The costs of overwintering in paper wasps (Polistes dominula and Polistes gallicus): the use of energy stores.

Overwintering insects are facing energetic challenges because of food shortage, low temperature, and desiccation stress. Paper wasps of the genus Polistes overwinter as mated adults (gynes) in hibernacula protecting them from predation, snow, and rain but barely from low environmental temperature. In different climates, they face differing overwintering temperature regimes, and therefore they may differ in their energy use. We investigated how much of energy resources built up until autumn is used during diapause dormancy in natural hibernacula by measuring lipid, glycogen, and free carbohydrate content in autumn and early spring in Polistes dominula from temperate European (Austrian) and warm Mediterranean (Italian) climate and Polistes gallicus from Mediterranean climate. Winter energy consumption amounted to ~ 339 and ~ 310 J per wasp in the Austrian and Italian Polistes dominula populations. The smaller Italian Polistes gallicus consumed ~ 247 J. This amounts to 2.62, 2.35, and 1.79 J per day. Of this, the energy demand was mainly fuelled by lipids (84%, 93%, and 90%, respectively), but glycogen stores contributed also considerably (16%, 6%, and 9%). Free carbohydrates decreased only by 0.7%, 1%, and 0.8%. While fat stores seem still sufficient in spring, the wasps depleted most of their carbohydrates. The energy reserves of 396, 400, and 147 J per wasp remaining in spring in the three populations seem sufficient to fuel rest or simple brood care activities for a whole summer but restrict foraging flights to a few hours (~ 3.5-6 h). Results suggest that energy supply might become challenging in expected future climate scenarios.

Venom Collection by Electrical Stimulation in the Invasive Species Polistes dominula Reared Using a Vespiculture Regime.

Specific Venom Immunotherapy (VIT) is practiced with venom extracted from insects, and is the specific therapy used for patients highly allergic to social insect (Hymenoptera) stings. Due to the dramatic shortage of vespid species in the local environment, we coupled vespiculture techniques of Polistes paper wasps with a venom collection procedure based on the electrical stimulation of individuals from entire colonies. The procedure involves little to no disturbance of the individual insects, and at the same time, successfully allows for the extraction of venom containing all allergens necessary for VIT.

Chemically Insignificant Social Parasites Exhibit More Anti-Dehydration Behaviors than Their Hosts.

Social parasites have evolved adaptations to overcome host resistance as they infiltrate host colonies and establish there. Among the chemical adaptations, a few species are chemically "insignificant"; they are poor in recognition cues (cuticular hydrocarbons) and evade host detection. As cuticular hydrocarbons also serve a waterproofing function, chemical insignificance is beneficial as it protects parasites from being detected but is potentially harmful because it exposes parasites to desiccation stress. Here I tested whether the social parasites Polistes atrimandibularis employ behavioral water-saving strategies when they live at Polistes biglumis colonies. Observations in the field showed that parasites were less active than their cohabiting host foundresses, spent more time at the nest, and rested in the shadowy, back face of the nest, rather than at the front face, which contradicted expectations for the use of space for dominant females-typically, dominants rest at the nest front-face. These data suggest that behavioral adaptations might promote resistance to desiccation stress in chemical insignificant social parasites.

Multi-level social organization and nest-drifting behaviour in a eusocial insect.

Stable social groups usually consist of families. However, recent studies have revealed higher level social structure, with interactions between family groups across different levels of social organization in multiple species. The explanations for why this apparently paradoxical behaviour arises appear to be varied and remain untested. Here, we use automated radio-tagging data from over 1000 wasps from 93 nests and social network analyses of over 30 000 nest visitation records to describe and explain interactions across levels of social organization in the eusocial paper wasp Polistes canadensis. We detected three levels of social organization (nest, aggregation and community) which exchange 'drifter' individuals within and between levels. The highest level (community) may be influenced by the patchiness of high-quality nesting habitats in which these insects exist. Networks of drifter movements were explained by the distance between nests, the group size of donor nests and the worker-to-brood ratios on donor and recipient nests. These findings provide some explanation for the multi-level social interactions, which may otherwise seem paradoxical. Fitness benefits across multiple levels of social organization should be considered when trying to understand animal societies.

