Eusocial Wasp Polistes Research Articles

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.

Causas de mortalidad de colonias de Polistes dominula (Christ, 1791) (Hymenoptera, Vespidae) en zonas urbanas del suroeste de la Península Ibérica

De 2017 a 2018 se estudiaron diversas poblaciones de la avispa eusocial Polistes dominula (Christ, 1791) en tres municipios del suroeste de la península ibérica, con la finalidad de identificar las causas de mortalidad de sus colonias. Los resultados mostraron que la causa principal de mortalidad en las zonas de estudio fue la actividad antrópica (43,55 %). La segunda causa más relevante fue el abandono del nido (20,19 %). Únicamente 82 de 411 nidos (19,95 %) demostraron un declive natural de la colonia, tras la aparición de reproductores.

Sight in a Clique, Scent in Society: Plasticity in the Use of Nestmate Recognition Cues Along Colony Development in the Social Wasp Polistes dominula

Nestmate recognition, i.e., the ability to discriminate nestmates from foreign individuals, is a crucial feature of insect societies, and it has been traditionally considered to be predominantly based on chemical cues. Recent empirical evidence, however, suggests a relevant plasticity in the use of different communication channels according to cue availability and reliability in different contexts. In particular, visual cues have been shown to influence various types of social recognition in several social insects, but their role in nestmate recognition is still under-investigated. We tested the hypothesis of plasticity in the use of visual and chemical recognition cues in the primitively eusocial wasp Polistes dominula, in which the availability and reliability of recognition cues vary across the colony cycle. Indeed, before the emergence of workers, P. dominula colonies are rather small (one to few individuals), and the variability in the facial pattern might allow resident wasps to use visual cues for nestmate recognition. After workers' emergence, the increase in the number of colony members reduces the reliability of visual cues, thus leaving chemical cues as the most reliable nestmate recognition cues. We thus predict a differential use of chemical and visual cues along colony life. We experimentally separated visual and chemical cues of nestmates and non-nestmates and presented them alone or in combination (with coherent or mismatched cues) to resident wasps to test which communication channel was used in the two stages and, in case, how visual and chemical cues interacted. Our results show, for the first time in a social insect, the differential use of visual and chemical cues for nestmate recognition in two different phases of colony, which supports the hypothesis of a plastic, reliability-based use of recognition cues in this species according to the different colonial contexts.

Orphaning does not affect the colony productivity of the primitive eusocial wasp Polistes snelleni

In colonies of primitively eusocial wasps, some dominant workers become successive queens and inherit queenship after the death of the foundress queens. Although workers in many species do not mate, workers of Polistes snelleni are capable of mating and female production. In this study, we removed foundress queens from colonies of P. snelleni to evaluate the effects of queen loss on the dominant–subordinate relationships among the remaining workers and the productivity of colonies in the species. The foundress queens were the sole egg layers in almost all of the queenright colonies. The frequency of dominance behaviour among the wasps in the queenright colonies was significantly less than in the orphan colonies. The frequency of dominance behaviour in the successive queens after queen removal was significantly more than in the foundress queens. Multiple workers had developed ovaries, including the successive queens in 66.7 % (10/15) of the orphan colonies after queen removal. The orphan colonies produced significantly more cells and eggs than the queenright colonies. Our results suggest that the reproductive potential of the successive queens in the orphan colonies is not lower than that of the foundress queens, and that the productivity of the orphan colonies is maintained rather than causing potential conflict over direct reproduction among workers.

