Swarming generates rebel workers in honeybees

According to kin selection theory, the colony kin structure of eusocial insects motivates workers' altruistic behaviors and therefore their sterility or restricted reproduction [1]. Indeed, theory and cross-species comparison confirm that workers engage in their own reproduction depending on relatedness among colony members [2, 3]. We show that in a honeybee colony, the workers switch from their typical altruistic role to a more selfish one if at their larval stage there are environmental cues of an upcoming decline in intracolony relatedness. This happens inevitably when a colony multiplies by swarming and replaces the mother queen with her daughter, because the mother queen's workers are faced with rearing the sister queen's offspring related to them half as much as between sisters. Workers developing from the mother queen's eggs immediately after swarming, in a temporarily queenless colony, had more ovarioles in their ovaries and less-developed hypopharyngeal glands producing brood food than control workers reared in queenright conditions. These "rebel" workers were more engaged in laying their own male-determined eggs than in rearing offspring, whether or not the sister queen was present in the colony. The finding of this previously unknown rebel strategy confirms that kin selection shapes both cooperation and conflict in honeybee societies.     

Cuticular hydrocarbon profiles differ between ant body parts: implications for communication and our understanding of CHC diffusion

Insect cuticular hydrocarbons (CHCs) serve as communication signals and protect against desiccation. They form complex blends of up to 150 different compounds. Due to differences in molecular packing, CHC classes differ in melting point. Communication is especially important in social insects like ants, which use CHCs to communicate within the colony and to recognize nestmates. Nestmate recognition models often assume a homogenous colony odor, where CHCs are collected, mixed, and redistributed in the postpharyngeal gland (PPG). Via diffusion, recognition cues should evenly spread over the body surface. Hence, CHC composition should be similar across body parts and in the PPG. To test this, we compared CHC composition among whole-body extracts, PPG, legs, thorax, and gaster, across 17 ant species from 3 genera. Quantitative CHC composition differed between body parts, with consistent patterns across species and CHC classes. Early-melting CHC classes were most abundant in the PPG. In contrast, whole body, gaster, thorax, and legs had increasing proportions of CHC classes with higher melting points. Intraindividual CHC variation was highest for rather solid, late-melting CHC classes, suggesting that CHCs differ in their diffusion rates across the body surface. Our results show that body parts strongly differ in CHC composition, either being rich in rather solid, late-melting, or rather liquid, early-melting CHCs. This implies that recognition cues are not homogenously present across the insect body. However, the unequal diffusion of different CHCs represents a biophysical mechanism that enables caste differences despite continuous CHC exchange among colony members.     

Fitness in invasive social wasps: the role of variation in viral load,immune response and paternity in predicting nest size and reproductive output

Within any one habitat, the relative fitness of organisms in a population can vary substantially. Social insects like the common wasp are among the most successful invasive animals, but show enormous variation in nest size and other fitness‐related traits. Some of this variation may be caused by pathogens such as viruses that can have serious consequences in social insects, which range from reduced productivity to colony death. Both individual immune responses and colony‐level traits such as genetic diversity are likely to influence effects of pathogen infections on colony fitness. Here we investigate how infections with Kashmir Bee Virus (KBV), immune response and intracolony genetic diversity (due to queen polyandry) affect nest size in the invasive common wasp Vespula vulgaris. We show that KBV is highly prevalent in wasps and expression of antiviral immune genes is significantly increased with higher viral loads across individuals. Patriline membership within a nest did not influence KBV susceptibility or immune response. A permutational MANCOVA revealed that polyandry, viral load and expression of the immune gene Dicer were significant predictors of variation in nest size. High intracolony genetic diversity due to polyandry has previously been hypothesized to improve colony‐level resistance to parasites and pathogens. Consistent with this hypothesis, we observed genetically diverse colonies to be significantly larger and to produce more queens, although this effect was not driven by the pathogen we investigated. Invasive wasps clearly suffer from pathogens and expend resources, as indicated here by elevated immune gene expression, toward reducing pathogen‐impact on colony fitness.     