Close-range cues used by males of Polistes dominula in sex discrimination.

Sexual pheromones are chemical molecules responsible for mediating sex recognition and mating events. Long- and close-range sexual pheromones act differently. The first type is released to attract potential partners, whereas the second coordinates the interactions after potential mating partners encounter each other. Cuticular hydrocarbons (CHCs) have been suggested to be important cues in the mating systems of several Hymenoptera species, although empirical data are still lacking for many species. Here, we evaluated whether males of the model species Polistes dominula can differentiate the sex of individuals based on their CHC composition. In August 2019, several post-worker emergent nests (n = 19) were collected in the vicinity of Leuven (Belgium) and taken to the lab (KU Leuven), where newly emerged females and males were sampled, marked individually, and kept in plastic boxes for at least a week before being used in the mating trials. Focal males were paired with females and males from different nests and subjected to five different conditions: (I) alive, (II) dead, (III) CHCs washed, (IV) CHCs partially returned, and (V) CHCs from the opposite sex. We videotaped the interactions for 10 min and analysed the duration and different behavioural interactions of the focal male. Our results indicate that CHCs may be used by males as cues to recognise a potential mating partner in P. dominula, since the focal males displayed specific courtship behaviours exclusively toward females. Although we cannot exclude that visual cues could also be used in combination with the chemical ones, we empirically demonstrate that CHCs may be important to convey sexual information at close range in mating systems, allowing fast decisions toward potential sexual partners or rivals.

Polistes versicolor (Hymenoptera: Vespidae), an Introduced Wasp in the Galapagos Islands: Its Life Cycle and Ecological Impact.

The yellow paper wasp, Polistes versicolor (Olivier) was first recorded in the Galapagos archipelago in 1988. Its life cycle and ecological impacts were studied on two islands 11 yr after it was first discovered. This invasive wasp adapted quickly and was found in most environments. Colony counts and adult wasp monitoring showed a strong preference for drier habitats. Nest activities were seasonally synchronized, nest building followed the rains in the hot season (typically January-May), when insect prey increases, and peaked as temperature and rains started to decline. Next, the number of adult wasps peaked during the cool season when there is barely any rain in the drier zones. In Galapagos, almost half of the prey loads of P. versicolor were lepidopteran larvae, but wasps also carried spiders, beetles, and flies back to the colonies. An estimated average of 329 mg of fresh insect prey was consumed per day for an average colony of 120-150 wasp larvae. The wasps preyed upon native and introduced insects, but likely also affect insectivorous vertebrates as competitors for food. Wasps may also compete with native pollinators as they regularly visited flowers to collect nectar, and have been recorded visiting at least 93 plant species in Galapagos, including 66 endemic and native plants. Colonies were attacked by a predatory moth, Taygete sphecophila (Meyrick) (Lepidoptera: Autostichidae), but colony development was not arrested. High wasp numbers also affect the activities of residents and tourists. A management program for this invasive species in the archipelago is essential.

Phylogenomics indicates Amazonia as the major source of Neotropical swarm-founding social wasp diversity.

The Neotropical realm harbours unparalleled species richness and hence has challenged biologists to explain the cause of its high biotic diversity. Empirical studies to shed light on the processes underlying biological diversification in the Neotropics are focused mainly on vertebrates and plants, with little attention to the hyperdiverse insect fauna. Here, we use phylogenomic data from ultraconserved element (UCE) loci to reconstruct for the first time the evolutionary history of Neotropical swarm-founding social wasps (Hymenoptera, Vespidae, Epiponini). Using maximum likelihood, Bayesian, and species tree approaches we recovered a highly resolved phylogeny for epiponine wasps. Additionally, we estimated divergence dates, diversification rates, and the biogeographic history for these insects in order to test whether the group followed a 'museum' (speciation events occurred gradually over many millions of years) or 'cradle' (lineages evolved rapidly over a short time period) model of diversification. The origin of many genera and all sampled extant Epiponini species occurred during the Miocene and Plio-Pleistocene. Moreover, we detected no major shifts in the estimated diversification rate during the evolutionary history of Epiponini, suggesting a relatively gradual accumulation of lineages with low extinction rates. Several lines of evidence suggest that the Amazonian region played a major role in the evolution of Epiponini wasps. This spatio-temporal diversification pattern, most likely concurrent with climatic and landscape changes in the Neotropics during the Miocene and Pliocene, establishes the Amazonian region as the major source of Neotropical swarm-founding social wasp diversity.

