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Abstract Vigilant animals detect and respond to threats in the environment, often changing posture and movement patterns. Vigilance is modulated not only by predators but also by conspecific threats. In social animals, precisely how conspecific threats alter vigilance behavior over time is relevant to long‐standing hypotheses about social plasticity. We report persistent effects of a simulated conspecific challenge on behavior of wild northern paper wasp foundresses,Polistes fuscatus. During the founding phase of the colony cycle, conspecific wasps can usurp nests from the resident foundress, representing a severe threat. We used automated tracking to monitor the movement and posture ofP. fuscatusfoundresses in response to simulated intrusions. Wasps displayed increased movement, greater bilateral wing extension, and reduced antennal separation after the threat was removed. These changes were not observed after presentation with a wooden dowel. By rapidly adjusting individual behavior after fending off an intruder, paper wasp foundresses might invest in surveillance of potential threats, even when such threats are no longer immediately present. The prolonged vigilance‐like behavioral state observed here is relevant to plasticity of social recognition processes in paper wasps. 

Abstract 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 genomics data alone. As a result, we have little sense of the number and identity of deleterious variants in wild populations. For haplodiploid species, it has been hypothesised that deleterious alleles will be directly exposed to selection in haploid males, but selection can be masked in diploid females when deleterious variants are recessive, 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 missense and nonsense variants per generation than females from the same population. Allele frequency differences are especially pronounced for rare missense and nonsense variants and these differences lead to a lower mutational load in males than females. Based on these data we infer that many 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 harbour abundant deleterious variants. 

Abstract Paper wasps are a model system for the study of social evolution due to a high degree of inter- and intraspecific variation in cooperation, aggression, and visual signals of social status. Increasing the taxonomic coverage of genomic resources for this diverse clade will aid comparative genomic approaches for testing predictions about the molecular basis of social evolution. Here, we provide draft genome assemblies for two well-studied species of paper wasps, Polistes exclamans and Mischocyttarus mexicanus. The P. exclamans genome assembly is 221.5 Mb in length with a scaffold N50 of 4.11 Mb. The M. mexicanus genome assembly is 227 Mb in length with a scaffold N50 of 1.1 Mb. Genomes have low repeat content (9.54–10.75%) and low GC content (32.06–32.4%), typical of other social hymenopteran genomes. The DNA methyltransferase gene, Dnmt3 , was lost early in the evolution of Polistinae. We identified a second independent loss of Dnmt3 within hornets (genus: Vespa). 

The ability to recognize others is a frequent assumption of models of the evolution of cooperation. At the same time, cooperative behavior has been proposed as a selective agent favoring the evolution of individual recognition abilities. Although theory predicts that recognition and cooperation may co-evolve, data linking recognition abilities and cooperative behavior with evidence of selection are elusive. Here, we provide evidence of a selective link between individual recognition and cooperation in the paper wasp Polistes fuscatus through a combination of clinal, common garden, and population genomics analyses. We identified latitudinal clines in both rates of cooperative nesting and color pattern diversity, consistent with a selective link between recognition and cooperation. In behavioral experiments, we replicated previous results demonstrating individual recognition in cooperative and phenotypically diverse P. fuscatus from New York. In contrast, wasps from a less cooperative and phenotypically uniform Louisiana population showed no evidence of individual recognition. In a common garden experiment, groups of wasps from northern populations formed more stable and individually biased associations, indicating that recognition facilitates group stability. The strength of recent positive selection on cognition-associated loci likely to mediate individual recognition is substantially greater in northern compared with southern P. fuscatus populations. Collectively, these data suggest that individual recognition and cooperative nesting behavior have co-evolved in P. fuscatus because recognition helps stabilize social groups. 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. 