Shared genes related to aggression, rather than chemical communication, are associated with reproductive dominance in paper wasps (Polistes metricus)

BackgroundIn social groups, dominant individuals may socially inhibit reproduction of subordinates using aggressive interactions or, in the case of highly eusocial insects, pheromonal communication. It has been hypothesized these two modes of reproductive inhibition utilize conserved pathways. Here, we use a comparative framework to investigate the chemical and genomic underpinnings of reproductive dominance in the primitively eusocial wasp Polistes metricus. Our goals were to first characterize transcriptomic and chemical correlates of reproductive dominance and second, to test whether dominance-associated mechanisms in paper wasps overlapped with aggression or pheromone-related gene expression patterns in other species. To explore whether conserved molecular pathways relate to dominance, we compared wasp transcriptomic data to previous studies of gene expression associated with pheromonal communication and queen-worker differences in honey bees, and aggressive behavior in bees, Drosophila, and mice.ResultsBy examining dominant and subordinate females from queen and worker castes in early and late season colonies, we found that cuticular hydrocarbon profiles and genome-wide patterns of brain gene expression were primarily associated with season/social environment rather than dominance status. In contrast, gene expression patterns in the ovaries were associated primarily with caste and ovary activation. Comparative analyses suggest genes identified as differentially expressed in wasp brains are not related to queen pheromonal communication or caste in bees, but were significantly more likely to be associated with aggression in other insects (bees, flies), and even a mammal (mice).ConclusionsThis study provides the first comprehensive chemical and molecular analysis of reproductive dominance in paper wasps. We found little evidence for a chemical basis for reproductive dominance in P. metricus, and our transcriptomic analyses suggest that different pathways regulate dominance in paper wasps and pheromone response in bees. Furthermore, there was a substantial impact of season/social environment on gene expression patterns, indicating the important role of external cues in shaping the molecular processes regulating behavior. Interestingly, genes associated with dominance in wasps were also associated with aggressive behavior in bees, solitary insects and mammals. Thus, genes involved in social regulation of reproduction in Polistes may have conserved functions associated with aggression in insects and other taxa.

Males do not like the working class: male sexual preference and recognition of functional castes in a primitively eusocial wasp

Discrimination among potential partners is a critical step in sexual selection to avoid wasting reproductive resources on an unsuitable mate. In the female-dominated hymenopteran societies males have often been regarded as ‘flying sperm containers’ spending all their time and energy in trying to acquire a mate. We investigated the male sexual preference for potential partners using as a model the primitively eusocial wasp Polistes dominula in which female caste is rather flexible and difficult to determine. By means of laboratory bioassays, we compared the males' behaviour towards females of different reproductive potential. Males were able to recognize female castes, strongly preferring reproductive females to workers, regardless of female age or health. The results show that in this species caste plays a key role in orienting male discrimination and preference, presumably through chemical cues, towards reproductive females both healthy and parasite-castrated. Overall, our study shows that social Hymenoptera males are not always ‘small mating machines’ eager to mate.

The effect of juvenile hormone on Polistes wasp fertility varies with cooperative behavior

Social insects provide good models for studying how and why the mechanisms that underlie reproduction vary, as there is dramatic reproductive plasticity within and between species. Here, we test how the effect of juvenile hormone (JH) on fertility covaries with cooperative behavior in workers and nest-founding queens in the primitively eusocial wasp Polistes metricus. P. metricus foundresses and workers appear morphologically similar and both are capable of reproduction, though there is variation in the extent of social cooperation and the probability of reproduction across castes. Do the endocrine mechanisms that mediate reproduction co-vary with cooperative behavior? We found dramatic differences in the effect of JH on fertility across castes. In non-cooperative nest-founding queens, all individuals responded to JH by increasing their fertility. However, in cooperative workers, the effect of JH on fertility varies with body weight; large workers increase their fertility in response to JH while small workers do not. The variation in JH response may be an adaptation to facilitate resource allocation based on the probability of independent reproduction. This work contrasts with previous studies in closely related Polistes dominulus paper wasps, in which both foundresses and workers form cooperative associations and both castes show similar, condition-dependent JH response. The variation in JH responsiveness within and between species suggests that endocrine responsiveness and the factors influencing caste differentiation are surprisingly evolutionarily labile.

Development of an RNA interference tool, characterization of its target, and an ecological test of caste differentiation in the eusocial wasp polistes.