The Venom Compound N-(3-methylbutyl)acetamide Attracts Several Polistes (Fuscopolistes) Species (Hymenoptera: Vespidae).

Polistes paper wasps in the Fuscopolistes subgenus (Hymenoptera: Vespidae) can be serious pests when they swarm at tall man-made structures. Chemical attractants may be useful to trap such paper wasps when they achieve pest status. Polistes venom has been shown to elicit a variety of behavioral responses in congeneric wasps, making it a source for potential chemical attractants. The compound N-(3-methylbutyl)acetamide is a principal volatile component in the venom of many female vespid wasps, including numerous Polistes species. We report the presence of N-(3-methylbutyl)acetamide in autumn gynes of Polistes metricus Say, Polistes bellicosus Cresson, and Polistes dorsalis (F.), as well as workers of Polistes aurifer (Saussure), P. bellicosus, P. metricus, and P. dorsalis. In field tests conducted in Florida, Georgia, South Carolina, and Washington, N-(3-methylbutyl)acetamide attracted male and female P. aurifer and P. metricus, as well as male P. dorsalis and P. bellicosus. Thus, N-(3-methylbutyl)acetamide may be a useful lure for trapping these paper wasps in pest situations.

Social wasps are effective biocontrol agents of key lepidopteran crop pests.

Biocontrol agents can help reduce pest populations as part of an integrated pest management scheme, with minimal environmental consequences. However, biocontrol agents are often non-native species and require significant infrastructure; overuse of single agents results in pest resistance. Native biocontrol agents are urgently required for more sustainable multi-faceted approaches to pest management. Social wasps are natural predators of lepidopteran pests, yet their viability as native biocontrol agents is largely unknown. Here, we provide evidence that the social paper wasp Polistes satan is a successful predator on the larvae of two economically important and resilient crop pests, the sugarcane borer Diatraea saccharalis (on sugarcane Saccharum spp.) and the fall armyworm Spodoptera frugiperda (on maize Zea mays); P. satan wasps significantly reduce crop pest damage. These results provide the much-needed baseline experimental evidence that social wasps have untapped potential as native biocontrol agents for sustainable crop production and food security.

Brain structure differences between solitary and social wasp species are independent of body size allometry.

Evolutionary transitions in social behavior are often associated with changes in species' brain architecture. A recent comparative analysis showed that the structure of brains of wasps in the family Vespidae differed between solitary and social species: the mushroom bodies, a major integrative brain region, were larger relative to brain size in the solitary species. However, the earlier study did not account for body size effects, and species' relative mushroom body size increases with body size in social Vespidae. Here we extend the previous analysis by measuring the effects of body size variation on brain structure differences between social and solitary vespid wasps. We asked whether total brain volume was greater relative to body size in the solitary species, and whether relative mushroom body size was greater in solitary species, after accounting for body size effects. Both total brain volume and relative mushroom body volume were significantly greater in the solitary species after accounting for body size differences. Therefore, body size allometry did not explain the solitary versus social species differences in brain structure. The evolutionary transition from solitary to social behavior in Vespidae was accompanied by decreases in total brain size and in relative mushroom body size.

Effect of temperature on the chemical profiles of nest materials of social wasps.

