profiles of queens could serve as an honest signal for workers. Indeed, gas chromatography showed that hydrocarbon composition differs between workers and mated queens and is linked to ovary development in queens. Workers and unmated queens exhibit complex profiles of short-chained hydrocarbons, whilst fertile queens carry few, long-chained alkenes and branched alkanes. Furthermore, ovary length was correlated to the relative amounts of characteristic hydrocarbons of queens. The chemical profile was also associated with eye size—an unalterable trait in adult insects—suggesting that larval nutrition and consequently body size affects adult ovary development.     

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.     

Queen control over reproductive decisions--no sexual deception in the ant Lasius niger

Queen-worker conflicts in social insect societies have received much attention in the past decade. In many species workers modify the colony sex ratio to their own advantage or produce their own male offspring. In some other species, however, queens seem to be able to prevent workers from making selfish reproductive decisions. So far, little effort has been made to find out how queens may keep control over sex ratio and male parentage. In this study we use a Lasius niger population under apparent queen control to show that sexual deception cannot explain queen dominance in this population. The sexual deception hypothesis postulates that queens should prevent workers from discriminating against males by disguising male brood as females. Contrary to the predictions of this hypothesis, we found that workers are able to distinguish male and female larvae early in their development: in early spring workers generally placed only either female or male larvae in the uppermost chambers of the nest, although both types of larvae must have been present. At this time males were only at 11% of their final dry weight, a developmental stage at which (according to two models) workers would still have benefited from replacing queen-produced males by females or worker-produced males. This study thus demonstrates that sexual deception cannot account for the apparent queen control over colony sex ratio and male parentage in L. niger.     

Independent colony founding by ergatoid queens in the ant genus Pogonomyrmex: queen foraging provides an alternative to dependent colony founding

Ant queens exhibit two primary strategies to initiate nests, independent colony founding (ICF) by solitary queens and dependent colony founding (DCF) when the queen starts a nest with a group of workers that disperse on foot from the parent nest. Numerous ant species have wingless (ergatoid) queens, and it is generally assumed that these species exhibit obligate DCF because their lack of wing musculature provides them with few resources to divert towards producing their first brood of workers. Thus, ICF by ergatoid queens is viewed as maladaptive because these queens need to take additional dangerous foraging trips to garner sufficient food to rear their first brood of workers. Contrary to this prediction, I document ICF by ergatoid queens for three species of harvester ants in the genus Pogonomyrmex (subfamily Myrmicinae), P. cunicularius cunicularius, P. cunicularius pencosensis, and P. huachucanus. Queens of P. huachucanus were obligate foragers, i.e., no minim workers could be produced without external food, and one queen of P. cunicularius pencosensis was observed foraging in the field. Abundant and/or predictable food resources likely select for the evolution of semi-claustral nest founding and ICF by these ergatoid queens. Under these conditions, foraging time would be minimized and the number and size of minim workers would be maximized. These benefits should increase founding success, which could compensate for loss of long-range dispersal. Overall, this study demonstrates that care should be taken before concluding that ant colonies employ DCF based solely on queen morphology.     

REPRODUCTIVE SKEW AND SPLIT SEX RATIOS IN SOCIAL HYMENOPTERA

Abstract I present a model demonstrating that, in social Hymenoptera, split sex allocation can influence the evolution of reproductive partitioning (skew). In a facultatively polygynous population (with one to several queens per colony), workers vary in their relative relatedness to females (relatedness asymmetry). Split sex‐ratio theory predicts that workers in monogynous (single‐queen) colonies should concentrate on female production, as their relatedness asymmetry is relatively high, whereas workers in the polygynous colonies should concentrate on male production, as their relatedness asymmetry is relatively low. By contrast, queens in all colonies value males more highly per capita than they value females, because the worker‐controlled population sex ratio is too female‐biased from the queens' standpoint. Consider a polygynous colony in a facultatively polygynous population of perennial, social Hymenoptera with split sex ratios. A mutant queen achieving reproductive monopoly would gain from increasing her share of offspring but, because the workers would assess her colony as monogynous, would lose from the workers rearing a greater proportion of less‐valuable females from the colony's brood. This sets an upper limit on skew. Therefore, in social Hymenoptera, skew evolution is potentially affected by queen‐worker conflict over sex allocation.     

Queen pheromones in Temnothorax ants: control or honest signal?

Background  

The division of reproductive labor among group members in insect societies is regulated by "queen pheromones". However, it remains controversial whether these are manipulative, i.e., actively suppress worker reproduction, or honestly signal the fertility status of the queen to which workers react in their own interest by refraining from laying eggs. Manipulative queen control is thought to lead to an evolutionary arms race between queens and workers, resulting in complex queen bouquets that diverge strongly among different populations and species. In contrast, honest signals would evolve more slowly and might therefore differ less strongly within and among species.     

