Eusocial Wasp Research Articles

Brain physiology during photoperiod-related caste determination in the primitively eusocial wasp Polistes jokahamae

Adult females of the primitively eusocial wasp Polistes jokahamae can change caste in response to photoperiod length. Short-day photoperiod females store more lipids but have less developed ovaries for hibernation (becoming gynes), whereas long-day photoperiod females have fewer lipid stores but more developed ovaries under queenless conditions (becoming egg-laying workers). To explore the physiological mechanisms underlying photoperiod-related caste determination, analyses of gene expression levels in the brains of short- or long-day females were performed. Results suggest that short-day females may exhibit higher expression of genes involved in tryptophan metabolism, insulin signaling, and nutrition, including the digestion of sugars and lipids, and production of royal jelly proteins. Oral administration of tryptophan resulted in a positive correlation between tryptophan levels in the brain and lipid stores in the abdomen, suggesting that tryptophan promotes lipid storage in gynes. Long-day females showed enhanced expression of genes involved in tyramine/dopamine syntheses, epidermal growth factor receptor, insulin degradation, and oogenesis. In these females, tyramine administration increased the brain levels of tyramine and dopamine, and activated initial ovarian development under queenless conditions. Together, these results indicate that photoperiod-related caste determination in P. jokahamae may involve gene expression pathways similar to those involved in caste determination during the preimaginal stage in other Polistes species.

Morphology, biology and phylogeny of Xenos gadagkari sp.nov. (Strepsiptera: Xenidae): an endoparasite of Polistes wattii (Hymenoptera: Vespidae).

We report the morphology, biology and phylogeny of a new strepsipteran endoparasitic species: Xenos gadagkari, which stylopises the primitively eusocial wasp Polistes wattii from Punjab, India. We report a high abundance of the endoparasite in P. wattii population of our study area and provide the morphological description of adult males, male puparium and neotenic females. This species is sufficiently different from other species of Xenos reported from social wasps and therefore, constitutes a new species, X. gadagkari Sen and Nain, sp. nov. Although there are a few reports of strepsipteran parasitoids from India, this is the first confirmed report with a description of a Xenos species from the Indian population of P. wattii. Our findings contribute to the growing body of knowledge on Xenos and provide a foundation for future behavioural, microbial and molecular studies on this enigmatic group of insects.

The heat shock response in Polistes spp. brood from differing climates following heat stress

Temperature is a crucial factor in many physiological processes, especially in small ectotherms whose body temperature is highly influenced by ambient temperature. Polistes (paper wasps) is a genus of primitively eusocial wasps found in widely varying thermal environments throughout the world. Paper wasps construct open-faced combs in which the brood is exposed to varying ambient temperatures. The Heat Shock Response is a physiological mechanism that has been shown to help cope with thermal stress. We investigated the expression of heat shock proteins in different life stages of three species of Polistes from different climates with the aim of deducing adaptive patterns. This was done by assaying heat shock protein (hsp70, hsp83, hsc70) expression during control conditions (25 °C) or a heat insult (35 or 45 °C) in individuals collected from natural populations in Alpine, Temperate, or Mediterranean climates. Basal expression of hsc70 and hsp83 was found to be high, while hsp70 and hsp83 expression was found to be highly responsive to severe heat stress. As expression levels varied based on species, geographical origin, and life stage as well as between heat shock proteins, the Heat Shock Response of Polistes was found to be complex. The results suggest that adaptive utilization of the heat shock response contributes to the ability of Polistes spp. to inhabit widely different thermal environments.

Body Size of Female Strepsipteran Parasites (Strepsiptera, Xenidae, Xenos) Depends on Several Key Factors in a Vespine Wasp (Hymenoptera, Vespidae, Vespa).

