Colony social organization of <Emphasis Type="Italic">Lasioglossum malachurum</Emphasis> Kirby (Hymenoptera,Halictidae) in southern Greece

Summary We studied the nesting and social biology of two aggregations of the obligately eusocial halictine bee Lasioglossum malachurum at Agios Nikolaos Monemvasias (ANM) in southern Greece. Observations and nest excavations carried out from May to June 2000, revealed social and demographic variation between aggregations and years at ANM, as well as notable differences between these and other European populations. In southern Greece, the colony cycle includes multiple broods: the first two broods comprise only workers, whereas the third brood comprises workers, males, and gynes. Although pleometrosis is unknown in other populations, in the ANM region, as many as 10% of nests have more than one foundress. Newly emerged workers and gynes exhibit non-overlapping size distributions, but a few queens are worker-sized, indicating that workers occasionally overwinter and become foundresses. Although the vast majority of workers are unmated and most exhibit no ovarian development, an increase in worker ovarian development at the time of male production suggests that many males may develop from worker-laid eggs. Worker reproduction seems to be inhibited by the presence of queens, and annual variation in queen mortality may underlie annual variation in worker ovarian development. Across Europe, the major demographic and social differences among L. malachurum populations are in the number of worker broods and the extent of worker ovarian development. This contrasts with the results of a principal components analysis of social traits among 15 social L. (Evylaeus) populations, which shows that interspecific social variation is defined by the proportion of males in the early brood, the proportion of workers mated, queen-worker size dimorphism, gyne overwintering locale, and the proportion of workers with developed ovaries.Received 17 June 2002; revised 16 January 2002; accepted 27 January 2003.     

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.     

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.     

Genetic relatedness and population structure in the social wasp,Mischocyttarus mexicanus (Hymenoptera: Vespidae)

Summary In primitively eusocial wasps workers often retain the ability to become queens, so their continued performance in the worker role is partly dependent on elevated genetic relatedness between workers and the brood they rear. In colonies of the social wasp,Mischocyttarus mexicanus, workers were related to female pupae by 0.29±0.12, a value that is significantly below the full sister value of 0.75, but not significantly below 0.50, worker relatedness to daughters. Though individuals often build new nests within meters of their natal nest, there was no genetic population structure discernable among four nest clusters, or inbreeding of any kind.     

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.     

A possible novel function of dominance behaviour in queen-less colonies of the primitively eusocial wasp Ropalidia marginata

Unlike the queens of other primitively eusocial species, Ropalidia marginata queens are strikingly docile and non-aggressive individuals, never at the top of the behavioural dominance hierarchy of their colonies. Nevertheless, these queens are completely successful at suppressing worker reproduction, suggesting that they do not use aggression but employ some other mechanism (e.g. pheromones) to do so. Upon removal of the queen from a colony, a single worker, the 'potential queen', immediately begins to display highly elevated levels of aggression towards her nest mates. This individual becomes the next docile queen if the original queen is not returned. We attempt to understand the function of the temporary and amplified dominance behaviour displayed by the potential queen. We find that the dominance behaviour shown by the potential queen is unrelated to the number of her nest mates, their dominance ranks or ovarian condition. This suggests that aggression may not be used to actively suppress other workers and counter threat. Instead we find evidence that dominance behaviour is required for the potential queen's rapid ovarian development, facilitating her speedy establishment as the sole reproductive individual in the colony.     

Ant workers selfishly bias sex ratios by manipulating female development.

Kin selection theory predicts that social insects should perform selfish manipulations as a function of colony genetic structure. We describe a novel mechanism by which this occurs. First, we use microsatellite analyses to show that, in a population of the ant Leptothorax acervorum, workers' relatedness asymmetry (ratio of relatedness to females and relatedness to males) is significantly higher in monogynous (single-queen) colonies than in polygynous (multiple-queen) colonies. Workers rear mainly queens in monogynous colonies and males in polygynous colonies. Therefore, split sex ratios in this population are correlated with workers' relatedness asymmetry. Together with significant female bias in the population numerical and investment sex ratios, this finding strongly supports kin-selection theory. Second, by determining the primary sex ratio using microsatellite markers to sex eggs, we show that the ratio of male to female eggs is the same in both monogynous and polygynous colonies and equals the overall ratio of haploids (males) to diploids (queens and workers) among adults. In contrast to workers of species with selective destruction of male brood, L. acervorum workers therefore rear eggs randomly with respect to sex and must achieve their favoured sex ratios by selectively biasing the final caste (queen or worker) of developing females.     