Recent advancements in genomics provide new tools for evolutionary ecological research. The paper wasp genus Polistes is a model for social insect evolution and behavioral ecology. We developed RNA interference (RNAi)-mediated gene silencing to explore proposed connections between expression of hexameric storage proteins and worker vs. gyne (potential future foundress) castes in naturally-founded colonies of P. metricus. We extended four fragments of putative hexamerin-encoding P. metricus transcripts acquired from a previous study and fully sequenced a gene that encodes Hexamerin 2, one of two proposed hexameric storage proteins of P. metricus. MALDI-TOF/TOF, LC-MSMS, deglycosylation, and detection of phosphorylation assays showed that the two putative hexamerins diverge in peptide sequence and biochemistry. We targeted the hexamerin 2 gene in 5th (last)-instar larvae by feeding RNAi-inducing double-stranded hexamerin 2 RNA directly to larvae in naturally-founded colonies in the field. Larval development and adult traits were not significantly altered in hexamerin 2 knockdowns, but there were suggestive trends toward increased developmental time and less developed ovaries, which are gyne characteristics. By demonstrating how data acquisition from 454/Roche pyrosequencing can be combined with biochemical and proteomics assays and how RNAi can be deployed successfully in field experiments on Polistes, our results pave the way for functional genomic research that can contribute significantly to learning the interactions of environment, development, and the roles they play in paper wasp evolution and behavioral ecology.

Colony kin structure and breeding patterns in the social wasp, Polistes biglumis

We used DNA microsatellites to study colony kin structure and breeding patterns in the primitively eusocial wasp Polistes biglumis. P. biglumis inhabits cool areas at high altitudes and, as a consequence, has a reduced colony cycle compared to more temperate Polistes. P. biglumis colonies are always founded and controlled by a single foundress, but nest failure is common and foundresses losing their nests do not have time to start new ones due to the short season. Instead, nests are characterized by frequent female turnover, in the form of females taking over (usurpation) other con-specific nests. Our results showed that most nests had offspring from multiple unrelated females, including some where multiple females were not observed in monitoring. Reconstruction of behavioural events from the genetic data revealed three types of multiple matriline nests: (a) nests that were usurped by another female, where the original nest owner disappeared following the usurpation event, (b) nests that were joined by another female, where the original nest owner stayed following the joining event, (c) nests that were both usurped and joined by other females. We also found, for the first time, a clear indication of multiple mating by Polistes females. Moreover, males mating with the same female were related, which may be explained by the lek mating system of P. biglumis. Finally, we analysed the nest sex ratios and how it changed during the season and found that sexes were produced sequentially, males before females.

Dominance hierarchy among workers changes with colony development in Polistes japonicus (Hymenoptera, Vespidae) paper wasp colonies with a small number of workers

Dominance hierarchy in the primitively eusocial wasp Polistes japonicus was analysed in four colonies for two periods: (1) the first-brood period, when only early emerging workers are present on the nest, and (2) the mixed-brood period, when the first and second (last) broods are present on the nest. The rank in the dominance hierarchy was determined based on a sociogram showing a dominance–subordinance relationship for all pairs of workers. During the first-brood period, older workers were likely to be more dominant (older dominance hierarchy), while the rank of workers was reversed during the mixed-brood period, with younger workers being likely to be more dominant (younger dominance hierarchy). However, the oldest and youngest workers were not always the top-ranked workers in the dominance hierarchy during the first- and mixed-brood periods, respectively, and during the mixed-brood period no younger dominance hierarchy was evident when the first or second brood was analysed separately. Higher ranked workers displayed dominance behaviour more frequently, and the lowest ranked worker hardly displayed dominance behaviour. Most workers displayed dominance behaviours primarily towards the worker ranked immediately below in the dominance hierarchy during the mixed-brood period but not during the first-brood period. The bodies of younger workers were larger for the mixed brood, but not for the first brood in some colonies or the second brood in all colonies. The association between body size and rank in the dominance hierarchy was negative during the first-brood period and positive during the mixed-brood period, with a nearly significant trend also seen even when the analysis was limited to the second brood. To explain the above temporal change from an older dominance hierarchy to a younger dominance hierarchy, we propose the hypothesis that the probability of a worker inheriting the colony increases rapidly with colony development, and consequently younger larger workers attempt to move up the dominance hierarchy in order to produce their own offspring by becoming the superseder late in colony development, rather than working harmoniously so as to boost the overall production of reproductive progeny for a colony, which is the strategy adopted early in colony development.