Parasite growth in hosts depends on their hosts' nutritional status. This study examined whether the body size of the strepsipteran parasite Xenos oxyodontes, which parasitizes the eusocial wasp Vespa analis, is affected by several key factors, including host body size. We collected V. analis using bait traps for three years in Niigata, Japan, and evaluated the number of male and female X. oxyodontes parasites throughout the seasons. A total of 185 female parasites were collected, and their cephalothorax widths were measured. The widths of female parasites did not statistically vary among seasons and were positively correlated with the head widths of female host wasps but negatively correlated with the number of parasites per host wasp. In addition, we examined whether the reproductive conditions of post-hibernation solitary queens affected the cephalothorax width of female parasites. The widths of the female parasites were greater when the queens had less-developed ovaries. These results suggested that nutrient availability by female parasites depends on the host wasp and competition with conspecific individuals.

Chemical Resemblance of Egg Surface Compounds and Dufour's Gland in Two Neotropical Polistinae Wasps Polistes versicolor (Olivier) and Mischocyttarus metathoracicus (de Saussure, 1854).

Chemical communication plays a major role in regulating social dynamics in social insect colonies. The most studied class of chemical compounds are the cuticular hydrocarbons (CHCs), compounds with high molecular weight that cover the insect body. CHCs are used in nestmate recognition and to signal reproductive status. Brood, in the form of larvae and eggs, is known to participate in chemical communication and social dynamics by performing hunger behaviour and inducing interaction with adults and conferring nest and maternity identity. CHCs of adults and egg surface compounds are similar in composition in social insect species. The main source of egg compounds is proposed to be Dufour's gland, an accessory reproductive gland found in several Hymenoptera females. There is still a lack of information about the level of similarity among CHCs, compounds of egg surface and Dufour's gland for several wasp species, which could provide correlational evidence about the origins of egg-marking compounds. Thus, we investigated whether egg surface compounds were more similar to CHCs or Dufour's gland secretions in two Neotropical primitively eusocial wasp species, Polistes versicolor (Olivier) and Mischocyttarus metathoracicus (de Saussure, 1854). As expected, there was a higher chemical similarity between eggs and Dufour's gland secretions in both studied species, supporting the hypothesis that this gland is the source of chemical compounds found over the eggs in these two primitively eusocial species.

Mutualistic Relationships between Microorganisms and Eusocial Wasps (Hymenoptera, Vespidae)

Eusocial wasps are represented in the Vespidae by the subfamilies Stenogastrinae, Vespinae and Polistinae. These wasps present colonies that are sometimes composed of thousands of individuals which live in nests built with paper materials. The high density of the adult and larval population, as well as the stable micro environment of the nests, make very favourable conditions for the flourishing of various types of microorganisms. These microorganisms, which may be pathogens, are beneficial and certainly contribute to model the sociality of these insects. The mutualistic relationships that we observe in some species, especially in Actinomycete bacteria and yeasts, could have important fallouts for the development of new medicines and for the use of these insects in agricultural environments.

The Evolution of Eusociality: Insights From Comparing Two Indian Paper Wasp Species

Eusocial species live in colonies with a reproductive division of labour into fertile reproductive castes and sterile non-reproductive castes, an overlap of generations and cooperative brood care. A further distinction can be usefully made between primitively eusocial species which do not have morphological caste differentiation and highly eusocial species which do. Ropalidia marginata is a tropical primitively eusocial wasp that has been extensively studied, especially compared to other tropical social wasps. R. marginata has several distinct traits, such as a docile queen, well-developed age polyethism, and decentralized work regulation, which makes it different from other primitively eusocial wasps and reminiscent of highly eusocial species. since tropical wasps, especially those belonging to the genus Ropalidia have been poorly studied, we cannot be sure whether R. marginata is unique or its traits are more common among tropical Ropalidia species. to begin to overcome this problem, we have extended our research to the congeneric and sympatric Ropalidia cyathiformis. Here, we compare and contrast what we now know about these two species, especially concerning their reproductive and non-reproductive division of labour. We find that R. cyathiformis, unlike R. marginata, has a behaviourally dominant queen, weak and rigid age polyethism, likely uses behavioural dominance to regulate worker reproduction and individual workers self-regulate their own non-reproductive activities. We, therefore, conclude that R. marginata is indeed unique and argue that R. marginata is intermediate between primitively and highly eusocial wasps.