Genetic population structure, queen supersedure and social polymorphism in a social Hymenoptera

In social insects, the emergence of multiple queening is linked to changes in a suite of traits such as the reproductive life span of queens, mating patterns and population structure. We investigated queen turnover, colony longevity, spatial distribution patterns and genetic differentiation in a population of the socially polymorphic ant Formica fusca. Genetic differentiation between the social forms was absent, and mating patterns were similar in the two forms. The spatial distribution of single- and multi-queen colonies indicated an absence of colony reproduction by budding in both colony types. However, the rate of queen supersedure was high in multi-queen colonies and absent in single-queen ones. The social structure of colonies remained stable across years, but colony mortality did not differ between the two social forms. These results imply that differences between social types may appear and persist also in sympatry, and that these differences may occur in some traits, but not others, despite the presence of homogenizing gene flow.     

Effect of food restriction on survival and reproduction of a termite

Food availability affects the trade-off between maintenance and reproduction in a wide range of organisms, but its effects on social insects remain poorly understood. In social insects, the maintenance-reproduction trade-off seems to be absent in individuals but may appear at the colony level, although this is rarely investigated. In this study, we restricted food availability in a termite species to test how it affects survival and reproduction, both at the individual and colony level. Using Bayesian multivariate response models, we found very minor effects of food restriction on the survival of queens, individual workers or on the colonies. In contrast, queen fecundity was significantly reduced, whereas colony-level fecundity (i.e., the number of dispersing alates, future reproductives) increased under food restriction as workers gave up cooperation within the colony and became alates that dispersed. Our study shows that life-history trade-offs can be mitigated by individuals' social behaviours in social organisms.     

Experimentally induced variation in the physical reproductive potential and mating success in honey bee queens

In honeybee colonies, reproduction is monopolized by the queen while her daughter workers are facultatively sterile. Caste determination is a consequence of environmental conditions during development, during which female larvae may become either queens or workers depending on their larval diet. This bipotency introduces significant variation in the reproductive potential of queen bees, with queens raised from young worker larvae exhibiting high reproductive potential and queens raised from older worker larvae exhibiting lower reproductive potential. We verify that low-quality queens are indeed produced from older worker larvae, as measured morphometrically (e.g., body size) and by stored sperm counts. We also show, for the first time, that low-quality queens mate with significantly fewer males, which significantly influences the resultant intracolony genetic diversity of the worker force of their future colonies. These results demonstrate a reproductive continuum of honeybee queens and provide insights into the reproductive constraints of social insects.     

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.     

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.     

Trophallaxis and reproductive conflicts in social bees

In the eusocial Hymenoptera, reproductive division of labour is a key aspect of colony organisation. In most of its species, workers are sterile and are unable to reproduce, while the queen monopolises reproduction. When workers are able to reproduce, a conflict with the queen or with other workers over male production is predicted. Because this reproduction may involve costs for the colony, the potential conflict over male parentage gives rise to important questions, such as what are the proximate mechanisms that allow a queen to control the reproductive potential of its workers, and which factors make some workers fertile and others not. In the groups where it occurs, an important mechanism for the regulation of reproduction is trophallaxis (the process of mutual feeding through regurgitation that occurs in several species of social insects). Trophallaxis gives dominant individuals a trophic advantage by taking nutrients from submissive individuals. In advanced eusocial species of bees, trophallaxis may also serve as an alternative hierarchical interaction in the absence of agonistic conflicts. In this way, trophallaxis not only represents an alternative path for hierarchical interactions, but it may be evolutionary linked to intracolonial conflict among workers.     