Brain transcriptomic analysis in paper wasps identifies genes associated with behaviour across social insect lineages

Comparative sociogenomics has the potential to provide important insights into how social behaviour evolved. We examined brain gene expression profiles of the primitively eusocial wasp Polistes metricus and compared the results with a growing base of brain gene expression information for the advanced eusocial honeybee, Apis mellifera. We studied four female wasp groups that show variation in foraging/provisioning behaviour and reproductive status, using our newly developed microarray representing approximately 3248 P. metricus genes based on sequences generated from high-throughput pyrosequencing. We found differences in the expression of approximately 389 genes across the four groups. Pathways known from Drosophila melanogaster to be related to lipid metabolism, heat and stress response, and various forms of solitary behaviour were associated with behavioural differences among wasps. Forty-five per cent of differentially expressed transcripts showed significant associations with foraging/provisioning status, and 14 per cent with reproductive status. By comparing these two gene lists with lists of genes previously shown to be differentially expressed in association with honeybee division of labour, we found a significant overlap of genes associated with foraging/provisioning, but not reproduction, across the two species. These results suggest common molecular roots for foraging division of labour in two independently evolved social insect species and the possibility of more lineage-specific roots of reproductive behaviour. We explore the implications of these findings for the idea that there is a conserved 'genetic toolkit' for division of labour across multiple lineages.

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.

The effect of juvenile hormone on temporal polyethism in the paper wasp Polistes dominulus

Juvenile hormone (JH) has an important role in the behavior of eusocial Hymenoptera. Previous work has shown that JH influences aggression and dominance behavior in primitive eusocial insects that lack discrete queen and worker castes (e.g. Bombus bees and Polistes wasps). In contrast, JH is one of the factors that mediates temporal polyethism among workers in advanced eusocial insects that have reproductive castes (e.g. Apis bees and Polybiawasps). Therefore, initial observations suggest that JH may have different roles in primitive and advanced eusocial taxa. Here, we use detailed behavioral observations of marked individuals to test whether JH influences temporal polyethism in the primitive eusocial wasp Polistes dominulus. First, we show that workers in P. dominulus have an age-related division of labor, as workers switch from nest work to foraging as they mature. Then, we show that application of JH accelerates the onset of foraging behavior.Workers treated with JH start foraging at a younger age than control workers. Therefore, JH mediates temporal polyethism in the primitively eusocial insect Polistes dominulus.

Wasp Gene Expression Supports an Evolutionary Link Between Maternal Behavior and Eusociality

The presence of workers that forgo reproduction and care for their siblings is a defining feature of eusociality and a major challenge for evolutionary theory. It has been proposed that worker behavior evolved from maternal care behavior. We explored this idea by studying gene expression in the primitively eusocial wasp Polistes metricus. Because little genomic information existed for this species, we used 454 sequencing to generate 391,157 brain complementary DNA reads, resulting in robust hits to 3017 genes from the honey bee genome, from which we identified and assayed orthologs of 32 honey bee behaviorally related genes. Wasp brain gene expression in workers was more similar to that in foundresses, which show maternal care, than to that in queens and gynes, which do not. Insulin-related genes were among the differentially regulated genes, suggesting that the evolution of eusociality involved major nutritional and reproductive pathways.