Conserved role of juvenile hormone in regulating behavioural maturation and division of labour in a highly eusocial wasp

Conserved role of juvenile hormone in regulating behavioural maturation and division of labour in a highly eusocial wasp

Both age and social environment shape the phenotype of ant workers

Position within the social group has consequences on individual lifespans in diverse taxa. This is especially obvious in eusocial insects, where workers differ in both the tasks they perform and their aging rates. However, in eusocial wasps, bees and ants, the performed task usually depends strongly on age. As such, untangling the effects of social role and age on worker physiology is a key step towards understanding the coevolution of sociality and aging. We performed an experimental protocol that allowed a separate analysis of these two factors using four groups of black garden ant (Lasius niger) workers: young foragers, old foragers, young nest workers, and old nest workers. We highlighted age-related differences in the proteome and metabolome of workers that were primarily related to worker subcaste and only secondarily to age. The relative abundance of proteins and metabolites suggests an improved xenobiotic detoxification, and a fuel metabolism based more on lipid use than carbohydrate use in young ants, regardless of their social role. Regardless of age, proteins related to the digestive function were more abundant in nest workers than in foragers. Old foragers were mostly characterized by weak abundances of molecules with an antibiotic activity or involved in chemical communication. Finally, our results suggest that even in tiny insects, extended lifespan may require to mitigate cancer risks. This is consistent with results found in eusocial rodents and thus opens up the discussion of shared mechanisms among distant taxa and the influence of sociality on life history traits such as longevity.

Surplus feeding reverses worker ovarian suppression and disrupts social cohesion in queen-right wasp colonies

Nutrition is an important component of oogenesis and ovarian development in insects. In social insect colonies where a large proportion of females are sterile, suppression of reproduction caused by differential acquisition and retention of nutrition has been hypothesized to cause worker sterility. This study, using the primitively eusocial wasp Ropalidia marginata (Lepeletier) (Hymenoptera: Vespidae), show that worker ovarian development in naturally foraging colonies is more similar to experimentally food-limited colonies than to surplus-fed colonies, indicating nutritional castration in workers whose ovaries are inhibited by food availability. Further, experimental provisioning of surplus nutrition led to higher ovarian development in workers as compared to naturally foraging and food-limited workers. Surplus feeding also led to higher nest desertion by workers, leading to a breakdown of the colony’s social structure, whereas food-limited colonies retained workers.

Next-Generation Sequencing of Four Mitochondrial Genomes of Dolichovespula (Hymenoptera: Vespidae) with a Phylogenetic Analysis and Divergence Time Estimation of Vespidae.

The wasp genus Dolichovespula (Hymenoptera: Vespidae: Vespinae) is a eusocial wasp group. Due to the taxonomic and phylogenetic issues with the family Vespidae, more genetic data should be gathered to provide efficient approaches for precise molecular identification. For this work, we used next-generation sequencing (also known as high-throughput sequencing) to sequence the mitochondrial genomes (mtgenomes) of four Dolichovespula species, viz. D. flora, D. lama, D. saxonica, and D. xanthicincta 16,064 bp, 16,011 bp, 15,682 bp, and 15,941 bp in length, respectively. The mitochondrial genes of the four species are rearranged. The A + T content of each mtgenome is more than 80%, with a control region (A + T-rich region), 13 protein-coding genes (PCGs), 22 tRNA genes, and two rRNA genes. There are 7 to 11 more genes on the majority strands than on the minority strands. Using Bayesian inference and Maximum-Likelihood methodologies as well as data from other species available on GenBank, phylogenetic trees and relationship assessments in the genus Dolichovespula and the family Vespidae were generated. The two fossil-based calibration dates were used to estimate the origin of eusociality and the divergence time of clades in the family Vespidae. The divergence times indicate that the latest common ancestor of the family Vespidae appeared around 106 million years ago (Ma). The subfamily Stenogastrinae diverged from other Vespidae at about 99 Ma, the subfamily Eumeninae at around 95 Ma, and the subfamily Polistinae and Vespinae diverged at approximately 42 Ma. The genus Dolichovespula is thought to have originated around 25 Ma. The origin and distribution pattern of the genus Dolichovespula are briefly discussed.