Effect of habitat saturation on the number and turnover of queens in the polygynous ant,Myrmica sulcinodis

In polygynous social insects more than one queen reproduces in a colony. In such populations ecological factors affecting survival and reproduction of queens are likely to be of prime importance for social organization. In particular, habitat saturation leading to severe limitations in the availability of nest sites has been suggested to promote high queen number. In this study we examine the social and genetic structure of colonies in the polygynous ant Myrmica sulcinodis. We investigated a single breeding population in two adjacent habitats which differed markedly in the availability of nest sites. In the main habitat M. sulcinodis occupied almost all suitable nest sites, whereas in the other (marginal) habitat most sites were unoccupied by ants, due to a recent fire. In support of the habitat saturation hypothesis, the number of queens per colony which could explain the estimated relatedness among workers was almost five times higher for the main habitat than for the marginal habitat. This is the first demonstration that the kin structure of a social insect population is plastic and responds adaptively to short-term changes in ecological constraints such as nest site availability. Based on combined genetic and demographic data we discuss queen reproductive strategies and suggest that a special class of queen ‘floaters’ only stays ephemerally in the colonies, thus causing a substantial turnover of reproducing queens across years.     

Colony social structure in native and invasive populations of the social wasp Vespula pensylvanica

Social insects rank among the most invasive of terrestrial species. The success of invasive social insects stems, in part, from the flexibility derived from their social behaviors. We used genetic markers to investigate if the social system of the invasive wasp, Vespula pensylvanica, differed in its introduced and native habitats in order to better understand variation in social phenotype in invasive social species. We found that (1) nestmate workers showed lower levels of relatedness in introduced populations than native populations, (2) introduced colonies contained workers produced by multiple queens whereas native colonies contained workers produced by only a single queen, (3) queen mate number did not differ significantly between introduced and native colonies, and (4) workers from introduced colonies were frequently produced by queens that originated from foreign nests. Thus, overall, native and introduced colonies differed substantially in social phenotype because introduced colonies more frequently contained workers produced by multiple, foreign queens. In addition, the similarity in levels of genetic variation in introduced and native habitats, as well as observed variation in colony social phenotype in native populations, suggest that colony structure in invasive populations may be partially associated with social plasticity. Overall, the differences in social structure observed in invasive V. pensylvanica parallel those in other, distantly related invasive social insects, suggesting that insect societies often develop similar social phenotypes upon introduction into new habitats.     

蜜蜂嗅觉相关蛋白的研究进展

蜜蜂是一类营社会性生活的昆虫,蜂群中的蜂王、工蜂和雄蜂相互依存,各司其职,共同维持着群体严密有序的生活。其中,嗅觉系统在它们的生存和繁衍过程中起到重要的作用。昆虫对气味物质的感受过程是非常复杂的,需要有多种蛋白的参与。研究蜜蜂的化学感受机制可以帮助我们更深入地了解蜜蜂特有的行为及生物学特性。本文重点综述了与蜜蜂嗅觉相关的3种蛋白质的生化特性、分子结构、基因表达及其生理功能等方面的研究进展,以期为今后开展相关研究工作提供理论参考。     

Workers do not mediate the inhibitory power of queens in a termite, <Emphasis Type="Italic">Reticulitermes speratus</Emphasis> (Isoptera,Rhinotermitidae)

In social insects, the caste systems are based on reproductive division of labor; queens specialize in reproduction and workers primarily maintain the colony. Recently, a volatile pheromone containing n-butyl-n-butyrate and 2-methyl-1-butanol was identified as a termite queen pheromone that inhibits the differentiation of female neotenic reproductives (secondary queens). Although this volatile inhibitory pheromone regulates caste differentiation directly, the method by which it reaches members without direct contact with the queen in large colonies is not well understood. Therefore, additional mechanisms of indirect communication must exist, such as worker-mediated queen signal transport. We found that workers exposed to female reproductives did not mediate queens’ inhibitory signal in a termite Reticulitermes speratus. The experiment assessed worker transfer from direct to indirect contact groups and determined that the differentiation of new female reproductives in the indirect contact groups was not influenced by the direct contact groups, whereas direct contact with functional female reproductives and artificial queen pheromone did suppress neotenic differentiation. This suggests that worker transfer of the queen signal is unlikely and that for colony-wide inhibition direct contact by the majority of infertile members with reproductives or eggs, which emit the same volatiles as female reproductives, is necessary within a certain time interval.     

