Annette Van Oystaeyen

Conserved class of queen pheromones stops social insect workers from reproducing

Long Live the Queen Eusociality is often considered to have arisen, at least in part, due to the inclusive fitness that workers gain through helping their queen sister to raise her offspring. Van Oystaeyen et al. (p. 287; see the Perspective by Chapuisat) characterized the sterility-inducing queen pheromone across three distantly related eusocial hymenopterans (a wasp, a bumblebee, and a desert ant) and synthesized data across 69 other species. Queen pheromones appear to be remarkably conserved, which suggests that reproductive manipulation has ancient roots. Social insect queens use an ancient, evolutionarily conserved class of pheromones to prevent worker reproduction. [Also see Perspective by Chapuisat] A major evolutionary transition to eusociality with reproductive division of labor between queens and workers has arisen independently at least 10 times in the ants, bees, and wasps. Pheromones produced by queens are thought to play a key role in regulating this complex social system, but their evolutionary history remains unknown. Here, we identify the first sterility-inducing queen pheromones in a wasp, bumblebee, and desert ant and synthesize existing data on compounds that characterize female fecundity in 64 species of social insects. Our results show that queen pheromones are strikingly conserved across at least three independent origins of eusociality, with wasps, ants, and some bees all appearing to use nonvolatile, saturated hydrocarbons to advertise fecundity and/or suppress worker reproduction. These results suggest that queen pheromones evolved from conserved signals of solitary ancestors.

The origin and evolution of social insect queen pheromones: Novel hypotheses and outstanding problems

Queen pheromones, which signal the presence of a fertile queen and induce daughter workers to remain sterile, are considered to play a key role in regulating the reproductive division of labor of insect societies. Although queen pheromones were long thought to be highly taxon-specific, recent studies have shown that structurally related long-chain hydrocarbons act as conserved queen signals across several independently evolved lineages of social insects. These results imply that social insect queen pheromones are very ancient and likely derived from an ancestral signalling system that was already present in their common solitary ancestors. Based on these new insights, we here review the literature and speculate on what signal precursors social insect queen pheromones may have evolved from. Furthermore, we provide compelling evidence that these pheromones should best be seen as honest signals of fertility as opposed to suppressive agents that chemically sterilize the workers against their own best interests.

Unusual modes of reproduction in social insects: shedding light on the evolutionary paradox of sex.

The study of alternative genetic systems and mixed modes of reproduction, whereby sexual and asexual reproduction is combined within the same lifecycle, is of fundamental importance as they may shed light on classical evolutionary issues, such as the paradox of sex. Recently, several such cases were discovered in social insects. A closer examination of these systems has revealed many amazing facts, including the mixed use of asexual and sexual reproduction for the production of new queens and workers, males that can clone themselves and the routine use of incest without deleterious genetic consequences. In addition, in several species, remarkable cases of asexually reproducing socially parasitic worker lineages have been discovered. The study of these unusual systems promises to provide insight into many basic evolutionary questions, including the maintenance of sex, the expression of sexual conflict and kin conflict and the evolution of cheating in asexual lineages.

Sneaky queens in Melipona bees selectively detect and infiltrate queenless colonies

Insect societies are characterized by advanced cooperation, but at the same time the complexity of their colonies renders them susceptible to reproductive parasitism. Recently, a genetic study on the Brazilian stingless bee Melipona scutellaris showed that unrelated queens frequently invade and take over colonies in which the mother queen had died. In the present study, we investigated this phenomenon using radio frequency identification (RFID) tags. We confirmed that alien queen take-overs are common within this species, and demonstrated that mated queens actively seek out colonies without a queen to reproduce in. Furthermore, we found that queens only penetrate their target colonies in the evening, when guarding efficiency is significantly reduced. We hypothesize that this strategy reduces the chance of the queens being attacked by entrance guards, thus maximizing their chance of successful infiltration.

No evidence of enemy release in pathogen and microbial communities of common wasps (Vespula vulgaris) in their native and introduced range.

When invasive species move to new environments they typically experience population bottlenecks that limit the probability that pathogens and parasites are also moved. The invasive species may thus be released from biotic interactions that can be a major source of density-dependent mortality, referred to as enemy release. We examined for evidence of enemy release in populations of the common wasp (Vespula vulgaris), which attains high densities and represents a major threat to biodiversity in its invaded range. Mass spectrometry proteomic methods were used to compare the microbial communities in wasp populations in the native (Belgium and England) and invaded range (Argentina and New Zealand). We found no evidence of enemy release, as the number of microbial taxa was similar in both the introduced and native range. However, some evidence of distinctiveness in the microbial communities was observed between countries. The pathogens observed were similar to a variety of taxa observed in honey bees. These taxa included Nosema, Paenibacillus, and Yersina spp. Genomic methods confirmed a diversity of Nosema spp., Actinobacteria, and the Deformed wing and Kashmir bee viruses. We also analysed published records of bacteria, viruses, nematodes and fungi from both V. vulgaris and the related invader V. germanica. Thirty-three different microorganism taxa have been associated with wasps including Kashmir bee virus and entomophagous fungi such as Aspergillus flavus. There was no evidence that the presence or absence of these microorganisms was dependent on region of wasp samples (i.e. their native or invaded range). Given the similarity of the wasp pathogen fauna to that from honey bees, the lack of enemy release in wasp populations is probably related to spill-over or spill-back from bees and other social insects. Social insects appear to form a reservoir of generalist parasites and pathogens, which makes the management of wasp and bee disease difficult.