Gastral Drumming in Vespula germanica (Hymenoptera: Vespidae): Vibrational Communication at Night Suggests Additional Roles in Colony Organization.

Gastral drumming (GD) is a type of vibrational communication that has been reported in several species of yellowjackets and hornets. Despite early claims that it acts as a hunger signal, a more recent study found evidence that it acts as a nest-based food-recruitment signal, the first reported for eusocial wasps. Early studies also claimed, without supporting data, that it is produced most often in the early morning hours when the sun rises. Here, I recorded drumming continuously in colonies of Vespula germanica (Fabricius) to assess whether production was highest in the morning. Although I found no evidence in support of greater early morning production, I found, surprisingly, that it is produced at night, a time when foraging does not occur. When these results are combined with the results from previous studies on this species and similar findings in honey bees, they suggest that GD may be a modulatory signal, which acts by increasing general activity levels and by increasing the rate that individuals come into contact with social cues.

Queen succession in the Indian paper wasp Ropalidia marginata: On the trail of the potential queen

Ropalidia marginata is a common primitively eusocial wasp in peninsular India. Their colonies contain a single egg-laying queen and several non-egg-laying workers. Queens and workers are morphologically indistinguishable, and individuals can change from one role to the other. Unlike most primitively eusocial species, queens of R. marginata are docile, non-aggressive and non-interactive. Nevertheless, the queens maintain a complete reproductive monopoly mediated by non-volatile pheromones. Upon the death or removal of the queen, one worker becomes temporarily hyper-aggressive and becomes the next queen within about a week; we refer to her as the 'potential queen'. Because only one individual becomes hyper-aggressive and reveals herself as the potential queen, and the other wasps never challenge her, we have been much interested in identifying the potential queen in the presence of the queen. However, we have failed to do so until recently. Here, we recount the four decades of search for the potential queen, ending with the recent resolution that emerged from applying the novel technique of multilayer network analysis. Identifying the potential queen in the presence of the previous queen is now possible by integrating behavioural information from multiple social situations to form a holistic view of the social structure of the wasps.

Interspecific variation of antennal lobe composition among four hornet species

Olfaction is a crucial sensory modality underlying foraging, social and mating behaviors in many insects. Since the olfactory system is at the interface between the animal and its environment, it receives strong evolutionary pressures that promote neuronal adaptations and phenotypic variations across species. Hornets are large eusocial predatory wasps with a highly developed olfactory system, critical for foraging and intra-specific communication. In their natural range, hornet species display contrasting ecologies and olfactory-based behaviors, which might match to adaptive shifts in their olfactory system. The first olfactory processing center of the insect brain, the antennal lobe, is made of morphological and functional units called glomeruli. Using fluorescent staining, confocal microscopy and 3D reconstructions, we compared antennal lobe structure, glomerular numbers and volumes in four hornet species (Vespa crabro, Vespa velutina, Vespa mandarinia and Vespa orientalis) with marked differences in nesting site preferences and predatory behaviors. Despite a conserved organization of their antennal lobe compartments, glomeruli numbers varied strongly between species, including in a subsystem thought to process intraspecific cuticular signals. Moreover, specific adaptations involving enlarged glomeruli appeared in two species, V. crabro and V. mandarinia, but not in the others. We discuss the possible function of these adaptations based on species-specific behavioral differences.