Social insects depend on their nests for protection against predation and abiotic threats. Accordingly, the chemical compounds present in the material wasps use to build their nests can both facilitate communication and repel predators. It is herein hypothesized that different wasp species build their nests with different structure and substrate materials and that such materials consist of chemical compounds related to unique wasp behavior and outside temperature variation. To test this hypothesis, nests were collected from three species of social wasps, the samples of which were subjected to temperature variation under laboratory conditions. The compounds present in the substrate were analyzed by gas chromatography coupled to mass spectrometry. Chemical compounds identified in the nest material of the three species responded differently to temperature variation. Chemical compounds from Polybia nests were altered significantly when subjected to temperature variation, whereas the nests of Polistes versicolor did not significantly change in relation to the control. The differences found between Polistes and Polybia nests may be related to genetic factors, but also to the type of nest they construct. It is possible that divergent evolutionary strategies for maintaining colony temperature, as a function of the chemical composition of the nests, may have appeared between wasps that have open and closed nests. In relatively small colonies, nest substrate is more resistant to temperature variation because it is composed of a greater diversity of elements and thus capable of holding heavier, longer carbon chains. Our results suggest that chemical compounds in the nest material of the three wasp species analysed responded differently to fluctuating ambient temperatures and that such variation could result from the biochemical differences of unique wasp species or from thermoregulation strategies of colonies.

Observation of intra- and interspecific differences in the nest chemical profiles of social wasps (Hymenoptera: Polistinae) using infrared photoacoustic spectroscopy.

The aim of this study was to explore whether the nest chemical profile (NCP) can be used to determine intra- and interspecific differences in social wasps of the subfamily Polistinae. For this purpose, Fourier transform infrared photoacoustic spectroscopy (FTIR-PAS) was used to directly analyze small pieces of nest as well as the gasters of females. An advantage of the methodology was that no sample preparation was required. FTIR-PAS combined with multivariate discriminant analyzes was used, to the best of our knowledge for the first time, to evaluate the NCPs of six species of polistine wasps, observing the influence of the nesting environment and investigating the relationships among the nest and female cuticular chemical profiles. The results revealed significant inter-species differences among the NCPs, as well as strong correlations with the environments in which the nests were located. The Mischocyttarus and Polistes species belong to the same tribe (Polistini) and therefore exhibited similar NCPs. These species were separated from the Polybia species in the NCP dendrogram, mainly because the Polybia belong to another tribe (Epiponini). Correlation was observed between the NCPs and the cuticular chemical profiles of females. The findings of the study demonstrated the importance of the NCP for differentiation of species and environments, and the utility of FTIR-PAS for identification of correlations between individuals and nests. The results confirmed the hypothesis that the NCP can be used as an additional tool for intra- and interspecific differentiation in social wasps of the subfamily Polistinae.

Heritable variation in colour patterns mediating individual recognition.

Understanding the developmental and evolutionary processes that generate and maintain variation in natural populations remains a major challenge for modern biology. Populations of Polistes fuscatus paper wasps have highly variable colour patterns that mediate individual recognition. Previous experimental and comparative studies have provided evidence that colour pattern diversity is the result of selection for individuals to advertise their identity. Distinctive identity-signalling phenotypes facilitate recognition, which reduces aggression between familiar individuals in P. fuscatus wasps. Selection for identity signals may increase phenotypic diversity via two distinct modes of selection that have different effects on genetic diversity. Directional selection for increased plasticity would greatly increase phenotypic diversity but decrease genetic diversity at associated loci. Alternatively, heritable identity signals under balancing selection would maintain genetic diversity at associated loci. Here, we assess whether there is heritable variation underlying colour pattern diversity used for facial recognition in a wild population of P. fuscatus wasps. We find that colour patterns are heritable and not Mendelian, suggesting that multiple loci are involved. Additionally, patterns of genetic correlations among traits indicated that many of the loci underlying colour pattern variation are unlinked and independently segregating. Our results support a model where the benefits of being recognizable maintain genetic variation at multiple unlinked loci that code for phenotypic diversity used for recognition.

Candidate genes for individual recognition in Polistes fuscatus paper wasps.