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.     

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.     

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.     

<Emphasis Type="Italic">Polistes japonicus</Emphasis> (Hymenoptera,Vespidae) queens monopolize ovipositing but are not the most active aggressor in dominant-subordinate interactions

In order to elucidate the dominant–subordinate relationship between the foundress and workers, five colonies of the paper wasp Polistes japonicus were observed in a netted and covered cage located outdoors. The number of workers in each colony ranged from four to eight. Workers were divided into first and second broods. Abdominal wagging and ovipositing were performed almost exclusively by the foundress throughout colony development. However, an analysis of aggressive encounters indicated that although the foundress hardly received dominance behaviors (aggression) from workers, it lacked either partially or completely the following characteristics of the queen that are usually seen in paper-wasp colonies with independent-founding queens (except in one colony that produced no second brood): the queen being socially dominant over any worker (the queen had more wins than losses in one-on-one dominance contests with any worker), exhibiting the highest frequency of dominance behaviors, and directing dominance behaviors primarily toward the socially most-dominant worker. In particular, during the mixed-brood period (when all first- and second-brood workers were present on the nest) the foundress hardly exhibited dominance behaviors toward socially dominant workers (mainly second brood) but frequently directed dominance behaviors toward socially subordinate workers (mainly first brood). The foundress disappeared in two colonies before the reproductives emerged; in these colonies the socially most-dominant worker inherited the colony and laid many eggs. The frequency of abdominal wagging by these two foundresses decreased during colony development, while it did not in the other colonies. This suggests that abdominal wagging provides information about the vigor of the performer. The superseder was socially dominant over all other workers, but spent little time wagging its abdomen and allowed some workers to lay eggs.     

蜜蜂群内生殖分工体系的形成及其维持

本文对蜜蜂群内生殖分工体系的形成及其维持机制进行综述。蜜蜂群体具有完善的劳动分工(包括生殖分工)体系,蜂王垄断生殖权力,而工蜂生殖器官发育不完全,在蜂王信息素和幼虫信息素的作用下产卵受到抑制。蜂王的多雄交配机制降低了群内个体间的亲缘关系,但也促进了工蜂间相互监督机制的形成。工蜂间的相互监督,结合蜂王和幼虫信息素对工蜂卵巢发育的影响,解决了蜂王与工蜂、工蜂与工蜂间的生殖利益冲突,保障了蜂群内的生殖分工体系,提高了群体效率,维护了蜂群的真社会性。     

The behaviour of queen honeybees and their attendants

Abstract. The behaviour of queen and worker honeybees (Apis mellifera L.) was observed using small colonies in observation hives. Workers paid more attention to queens which had been mated for 2 months or more than to those which were newly mated; virgin queens received least attention. Queens received most attention when they were stationary and least when they were walking over the comb; virgin queens were most active. Queen cells had as many attendants as virgin queens and queen larvae were inspected almost continuously. The queen pheromone component 9–oxo-trans-2–decenoic acid stimulated 'court' behaviour when presented on small polyethylene blocks, but workers responded aggressively to complete extracts of queens' heads. Both the heads and abdomens of mated queens received much attention from court workers but the abdomens were palpated by more workers for longer and were licked much more. The queens' thoraces were least attended. Abdominal tergites posterior to tergite glands were licked for longer than those anterior to the glands. Only worker bees very near to the queen reacted to her and joined her 'court'.
No evidence was found of a diel periodicity in the behaviour of a queen or her 'court'. During the winter the queen's court was smaller than in summer and she walked less and laid fewer eggs. When colonies were fed with sucrose syrup in winter, their queens laid more eggs and workers reared more brood but there was no change in the attention received by the queens.
The implications of these findings for the secretion and distribution of queen pheromones are discussed.     

Intraspecific usurpation of incipient fire ant colonies

Brood raiding, or reciprocal stealing of brood, is common amongincipient colonies of the fire ant Solenopsis invicta. Paradoxically,workers from a colony that loses its brood during a raid oftenabandon their nest and join the winning colony. Queens abandonedby their workers may then migrate from their original nest siteand attempt to forcefully usurp another incipient colony bydisplacing that colony's queen or queens. This study examinedfactors that influence the success of usurpation attempts. Queensattempting to usurp a nearby colony after laboratory brood raidswere successful in less than 30% of trials. Usurpation attemptswere more successful if workers familiar to the migrating queenwere present in the nest, as would happen if a queen were tofind the colony to which her workers had moved. Cross-fosteringexperiments showed that this effect was due to familiarity ratherthan relatedness. Usurpation attempts were less successful ifthey were delayed by 16 h. The probability of usurpation successwas not reduced by doubling the number of defending workersin the invaded colony. However, colonies founded by three queenswere almost always able to resist usurpation attempts. Theseresults support the hypothesis that workers abandon their natalcolony after losing a brood raid to increase the likelihoodthat their queen can usurp the colony to which they migrate.These results also provide the first evidence that coloniesof ants founded by several queens are better able to resistusurpation attempts than colonies founded by a single queen     