Ontogeny of cephalic volatile patterns in queens and mating biology of the neotropical stingless bee,Scaptotrigona postica

Summary

Chemical communication is an ancient yet still immensely important part of reproduction. Amongst all invertebrates, the most sophisticated “chemical languages” are used by social insects. Here the sex- and caste-specific pheromonal messages consist of multicomponent mixtures. In the neotropical stingless bee Scaptotrigona postica, an inhabitant of dense tropical rain forests, the cephalic volatiles of a queen transmit information on her reproductive status to males. A distinct ontogenetic pattern of the queen pheromone composition allows drones to discriminate receptive virgins which are then chased during the short nuptial flight through the forest understorey. By means of gas chromatographic/mass spectroscopic analyses, the numerous volatile compounds found in pentane extracts of individual bee heads could be identified. Qualitative as well as quantitative changes of these volatiles in the course of imaginal development could be determined, and bioassays with synthetic compounds were undertaken in order to decode the chemical signals used during the short encounter of a young queen and her mate.     

Colony-level chemical profiles do not provide reliable information about colony size in the honey bee

1. Chemical communication facilitates colony function across social insects, providing workers with information about individual and colony state. Although workers use chemical cues to detect developmental transitions in individuals, it is unknown whether workers can also use colony-level chemical profiles to detect the developmental state of their colony. Indeed, it is largely unknown how colony-level chemical profiles change as colonies grow and develop. 2. Reproductive onset is a major developmental transition and, in the honey bee, Apis mellifera, colonies must surpass a threshold colony size before workers will invest in reproduction. Given the ubiquity of chemical communication, the present study investigated whether colony-level chemical profiles change with colony size. 3. Chemical compounds deposited by workers of three colony sizes (5000, 10 000, 15 000 workers) collected over a 4-day time-series (0, 12, 24, 48, 72, and 96 h), as well as worker cuticular lipids, were sampled. 4. In total, 26 compounds deposited on nest surfaces and 20 compounds in worker cuticular lipids were identified; it took up to 24 h for sampled nest surfaces to reach saturation in the number and amount of deposited compounds. 5. Among these compounds, no qualitative or quantitative indicators of colony size were found, suggesting that deposited chemical compounds are not semiochemicals in this context. Volatile pheromones have also been shown previously to not play a role in signaling colony size. Therefore, honey bee workers are unlikely to use deposited chemical cues to detect colony size, and must rely instead on other modalities, such as physical cues of worker density.     

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

The regulation of reproductive division of labour is a key component in the evolution of social insects. Chemical signals are important mechanisms to regulate worker reproduction, either as queen-produced pheromones that coercively inhibit worker reproduction or as queen signals that honestly advertise her fecundity. A recent study suggested that a conserved class of hydrocarbons serve as queen pheromones across three independent origins of eusociality. In bumblebees (Bombus terrestris), pentacosane (_C25) was suggested to serve as a queen pheromone. Here, we repeat these studies using a different species of bumblebee (Bombus impatiens) with a more controlled experimental design. Instead of dequeened colonies, we used same-aged, three-worker queenless groups comprising either experienced or naive workers (with/without adult exposure to queen pheromone). We quantified three hydrocarbons (_C23, _C25 and _C27) on the cuticular surfaces of females and tested their effects on the two worker types. Our results indicate differences in responses of naive and experienced workers, genetic effects on worker reproduction, and general effects of hydrocarbons and duration of egg laying on ovary resorption rates. However, we found no evidence to support the theory that a conserved class of hydrocarbons serve as queen pheromones or queen signals in Bombus impatiens.     