Few animals are known to individually recognize conspecifics, i.e. learn and recall unique individuals during subsequent encounters, and nearly all are social vertebrates. Remarkably, the social paper wasp Polistes fuscatus has recently been discovered to possess this ability, which is useful for remembering identities during competitive social interactions. We analyzed brain gene expression in staged encounters between pairs of individuals to explore potential mechanisms underlying wasps' ability to recall familiar individuals using real-time qRT-PCR. We identified four candidate genes (IP3K, IP3R, Nckx30C and Su(var)2-10) that were down-regulated in the presence of familiar individuals compared to single wasps and pairs of wasps meeting for the first time. These candidate genes are related to calcium signaling, therefore, we treated wasps with lithium chloride, a pharmacological agent that inhibits calcium signaling in neurons. This treatment decreased aggression in paper wasps, but did not affect expression of genes related to calcium signaling. The results suggest calcium signaling differences may be related to individual memory recall in wasps, and we present four promising candidate genes for future study. These data suggest genes associated with dominance behavior may be co-opted for individual recognition, but further work is needed to establish a causal association with the behavior.

Distributed cognition and social brains: reductions in mushroom body investment accompanied the origins of sociality in wasps (Hymenoptera: Vespidae).

The social brain hypothesis assumes the evolution of social behaviour changes animals' ecological environments, and predicts evolutionary shifts in social structure will be associated with changes in brain investment. Most social brain models to date assume social behaviour imposes additional cognitive challenges to animals, favouring the evolution of increased brain investment. Here, we present a modification of social brain models, which we term the distributed cognition hypothesis. Distributed cognition models assume group members can rely on social communication instead of individual cognition; these models predict reduced brain investment in social species. To test this hypothesis, we compared brain investment among 29 species of wasps (Vespidae family), including solitary species and social species with a wide range of social attributes (i.e. differences in colony size, mode of colony founding and degree of queen/worker caste differentiation). We compared species means of relative size of mushroom body (MB) calyces and the antennal to optic lobe ratio, as measures of brain investment in central processing and peripheral sensory processing, respectively. In support of distributed cognition predictions, and in contrast to patterns seen among vertebrates, MB investment decreased from solitary to social species. Among social species, differences in colony founding, colony size and caste differentiation were not associated with brain investment differences. Peripheral lobe investment did not covary with social structure. These patterns suggest the strongest changes in brain investment--a reduction in central processing brain regions--accompanied the evolutionary origins of eusociality in Vespidae.

Coevolution of visual signals and eye morphology in Polistes paper wasps.

To be effective, signals must propagate through the environment and be detected by receivers. As a result, signal form evolves in response to both the constraints imposed by the transmission environment and receiver perceptual abilities. Little work has examined the extent to which signals may act as selective forces on receiver sensory systems to improve the efficacy of communication. If receivers benefit from accurate signal assessment, selection could favour sensory organs that improve discrimination of established signals. Here, we provide evidence that visual resolution coevolves with visual signals in Polistes wasps. Multiple Polistes species have variable facial patterns that function as social signals, whereas other species lack visual signals. Analysis of 19 Polistes species shows that maximum eye facet size is positively associated with both eye size and presence of visual signals. Relatively larger facets within the eye's acute zone improve resolution of small images, such as wasp facial signals. Therefore, sensory systems may evolve to optimize signal assessment. Sensory adaptations to facilitate signal detection may represent an overlooked area of the evolution of animal communication.

Guia de identificação dos ninhos de vespas sociais (Hymenoptera, Vespidae, Polistinae) na Reserva Ducke, Manaus, Amazonas, Brasil / Identification guide for nests of social wasps (Hymenoptera: Vespidae: Polistinae) in Reserva Ducke, Manaus, Amazonas, Brazil