Breeding system and reproductive skew in a highly polygynous ant population

Factors affecting relatedness among nest members in ant colonies with high queen number are still poorly understood. In order to identify the major determinants of nest kin structure, we conducted a detailed analysis of the breeding system of the ant Formica exsecta. We estimated the number of mature queens by mark-release-recapture in 29 nests and dissected a sub-sample of queens to assess their reproductive status. We also used microsatellites to estimate relatedness within and between all classes of nestmates (queens, their mates, worker brood, queen brood and male brood). Queen number was very high, with an arithmetic mean of 253 per nest. Most queens (90%) were reproductively active, consistent with the genetic analyses revealing that there was only a minimal reproductive skew among nestmate queens. Despite the high queen number and low reproductive skew, almost all classes of individuals were significantly related to each other. Interestingly, the number of resident queens was a poor predictor of kin structure at the nest level, consistent with the observation that new queens are produced in bursts leading to highly fluctuating queen number across years. Queen number also varied tremendously across nests, with estimates ranging from five to several hundred queens. Accordingly, the harmonic mean queen number (40.5) was six times lower than the arithmetic mean. The variation in queen number was the most important factor of the breeding system contributing to a significant relatedness between almost all classes of nestmates despite a high average number of queens per nest. Electronic supplementary material  The online version of this article (doi:) contains supplementary material, which is available to authorized users. Received 12 November 2007; revised 4 May 2008; accepted 8 May 2008.     

An alternative strategy for maintenance of eusociality after nest destruction: new nest construction in a primitively eusocial wasp

Although nests are central to colonial life in social insects, nests are sometimes damaged by predators or natural disasters. After nest destruction, individuals usually construct new nests. In this case, a sophisticated mechanism like the scent trail pheromone used in large insect colonies that recruit individuals to new nest sites would be important for the maintenance of eusociality. In independent-founding Polistes wasps, it is well known that queens enforce workers physiologically on the natal nests even if evidence of trail pheromone use has not been exhibited. We investigated the effect of the queen on an alternative strategy for the maintenance of eusociality by first females after nest destruction in the primitively eusocial wasp Polistes chinensis. We predicted that the first females in queen-absent colonies have various behavioral options after nest destruction. Even if the females construct new nests cooperatively with other individuals, the new nest construction should be conducted more smoothly in queen-present colonies because the queens regulate the behavior of wasps. We made wasps construct new nests by removing the entire brood from existing nests. The presence of the queen did not cause variation in the alternative strategy of the first females, as the first females (workers) usually constructed new nests cooperatively irrespective of the queen-presence. Thus, the workers in the queenpresent colonies affiliated to the new nest construction more smoothly and constructed new nests more efficiently than workers in the queen-absent colonies. Our results suggest that the presence of the queen is important for maintaining eusociality in primitively eusocial wasps after nest destruction. Received 8 February 2005; revised 5 October 2005; accepted 17 October 2005.     

Workers influence royal reproduction

Understanding which parties regulate reproduction is fundamental to understanding conflict resolution in animal societies. In social insects, workers can influence male production and sex ratio. Surprisingly, few studies have investigated worker influence over which queen(s) reproduce(s) in multiple queen (MQ) colonies (skew), despite skew determining worker-brood relatedness and so worker fitness. We provide evidence for worker influence over skew in a functionally monogynous population of the ant Leptothorax acervorum. Observations of MQ colonies leading up to egg laying showed worker aggressive and non-aggressive behaviour towards queens and predicted which queen monopolized reproduction. In contrast, among-queen interactions were rare and did not predict queen reproduction. Furthermore, parentage analysis showed workers favoured their mother when present, ensuring closely related fullsibs (average r = 0.5) were reared instead of less related offspring of other resident queens (r ≤ 0.375). Discrimination among queens using relatedness-based cues, however, seems unlikely as workers also biased their behaviour in colonies without a mother queen. In other polygynous populations of this species, workers are not aggressive towards queens and MQs reproduce, showing the outcome of social conflicts varies within species. In conclusion, this study supports non-reproductive parties having the power and information to influence skew within cooperative breeding groups.     