Temporal Analysis of Effective Population Size and Mating System in a Social Wasp

Highly social species are successful because they cooperate in obligately integrated societies. We examined temporal genetic variation in the eusocial wasp Vespula maculifrons to gain a greater understanding of evolution in highly social taxa. First, we wished to test if effective population sizes of eusocial species were relatively low due to the reproductive division of labor that characterizes eusocial taxa. We thus estimated the effective population size of V. maculifrons by examining temporal changes in population allele frequencies. We sampled the genetic composition of a V. maculifrons population at 3 separate timepoints spanning a 13-year period. We found that effective population size ranged in the hundreds of individuals, which is similar to estimates in other, non-eusocial taxa. Second, we estimated levels of polyandry in V. maculifrons in different years to determine if queen mating system varied over time. We found no significant change in the number or skew of males mated to queens. In addition, mating skew was not significant within V. maculifrons colonies. Therefore, our data suggest that queen mate number may be subject to stabilizing selection in this taxon. Overall, our study provides novel insight into the selective processes operating in eusocial species by analyzing temporal genetic changes within populations.

Nutrition induced direct fitness for workers in a primitively eusocial wasp

Eusocial insects are characterised by a reproductive caste differentiation such that egg-laying is restricted to a small number of queens. The majority of the colony members function as non-reproducing workers and gain indirect fitness by rearing the offspring of the reproductives. In primitively eusocial species, some workers can also get direct fitness by sneaking in some eggs in the presence of the queens, replacing the queens and becoming new queens, or initiating new nests. Here we aimed to understand the factors that permit some workers to gain direct fitness and alter the number of workers doing so, using the primitively eusocial wasp Ropalidia marginata. We transplanted 12 naturally occurring colonies into large laboratory cages where there was adequate space for the workers to leave their natal nests and initiate new colonies. We compared six control colonies that we provided with ad libitum food placed near the nest to six test colonies in which we hand-fed the wasps in addition to the ad libitum food. Wasps in test colonies consumed more food, showed more aggression, replaced their queens, and initiated new nests significantly more often than those in control colonies. When considering all 12 colonies, the rates of queen replacement and nest foundation were significantly positively correlated with food consumption rates. The additional nutrition gained by hand-fed wasps appears to help workers in test colonies to develop their ovaries and lay eggs, implying that they are nutritionally castrated in control colonies.

Effects of juvenile hormone in fertility and fertility-signaling in workers of the common wasp Vespula vulgaris.

In the highly eusocial wasp, Vespula vulgaris, queens produce honest signals to alert their subordinate workers of their fertility status, and therefore they are reproductively suppressed and help in the colony. The honesty of the queen signals is likely maintained due to hormonal regulation, which affects fertility and fertility cue expression. Here, we tested if hormonal pleiotropy could support the hypothesis that juvenile hormone controls fertility and fertility signaling in workers. In addition, we aimed to check oocyte size as a proxy of fertility. To do that, we treated V. vulgaris workers with synthetic versions of juvenile hormone (JH) analogue and a JH inhibitor, methoprene and precocene, respectively. We dissected the treated females to check ovary activation and analyzed their chemical profile. Our results showed that juvenile hormone has an influence on the abundance of fertility linked compounds produced by workers, and it also showed to increase oocyte size in workers. Our results corroborate the hypothesis that juvenile hormone controls fertility and fertility signaling in workers, whereby workers are unable to reproduce without alerting other colony members of their fertility. This provides supports the hypothesis that hormonal pleiotropy contributes to keeping the queen fertility signals honest.