Abstract Independent origins of sociality in bees and ants are associated with independent expansions of particular odorant receptor (OR) gene subfamilies. In ants, one clade within the OR gene family, the 9-exon subfamily, has dramatically expanded. These receptors detect cuticular hydrocarbons (CHCs), key social signaling molecules in insects. It is unclear to what extent 9-exon OR subfamily expansion is associated with the independent evolution of sociality across Hymenoptera, warranting studies of taxa with independently derived social behavior. Here, we describe OR gene family evolution in the northern paper wasp, Polistes fuscatus, and compare it to four additional paper wasp species spanning ∼40 million years of evolutionary divergence. We find 200 putatively functional OR genes in P. fuscatus, matching predictions from neuroanatomy, and more than half of these are in the 9-exon subfamily. Most OR gene expansions are tandemly arrayed at orthologous loci in Polistes genomes, and microsynteny analysis shows species-specific gain and loss of 9-exon ORs within tandem arrays. There is evidence of episodic positive diversifying selection shaping ORs in expanded subfamilies. Values of omega (dN/dS) are higher among 9-exon ORs compared to other OR subfamilies. Within the Polistes OR gene tree, branches in the 9-exon OR clade experience relaxed negative (relaxed purifying) selection relative to other branches in the tree. Patterns of OR evolution within Polistes are consistent with 9-exon OR function in CHC perception by combinatorial coding, with both natural selection and neutral drift contributing to interspecies differences in gene copy number and sequence. 

Many animals are able to perform recognition feats that astound us—such as a rodent recognizing kin it has never met. Yet in other contexts, animals appear clueless as when reed warblers rear cuckoo chicks that bear no resemblance to their own species. Failures of recognition when it would seem adaptive have been especially puzzling. Here, we present a simple tug-of-war game theory model examining how individuals should optimally invest in affecting the accuracy of discrimination between desirable and undesirable recipients. In the game, discriminating individuals (operators) and desirable and undesirable recipients (targets and mimics, respectively) can all invest effort into their own preferred outcome. We demonstrate that stable inaccurate recognition will arise when undesirable recipients have large fitness gains from inaccurate recognition relative to the pay-offs that the other two parties receive from accurate recognition. The probability of accurate recognition is often determined by just the relative pay-offs to the desirable and undesirable recipients, rather than to the discriminator. Our results provide a new lens on long-standing puzzles including a lack of nepotism in social insect colonies, tolerance of brood parasites and male birds caring for extra-pair young in their nests, which our model suggests should often lack accurate discrimination. This article is part of the theme issue ‘Signal detection theory in recognition systems: from evolving models to experimental tests'. 

Social interactions are mediated by recognition systems, meaning that the cognitive abilities or phenotypic diversity that facilitate recognition may be common targets of social selection. Recognition occurs when a receiver compares the phenotypes produced by a sender with a template. Coevolution between sender and receiver traits has been empirically reported in multiple species and sensory modalities, though the dynamics and relative exaggeration of traits from senders versus receivers have received little attention. Here, we present a coevolutionary dynamic model that examines the conditions under which senders and receivers should invest effort in facilitating individual recognition. The model predicts coevolution of sender and receiver traits, with the equilibrium investment dependent on the relative costs of signal production versus cognition. In order for recognition to evolve, initial sender and receiver trait values must be above a threshold, suggesting that recognition requires some degree of pre-existing diversity and cognitive abilities. The analysis of selection gradients demonstrates that the strength of selection on sender signals and receiver cognition is strongest when the trait values are furthest from the optima. The model provides new insights into the expected strength and dynamics of selection during the origin and elaboration of individual recognition, an important feature of social cognition in many taxa. This article is part of the theme issue ‘Signal detection theory in recognition systems: from evolving models to experimental tests’. 

Abstract Relatively little is known about the processes shaping population structure in cooperatively breeding insect species, despite the long-hypothesized importance of population structure in shaping patterns of cooperative breeding. Polistes paper wasps are primitively eusocial insects, with a cooperative breeding system in which females often found nests in cooperative associations. Prior mark-recapture studies of Polistes have documented extreme female philopatry, although genetic studies frequently fail to detect the strong population structure expected for highly philopatric species. Together these findings have led to lack of consensus on the degree of dispersal and population structure in these species. This study assessed population structure of female Polistes fuscatus wasps at three scales: within a single site, throughout Central New York, and across the Northeastern United States. Patterns of spatial genetic clustering and isolation by distance were observed in nuclear and mitochondrial genomes at the continental scale. Remarkably, population structure was evident even at fine spatial scales within a single collection site. However, P. fuscatus had low levels of genetic differentiation across long distances. These results suggest that P. fuscatus wasps may employ multiple dispersal strategies, including extreme natal philopatry as well as longer-distance dispersal. We observed greater genetic differentiation in mitochondrial genes than in the nuclear genome, indicative of increased dispersal distances in males. Our findings support the hypothesis that limited female dispersal contributes toward population structure in paper wasps.