Parasites delay worker reproduction in bumblebees: consequences for eusociality

Workers in eusocial insects usually tend the brood of the queenand so achieve representation in the next generation throughaiding relatives to reproduce. However, workers of some eusocialspecies, such as bumblebees, are capable of reproductive activityeven in the presence of the queen (in queen-right colonies),and worker reproduction is associated with aggressive behaviorsand egg cannibalism, both of which reduce colony efficiency.Thus, factors that affect worker ovariandevelopment, a preconditionfor reproduction, can influence social harmony and colony productivity.Parasites are a ubiquitous and important part of the bioticenvironment of all organisms. Here we show that parasites playan important role in the reproductive physiology of worker bumblebeesin queen-right colonies of Bombus terrestris, affecting thepattern and timing of ovarian development and oviposition. Workersfrom colonies parasitized with the intestinal trypanosome Crithidiabombi had less developed ovaries than workers of the same agefrom unparasitized colonies. In addition, parasitized colonieswere smaller than unparasitized colonies for about the firsthalf of colony development. This generated further demographiceffects such that workers were on average younger in parasitizedthan in unparasitized colonies around the time of the onsetof worker oviposition, and worker oviposition occurred significantlylater in parasitized colonies. Workers in parasitized coloniestherefore had lower individual reproductive potential and werecooperative for a larger proportion of the colony cycle thanthose in unparasitized colonies. In this system, where transmissionof the parasite between years probably occurs only in infested,young queens, this effect may represent an adaptation on thepart of the parasite to ensure its successful passage throughthe winter. Parasites, by reducing the cost of worker cooperation,may facilitate queen control over her worker force and playan important role in moderating the social organization of eusocialinsect colonies.     

The effects of honey bee (Apis mellifera L.) queen reproductive potential on colony growth

Reproduction in species of eusocial insects is monopolized by one or a few individuals, while the remaining colony tasks are performed by the worker caste. This reproductive division of labor is exemplified by honey bees (Apis mellifera L.), in which a single, polyandrous queen is the sole colony member that lays fertilized eggs. Previous work has revealed that the developmental fate of honey bee queens is highly plastic, with queens raised from younger worker larvae exhibiting higher measures in several aspects of reproductive potential compared to queens raised from older worker larvae. Here, we investigated the effects of queen reproductive potential (“quality”) on the growth and winter survival of newly established honey bee colonies. We did so by comparing the growth of colonies headed by “high-quality” queens (i.e., those raised from young worker larvae, which are more queen-like morphologically) to those headed by “low-quality” queens (i.e., those raised from older worker larvae, which are more worker-like morphologically). We confirmed that queens reared from young worker larvae were significantly larger in size than queens reared from old worker larvae. We also found a significant positive effect of queen grafting age on a colony’s production of worker comb, drone comb, and stored food (honey and pollen), although we did not find a statistically significant difference in the production of worker and drone brood, worker population, and colony weight. Our results provide evidence that in honey bees, queen developmental plasticity influences several important measures of colony fitness. Thus, the present study supports the idea that a honey bee colony can be viewed (at least in part) as the expanded phenotype of its queen, and thus selection acting predominantly at the colony level can be congruent with that at the individual level.     

Gene expression patterns associated with caste and reproductive status in ants: worker‐specific genes are more derived than queen‐specific ones

Variation in gene expression leads to phenotypic diversity and plays a central role in caste differentiation of eusocial insect species. In social Hymenoptera, females with the same genetic background can develop into queens or workers, which are characterized by divergent morphologies, behaviours and lifespan. Moreover, many social insects exhibit behaviourally distinct worker castes, such as brood‐tenders and foragers. Researchers have just started to explore which genes are differentially expressed to achieve this remarkable phenotypic plasticity. Although the queen is normally the only reproductive individual in the nest, following her removal, young brood‐tending workers often develop ovaries and start to reproduce. Here, we make use of this ability in the ant Temnothorax longispinosus and compare gene expression patterns in the queens and three worker castes along a reproductive gradient. We found the largest expression differences between the queen and the worker castes (~2500 genes) and the smallest differences between infertile brood‐tenders and foragers (~300 genes). The expression profile of fertile workers is more worker‐like, but to a certain extent intermediate between the queen and the infertile worker castes. In contrast to the queen, a high number of differentially expressed genes in the worker castes are of unknown function, pointing to the derived status of hymenopteran workers within insects.