Queen reproduction, chemical signalling and worker behaviour in polygyne colonies of the ant Formica fusca

Potential reproductive conflicts are common in social insects and may occur between and within castes. In multiqueen (polygyne) colonies of ants, reproductive conflicts among coexisting queens may be resolved by aggressive interactions and/or by pheromonal signalling. Pheromonal signals may be directed at workers, which may adjust the reproductive shares of queens behaviourally. Workers are expected to favour a queen that is more likely to be their mother and to produce offspring of close kin to them. We used microsatellite markers to study reproductive partitioning between cobreeding Formica fusca queens in a laboratory experiment where workers received a choice between two queens. We expected queens of this species to communicate their reproductive status by chemical communication, because no aggressive interactions between queens have been observed. We found that queens of different reproductive status (with majority, minority or no production) differed in their cuticular hydrocarbon (CHC) profiles. The fecundity of a queen was associated with worker behaviour; the higher a queen's fecundity, the more attention she received from workers. Our results suggest that a queen fecundity signal is encoded in her CHC profile and acts as a pheromone for workers, which respond to the signal by discriminating between queens. Copyright 2002 Published by Elsevier Science Ltd on behalf of The Association for the Study of Animal Behaviour     

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.     

Egg Cannibalism in a Facultative Polygynous Ant: Conflict for Reproduction or Strategy to Survive?

Policing, i.e. all behaviours that prevent a nestmate from reproducing, is currently observed in social insects. It is presumed to have evolved to regulate potential conflicts generated by genetic asymmetries or to enhance colony efficiency by avoiding surplus reproductives and brood. In the ant, Ectatomma tuberculatum, individual queen fecundity was similar in monogynous and polygynous colonies issued from a Mexican population. Egg cannibalism, however, occurred in the polygynous colonies. The stealing and destruction of reproductive queen‐laid eggs involved only nestmate queens, even if they were highly related. No queen appeared to monopolize reproduction in the polygynous colonies. But, the observed value of relatedness among workers differed from the expected value, suggesting an unequal sharing of reproduction between queens. We discussed whether the cannibalism of queen‐laid eggs in E. tuberculatum results from a competition for reproduction among queens or if this phenomenon is related to constraints on nutritional resources.     

Variation in social structure alters queen body mass and productivity in the desert seed-harvester ant Messor pergandei

Parent–offspring conflict theory predicts conflict between parents and their offspring over per-offspring resource investment. Across the range of the desert seed-harvester ant, Messor pergandei, daughter queens use three different social strategies during colony founding that are expected to alter the optimal level of parental investment. To test whether social strategy variation is associated with shifts in body mass, we surveyed queen live mass over 3 years at 25 sites that spanned the range of behavioral strategies and founding group sizes. To test whether reduction in parental investment into individual offspring negatively impacts their productivity, queens were individually isolated and allowed to produce a single worker cohort under common garden conditions. Queen live mass was highly variable, from 24 mg on average at the site with the lightest queens to 1.5 times that size, 37 mg, at the site with the heaviest queens. As predicted by parent–offspring conflict over investment, solitary colony founding sites contained the heaviest queens, followed by secondary monogyny. Polygynous queens were lightest, with a strong negative relationship between group size and live mass. Reductions in body mass had a negative effect on queen productivity across all queen social types; however, queens from sites where queen–queen aggression is typical were significantly more efficient at brood rearing, resulting in lower mass loss during founding per unit offspring biomass. This may represent an adaptation to queen competition to gain a strength advantage over potential rivals.     

Lack of conflict during queen production in the social wasp Vespula maculifrons

Social insects display extreme cooperative and helping behaviours. However, social insect colonies are also arenas of intense competitive interactions. One particularly important matter over which colony members may compete centres on the development of sexual offspring. Specifically, colony members may engage in selfish behaviours leading to reproductive competition, whereby individuals either strive to develop as sexuals or assist kin so that close relatives emerge as new reproductives. We investigated whether reproductive competition occurred in the polyandrous social wasp Vespula maculifrons. We genotyped V. maculifrons workers and new queens at eight polymorphic microsatellite loci to determine if larvae of particular genotypes were reared as gynes more frequently than expected by chance. However, we found no significant evidence of reproductive competition in this species. The proportional contributions of males to workers and new queens did not vary within colonies. Moreover, male reproductive skew did not differ between workers and new queens. Finally, novel statistical techniques uncovered no evidence of patriline reversal, the phenomenon whereby males that contribute little to worker production contribute substantially to new queen production. Consequently, we conclude that individual level selection operating to increase the frequency of selfish behaviours that would lead to reproductive competition has been nullified by colony-level selection acting to maintain colony efficiency and cooperation.     

Queen signal should be honest to be involved in maintenance of eusociality: chemical correlates of fertility in <Emphasis Type="Italic">Ropalidia marginata</Emphasis>

Queens of many social insect species are known to maintain reproductive monopoly by pheromonal signalling of fecundity. Queens of the primitively eusocial wasp Ropalidia marginata appear to do so using secretions from their Dufour’s glands, whose hydrocarbon composition is correlated with fertility. Solitary nest foundresses of R. marginata are without nestmates; hence expressing a queen signal can be redundant, since there is no one to receive the signal. But if queen pheromone is an honest signal inextricably linked with fertility, it should correlate with fertility and be expressed irrespective of the presence or absence of receivers of the signal, by virtue of being a byproduct of the state of fertility. Hence we compared the Dufour’s gland hydrocarbons and ovaries of solitary foundresses with queens and workers of post-emergence nests. Our results suggest that queen pheromone composition in R. marginata is a byproduct of fertility and hence can honestly signal fertility. This provides important new evidence for the honest signalling hypothesis.