Colony fusion and worker reproduction after queen loss in army ants

Theory predicts that altruism is only evolutionarily stable if it is preferentially directed towards relatives, so that any such behaviour towards seemingly unrelated individuals requires scrutiny. Queenless army ant colonies, which have anecdotally been reported to fuse with queenright foreign colonies, are such an enigmatic case. Here we combine experimental queen removal with population genetics and cuticular chemistry analyses to show that colonies of the African army ant Dorylus molestus frequently merge with neighbouring colonies after queen loss. Merging colonies often have no direct co-ancestry, but are on average probably distantly related because of overall population viscosity. The alternative of male production by orphaned workers appears to be so inefficient that residual inclusive fitness of orphaned workers might be maximized by indiscriminately merging with neighbouring colonies to increase their reproductive success. We show that worker chemical recognition profiles remain similar after queen loss, but rapidly change into a mixed colony Gestalt odour after fusion, consistent with indiscriminate acceptance of alien workers that are no longer aggressive. We hypothesize that colony fusion after queen loss might be more widespread, especially in spatially structured populations of social insects where worker reproduction is not profitable.     

Chemical Profiles of Two Pheromone Glands Are Differentially Regulated by Distinct Mating Factors in Honey Bee Queens (Apis mellifera L.)

Pheromones mediate social interactions among individuals in a wide variety of species, from yeast to mammals. In social insects such as honey bees, pheromone communication systems can be extraordinarily complex and serve to coordinate behaviors among many individuals. One of the primary mediators of social behavior and organization in honey bee colonies is queen pheromone, which is produced by multiple glands. The types and quantities of chemicals produced differ significantly between virgin and mated queens, and recent studies have suggested that, in newly mated queens, insemination volume or quantity can affect pheromone production. Here, we examine the long-term impact of different factors involved during queen insemination on the chemical composition of the mandibular and Dufour''s glands, two of the major sources of queen pheromone. Our results demonstrate that carbon dioxide (an anesthetic used in instrumental insemination), physical manipulation of genital tract (presumably mimicking the act of copulation), insemination substance (saline vs. semen), and insemination volume (1 vs. 8 µl) all have long-term effects on mandibular gland chemical profiles. In contrast, Dufour''s gland chemical profiles were changed only upon insemination and were not influenced by exposure to carbon dioxide, manipulation, insemination substance or volume. These results suggest that the chemical contents of these two glands are regulated by different neuro-physiological mechanisms. Furthermore, workers responded differently to the different mandibular gland extracts in a choice assay. Although these studies must be validated in naturally mated queens of varying mating quality, our results suggest that while the chemical composition of Dufour''s gland is associated with mating status, that of the mandibular glands is associated with both mating status and insemination success. Thus, the queen appears to be signaling both status and reproductive quality to the workers, which may impact worker behavior and physiology as well as social organization and productivity of the colony.     

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.     

Cuticular hydrocarbon dynamics in young adult Polistes dominulus (Hymenoptera: Vespidae) and the role of linear hydrocarbons in nestmate recognition systems

In social insects, cuticular hydrocarbons (CHCs) play an important role in nestmate discrimination processes, but young individuals are usually not discriminated. We studied CHC changes in young workers of the social wasp Polistes dominulus. A quantitative estimation demonstrated that total quantities of CHCs increased after emergence, with branched alkanes increasing drastically when compared with other classes of hydrocarbons. The relative quantity of longer-chain compounds increased with respect to shorter ones; unsaturated compounds decreased. These changes might reduce the capacity of the cuticle to acquire compounds of environmental origin. We then tested whether individuals acquire hydrocarbons from the environment, and whether this capability equally characterises newly emerged and mature wasps. We exposed wasps of two age classes (adults younger or older than 24 h) to four linear hydrocarbons in turn, and observed how nestmates reacted to their re-introduction into the natal colony. Exposed young wasps elicited significantly more aggressive responses than control sisters; but treated wasps older than 24 h were generally accepted by nestmates. Chemical assays showed that exposed young wasps readily absorbed hydrocarbons; older ones did not incorporate hydrocarbons, suggesting that the chemical profiles of mature wasps are less prone to chemical shifts than those of newly emerged wasps.