Viral load, not food availability or temperature, predicts colony longevity in an invasive eusocial wasp with plastic life history

Social insect colonies exhibit a variety of life history strategies, from the annual, semelparous colonies of temperate bees and wasps to the long-lived colonies of many ants and honeybees. Species introduced to novel habitats may exhibit plasticity in life history strategies as a result of the introduction, but the factors governing these changes often remain obscure. Vespula pensylvanica, a yellowjacket wasp, exhibits such plasticity in colony longevity. Multi-year (perennial) colonies are relatively common in introduced populations in Hawaii, while source populations in the western United States are typically on an annual cycle. Here, we use experiments and observational data to examine how diet, disease, nest thermal environment, and nest location influence colony longevity in a population with both annual and perennial colonies. Counter to our predictions, experimental feeding and warming did not increase colony survival in the winter in the introduced range. However, Moku Virus load and wasp colony density predicted colony survival in one year, suggesting a potential role for disease in modulating colony phenology. We also found that local V. pensylvanica colony density was positively correlated with Moku Virus loads, and that Arsenophonus sp. bacterial loads in V. pensylvanica colonies were positively associated with proximity to feral honeybee (Apis mellifera) hives, suggesting potential transmission routes for these poorly understood symbionts. The factors influencing colony longevity in this population are likely multiple and interactive. More important than food availability, we propose winter precipitation as a critical factor that may explain temporal and spatial variation in colony longevity in these invasive wasps.

Hormonal modulation of reproduction and fertility signaling in polistine wasps

In social insects, it has been suggested that reproduction and the production of particular fertility-linked cuticular hydrocarbons (CHC) may be under shared juvenile hormone (JH) control, and this could have been key in predisposing such cues to later evolve into full-fledged queen pheromone signals. However, to date, only few studies have experimentally tested this “hormonal pleiotropy” hypothesis. Here, we formally test this hypothesis using data from four species of Polistine wasps, Polistes dominula, Polistes satan, Mischocyttarus metathoracicus, and Mischocyttarus cassununga, and experimental treatments with JH using the JH analogue methoprene and the anti-JH precocene. In line with reproduction being under JH control, our results show that across these four species, precocene significantly decreased ovary development when compared with both the acetone solvent-only control and the methoprene treatment. Consistent with the hormonal pleiotropy hypothesis, these effects on reproduction were further matched by subtle shifts in the CHC profiles, with univariate analyses showing that in P. dominula and P. satan the abundance of particular linear alkanes and mono-methylated alkanes were affected by ovary development and our hormonal treatments. The results indicate that in primitively eusocial wasps, and particularly in Polistes, reproduction and the production of some CHC cues are under joint JH control. We suggest that pleiotropic links between reproduction and the production of such hydrocarbon cues have been key enablers for the origin of true fertility and queen signals in more derived, advanced eusocial insects.

Streptomyces sp. M54: an actinobacteria associated with a neotropical social wasp with high potential for antibiotic production.

Streptomyces symbionts in insects have shown to be a valuable source of new antibiotics. Here, we report the genome sequence and the potential for antibiotic production of "Streptomyces sp. M54", an Actinobacteria associated with the eusocial wasp, Polybia plebeja. The Streptomyces sp. M54 genome is composed of a chromosome (7.96Mb), and a plasmid (1.91Kb) and harbors 30 biosynthetic gene clusters for secondary metabolites, of which only one third has been previously characterized. Growth inhibition bioassays show that this bacterium produces antimicrobial compounds that are active against Hirsutella citriformis, a natural fungal enemy of its host, and the human pathogens Staphylococcus aureus and Candida albicans. Analyses through TLC-bioautography, LC-MS/MS and NMR allowed the identification of five macrocyclic ionophore antibiotics, with previously reported antibacterial, antitumor and antiviral properties. Phylogenetic analyses placed Streptomyces sp. M54 in a clade of other host-associated strains taxonomically related to Streptomyces griseus. Pangenomic and ANI analyses confirm the identity of one of its closest relatives as Streptomyces sp. LaPpAH-199, a strain isolated from an ant-plant symbiosis in Africa. In summary, our results suggest an insect-microbe association in distant geographic areas and showcase the potential of Streptomyces sp. M54 and related strains for the discovery of novel antibiotics.