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

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

Juvenile hormone, reproduction, and worker behavior in the neotropical social waspPolistes canadensis

Previous studies of the division of labor in colonies of eusocial Hymenoptera (wasps and bees) have led to two hypotheses regarding the evolution of juvenile hormone (JH) involvement. The novel- or single-function hypothesis proposes that the role of JH has changed from an exclusively reproductive function in primitively eusocial species (those lacking morphologically distinct queen and worker castes), to an exclusively behavioral function in highly eusocial societies (those containing morphologically distinct castes). In contrast, the split-function hypothesis proposes that JH originally functioned in the regulation of both reproduction and behavior in ancestral solitary species. Then, when reproductive and brood-care tasks came to be divided between queens and workers, the effects of JH were divided as well, with JH involved in regulation of reproductive maturation of egg-laying queens, and behavioral maturation, manifested as age-correlated changes in worker tasks, of workers. We report experiments designed to test these hypotheses. After documenting age-correlated changes in worker behavior (age polyethism) in the neotropical primitively eusocial wasp Polistes canadensis, we demonstrate that experimental application of the JH analog methoprene accelerates the onset of guarding behavior, an age-correlated task, and increases the number of foraging females; and we demonstrate that JH titers correlate with both ovarian development of queens and task differentiation in workers, as predicted by the split-function hypothesis. These findings support a view of social insect evolution that sees the contrasting worker and queen phenotypes as derived via decoupling of reproductive and brood-care components of the ancestral solitary reproductive physiology.

Queen and worker policing in monogynous and monandrous colonies of a primitively eusocial wasp

Kin-selection theory predicts that a worker prefers to produce her own sons in a colony with monandry and monogyny because relatedness to her sons (0.5) and nephews (0.375) exceeds that to brothers (0.25). In spite of this prediction, recent studies reveal that workers police each other (mutual-worker egg removal) even in monandrous and monogynous colonies. We conducted field and laboratory studies to evaluate queen and worker policing in queen-right colonies of the primitively eusocial wasp Polistes chinensis antennalis. Genetic studies using microsatellite markers, as well as extensive observations of natural colonies, revealed that both queen and workers removed both queen- and worker-laid eggs in monogynous and monandrous colonies. The queen's eggs survived to hatching more successfully than those of the workers (88.5% versus 1.4%). We discuss the likely factors to explain these worker-policing behaviours.

Why do workers of the primitively eusocial wasp Polistes chinensis antennalis remain at their natal nest?

In social insects, workers stay in their natal nests and help to rear their siblings, rather than founding independent nests. In three field experiments, we investigated the factors influencing the decision of workers of the paper wasp Polistes chinensis antennalis to stay in their natal nest. We divided nests of P.chinensis antennalis in half and placed each half separately in the field. Workers were then allowed to choose one of the halves, one of which had a queen and the other did not. Workers initially visited both halves, but later visited only one. When both half-nests contained brood, they were maintained by a group of wasps as two independent colonies, even though one had no queen. In addition, the initial presence of workers in the nests did not affect which nests were maintained. When one half-nest contained brood and the other did not, only the half with brood was maintained. This result is consistent with the ‘life insurance advantage’ hypothesis for the evolution of eusociality.

Self-organization of hierarchies in animal societies: the case of the primitively eusocial wasp Polistes dominulusChrist

Possible self-organizing processes leading to the formation of hierarchies in animal societies are studied. Biological data collected on the eusocial wasp Polistes dominulusChrist are first presented and used as a basis for building simple models. The models rely on a basic positive feedback mechanism, and assume that individuals do not recognize each other. Models were tested with Monte Carlo simulations, and, depending on parameters such as the functional forms used to describe the probabilities that an individual starts and subsequently wins a fight, we found an ensemble of different profiles whose functional implications are discussed.

Nestmate Copulation in the Neotropical Eusocial Wasp Polistes Instabilis de Saussure (Hymenoptera: Vespidae)

Copulation between individually marked nestmates of the Neotropical eusocial wasp Polistes instabilis is reported. Polistes copulations are rarely observed in the field; this observation is the first documented case of nestmate copulation in the genus. Hamilton (1964) predicted high rates of nestmate copulation for tropical Polistes populations which have asynchronous colony cycles relative to temperate populations. Nestmate copulation may lead to relatively high levels of inbreeding in tropical Polistes species.