Social wasps repair emergent topological defects

Social insects have evolved a variety of architectural formations. Bees and wasps are well known for their ability to achieve compact structures by building hexagonal cells. Polistes wattii, an open nesting paper wasp species, builds planar hexagonal structures. Here, using the pair correlation function approach, we show that their nests exhibit short-range hexagonal order but no long-range order akin to amorphous materials. Hexagonal orientational order was well preserved globally. We also show the presence of emergent topological defects such as disclination pairs (pentagon-heptagon dipoles), Stone-Wales quadrupoles, and other higher-order defects and discuss how these defects were fixed in the nest, thereby restoring order. Furthermore, we suggest the possible role of such defects in shaping nesting architectures of other social insect species.

Origin of an evolutionary novelty: the worker phenotype of eusocial wasps

Complex problems in evolutionary biology can be approached in two ways, top down using theoretical constructs and bottom up using empirical studies . Theoretical concepts predominate evolutionary interpretations of eusociality in a literature that is small relative to an enormous literature of natural history and basic research that is not synthesized into a conceptual whole. Here, I draw insights from this literature to show how paper wasps’ allomaternal non-reproductive worker phenotype originates in every colony cycle via confluence of multiple factors of paper wasp biology. These include behavior, development, nutrient dynamics, indirect genetic effects, sex ratio, and demography. A novel perspective on the colony cycle, based on individuals’ reproductive physiology, serves as context to examine of each of these. It will be shown that the allomaternal non-reproductive worker phenotype does not require relatedness among colony members to originate. Allomaternal care of non-relatives is frequent and can occur in at least twelve contexts. Life histories of living species as they will be presented here show that relatedness among colony members is not the target of selection in simple eusociality. However, the novel allomaternal non-reproductive worker phenotype had to be present at the ancestral origins of complex eusociality in which relatedness among colony members is essential.

Color is necessary for specialized face learning in the Northern paper wasp, Polistes fuscatus

Visual individual recognition requires animals to distinguish among conspecifics based on appearance. Though visual individual recognition has been reported in a range of taxa, the features that animals rely on to discriminate between individuals are often not well understood. Northern paper wasp females, Polistes fuscatus, possess individually distinctive color patterns on their faces, which mediate individual recognition. It is currently unclear what facial features P. fuscatus use to distinguish individuals. The anterior optic tubercle, a chromatic processing brain region, is especially sensitive to social experience during development, suggesting that color may be important for recognition in this species. We sought to test the roles of color in wasp facial recognition. Color may be important simply because it creates a pattern. If this is the case, then wasps should perform similarly when discriminating color or grayscale images of the same faces. Alternatively, color itself may be important for recognition, which would predict poorer performance on grayscale image discrimination relative to color images. We found wasps trained on grayscale faces, unlike those trained on color images, did not perform better than chance. Suggesting that color is necessary for the recognition of an image as a face by the wasp visual system.

Evidence for a selective link between cooperation and individual recognition

The ability to recognize and discriminate among others is a frequent assumption of models of the evolution of cooperative behavior. At the same time, cooperative behavior has been proposed as a selective agent favoring the evolution of individual recognition abilities. While theory predicts that recognition and cooperation may co-evolve, data linking recognition abilities and cooperative behavior with fitness or evidence of selection are elusive. Here, we provide evidence of a fitness link between individual recognition and cooperation in the paper wasp Polistes fuscatus. Nest founding females in northern populations frequently form cooperative multiple foundress nests and possess highly variable facial patterns that mediate individual recognition. We describe a dearth of cooperative nesting, low phenotypic diversity, and a lack of individual recognition in southern populations. In a common garden experiment, northern co-foundress associations successfully reared offspring while all cooperative southern groups failed to rear any offspring, suggesting a fitness link between individual recognition and successful cooperation. Consistent with a selective link between individual recognition and cooperation, we find that rates of cooperative co-nesting correlate with identity-signaling color pattern diversity across the species’ range. Moreover, genomic evidence of recent positive selection on cognition loci likely to mediate individual recognition is substantially stronger in northern compared to southern P. fuscatus populations. Collectively, these data suggest that individual recognition and cooperative nesting behavior have co-evolved in P. fuscatus because recognition helps mediate conflict among co-nesting foundresses. This work provides evidence of a specific cognitive phenotype under selection because of social interactions, supporting the idea that social behavior can be a key driver of cognitive evolution.

Dynamic neurogenomic responses to social interactions and dominance outcomes in female paper wasps

Social interactions have large effects on individual physiology and fitness. In the immediate sense, social stimuli are often highly salient and engaging. Over longer time scales, competitive interactions often lead to distinct social ranks and differences in physiology and behavior. Understanding how initial responses lead to longer-term effects of social interactions requires examining the changes in responses over time. Here we examined the effects of social interactions on transcriptomic signatures at two times, at the end of a 45-minute interaction and 4 hours later, in female Polistes fuscatus paper wasp foundresses. Female P. fuscatus have variable facial patterns that are used for visual individual recognition, so we separately examined the transcriptional dynamics in the optic lobe and the non-visual brain. Results demonstrate much stronger transcriptional responses to social interactions in the non-visual brain compared to the optic lobe. Differentially regulated genes in response to social interactions are enriched for memory-related transcripts. Comparisons between winners and losers of the encounters revealed similar overall transcriptional profiles at the end of an interaction, which significantly diverged over the course of 4 hours, with losers showing changes in expression levels of genes associated with aggression and reproduction in paper wasps. On nests, subordinate foundresses are less aggressive, do more foraging and lay fewer eggs compared to dominant foundresses and we find losers shift expression of many genes in the non-visual brain, including vitellogenin, related to aggression, worker behavior, and reproduction within hours of losing an encounter. These results highlight the early neurogenomic changes that likely contribute to behavioral and physiological effects of social status changes in a social insect.

Sex differences in deleterious genetic variants in a haplodiploid social insect

Deleterious variants are selected against but can linger in populations at low frequencies for long periods of time, decreasing fitness and contributing to disease burden in humans and other species. Deleterious variants occur at low frequency but distinguishing deleterious variants from low frequency neutral variation is challenging based on population genetics data. As a result, we have little sense of the number and identity of deleterious variants in wild populations. For haplodiploid species, it has been hypothesized that deleterious alleles will be directly exposed to selection in haploid males, but selection can be masked in diploid females due to partial or complete dominance, resulting in more efficient purging of deleterious mutations in males. Therefore, comparisons of the differences between haploid and diploid genomes from the same population may be a useful method for inferring rare deleterious variants. This study provides the first formal test of this hypothesis. Using wild populations of Northern paper wasps (Polistes fuscatus), we find that males have fewer overall variants, and specifically fewer missense and nonsense variants, than females from the same population. Allele frequency differences are especially pronounced for rare missense and nonsense mutations and these differences lead to a lower genetic load in males than females. Based on these data we estimate that a large number of highly deleterious mutations are segregating in the paper wasp population. Stronger selection against deleterious alleles in haploid males may have implications for adaptation in other haplodiploid insects and provides evidence that wild populations harbor abundant deleterious variants.