Vespidae sociais utilizam principalmente material vegetal para a elaboração de seus ninhos. Embora existam alguns estudos referentes à fauna de vespas na região Amazônica, nenhum trabalho trata exclusivamente dos ninhos. Além disso, nas coleções biológicas poucos são os ninhos tombados, devido principalmente à fragilidade e difícil conservação dos mesmos. O objetivo desse trabalho foi o conhecimento de alguns ninhos encontrados na Reserva Ducke, apresentando informações a respeito dos mesmos e uma chave de identificação dos gêneros. Os ninhos foram coletados através da busca direta, percorrendo os transectos da grade do Programa de Pesquisa em Biodiversidade; locais como margens de igarapés, bordas de acampamentos e construções na sede da reserva também foram explorados. Para todos os ninhos obteve-se o registro fotográfico e a localização exata por GPS. Foram registrados 39 ninhos de vespas sociais alocados em 17 espécies de Polistinae: Agelaia constructor, A. pallipes, Angiopolybia pallens, Apoica pallens, Metapolybia unilineata, Mischocyttarus lecointei, M. saturatus, Polybia bistriata, P. dimidiata, P. jurinei, P. liliacea, P. occidentalis, P. procellosa, P. rejecta, Protopolybia bituberculata, P. chartergoides e Synoeca virginea. Cinco ninhos desabitados de Mischocyttarus, Polybia e Polistes também foram coletados.

Nests of social wasps are composed mainly out of plant material. Although there are some studies about the social wasp fauna in the Amazon region, there is no work exclusively about these wasps' nests. Also, there are few catalogued nests in biological collections, because of their fragility and difficult conservation. The purpose of this study was to evaluate the kinds of nests found at "Reserva Ducke", compiling information about them and developing a key to identify the nests of each genera. The nests were actively collected in tracks of the "Programa de Pesquisa em Biodiversidade" plot; areas such as "igarapés" margins, base camp's surroundings and buildings at the reserve headquarters were also explored. All the nests were photographed and their precise location was obtained by GPS. Thirty-nine wasp's nests from 17 species of Polistinae were recorded: Agelaia constructor, A. pallipes, Angiopolybia pallens, Apoica pallens, Metapolybia unilineata, Mischocyttarus lecointei, M. saturatus, Polybia bistriata, P. dimidiata, P. jurinei, P. liliacea, P. occidentalis, P. procellosa, P. rejecta, Protopolybia bituberculata, P. chartergoides and Synoeca virginea. Five uninhabited nests of Mischocyttarus, Polybia and Polistes were collected.

Sociogenetic structure of Polistes (Aphanilopterus) versicolor Olivier, 1791 colonies (Hymenoptera, Vespidae, Polistini).

The observation of two distinct, well-defined oviposition areas in nests of the primitively eusocial wasp Polistes versicolor suggests the presence of multiple egg-layers and territorial behaviors. Electrophoretic analysis of enzyme loci in pupae from 35 colonies revealed an average observed heterozygosity of 0.10 and the existence of private polymorphisms, thereby indicating a low dispersion in this species. No evidence of diploid males was found. Phenotypic segregation analysis revealed the presence of more than one egg-laying female in 15 out of 35 colonies, as well as spatially preferential oviposition in 2 out of 13 nests, with distinct oviposition areas. Genetic relatedness estimates for brood were lower than expected for haplodiploid species under monogynous conditions (r = 0.75 for female broods and r = 0.5 for male) in 4 of those 13 nests, thereby inferring complex sociogenetic structuring in Polistes versicolor colonies.

Sociogenetic structure of Polistes (Aphanilopterus) versicolor Olivier, 1791 colonies (Hymenoptera, Vespidae, Polistini)

The observation of two distinct, well-defined oviposition areas in nests of the primitively eusocial wasp Polistes versicolor suggests the presence of multiple egg-layers and territorial behaviors. Electrophoretic analysis of enzyme loci in pupae from 35 colonies revealed an average observed heterozygosity of 0.10 and the existence of private polymorphisms, thereby indicating a low dispersion in this species. No evidence of diploid males was found. Phenotypic segregation analysis revealed the presence of more than one egg-laying female in 15 out of 35 colonies, as well as spatially preferential oviposition in 2 out of 13 nests, with distinct oviposition areas. Genetic relatedness estimates for brood were lower than expected for haplodiploid species under monogynous conditions (r = 0.75 for female broods and r = 0.5 for male) in 4 of those 13 nests, thereby inferring complex sociogenetic structuring in Polistes versicolor colonies.