Effect of oral administration of lactic acid bacteria on colony performance and gut microbiota in indoor-reared bumblebees (Bombus terrestris)

In this study, we investigated if oral administration of lactic acid bacteria could increase the colony performance of reared bumblebees. We found that a continuous administration of Lactobacillus kunkeei LMG 18925 and Lactobacillus crispatus LMG 9479 could partly compensate the effects of low nutritional pollen, but a permanent colonization in the gut was not detected with Illumina MiSeq 16S rRNA sequencing. Contrary to expectations, a single administration of L. kunkeei LMG 18925 to a high nutritional pollen led to a lower total drone mass. A Bombus-specific strain, Bifidobacterium actinocoloniiforme R-53049, showed potential to colonize the gut permanently after three administrations. Our study represents a first screening for the potential use of probiotic strains in bumblebees. We conclude that both diet and host specificity of bacteria might have an effect on colony performance of indoor-reared bumblebees and play a role in the gut colonization success.

Conserved queen pheromones in bumblebees: a reply to Amsalem et al.

In a recent study, Amsalem, Orlova & Grozinger (2015) performed experiments with Bombus impatiens bumblebees to test the hypothesis that saturated cuticular hydrocarbons are evolutionarily conserved signals used to regulate reproductive division of labor in many Hymenopteran social insects. They concluded that the cuticular hydrocarbon pentacosane (C25), previously identified as a queen pheromone in a congeneric bumblebee, does not affect worker reproduction in B. impatiens. Here we discuss some shortcomings of Amsalem et al.’s study that make its conclusions unreliable. In particular, several confounding effects may have affected the results of both experimental manipulations in the study. Additionally, the study’s low sample sizes (mean n per treatment = 13.6, range: 4–23) give it low power, not 96–99% power as claimed, such that its conclusions may be false negatives. Inappropriate statistical tests were also used, and our reanalysis found that C25 substantially reduced and delayed worker egg laying in B. impatiens. We review the evidence that cuticular hydrocarbons act as queen pheromones, and offer some recommendations for future queen pheromone experiments.

Chemical Strategies of the Beetle Metoecus Paradoxus, Social Parasite of the Wasp Vespula Vulgaris.

The parasitoid beetle Metoecus paradoxus frequently parasitizes colonies of the common wasp, Vespula vulgaris. It penetrates a host colony as a larva that attaches itself onto a foraging wasp’s body and, once inside the nest, it feeds on a wasp larva inside a brood cell and then pupates. Avoiding detection by the wasp host is crucial when the beetle emerges. Here, we tested whether adult M. paradoxus beetles avoid detection by mimicking the cuticular hydrocarbon profile of their host. The beetles appear to be chemically adapted to their main host species, the common wasp, because they share more hydrocarbon compounds with it than they do with the related German wasp, V. germanica. In addition, aggression tests showed that adult beetles were attacked less by common wasp workers than by German wasp workers. Our results further indicated that the host-specific compounds were, at least partially, produced through recycling of the prey’s hydrocarbons, and were not acquired through contact with the adult host. Moreover, the chemical profile of the beetles shows overproduction of the wasp queen pheromone, nonacosane (n-C29), suggesting that beetles might mimic the queen’s pheromonal bouquet.

Surviving in the absence of flowers: do nectar yeasts rely on overwintering bumblebee queens to complete their annual life cycle?

Floral nectar represents an ephemeral habitat that is restricted in time and space to zoophilous flowering vegetation. To survive in these habitats, nectar-inhabiting microorganisms rely on animal vectors to disperse from one flower to the next. However, it remains unclear how nectar yeasts persist when flowers and nectar cease to be present. Here, we tested the hypothesis that hibernating bumblebee queens function as a reservoir for nectar yeasts in the absence of plants or pollinators during winter. Our results show that the nectar yeast, Metschnikowia reukaufii, was present in the gastrointestinal tract of wild bumblebee queens that emerged from hibernation and that it could persist inside the gut of hibernating queens under experimental conditions. However, no evidence for such persistence was found in the case of the second most frequent nectar yeast, M. gruessii. Furthermore, a phylloplane yeast that occasionally inhabits nectar, Rhodotorula mucilaginosa, was able to colonize the gut under experimental conditions. Two bumblebee-associated yeasts, Candida bombi and C. bombiphila, were successfully passed down generations after administration in commercial lab-reared bumblebees. Overall, these results demonstrate that bumblebees could act as a reservoir for nectar yeasts during winter when floral nectar is absent.