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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 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). 

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 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. 

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. 

Cognitive abilities can vary dramatically among species. The relative importance of social and ecological challenges in shaping cognitive evolution has been the subject of a long-running and recently renewed debate, but little work has sought to understand the selective dynamics underlying the evolution of cognitive abilities. Here, we investigate recent selection related to cognition in the paper waspPolistes fuscatus—a wasp that has uniquely evolved visual individual recognition abilities. We generate high quality de novo genome assemblies and population genomic resources for multiple species of paper wasps and use a population genomic framework to interrogate the probable mode and tempo of cognitive evolution. Recent, strong, hard selective sweeps inP. fuscatuscontain loci annotated with functions in long-term memory formation, mushroom body development, and visual processing, traits which have recently evolved in association with individual recognition. The homologous pathways are not under selection in closely related wasps that lack individual recognition. Indeed, the prevalence of candidate cognition loci within the strongest selective sweeps suggests that the evolution of cognitive abilities has been among the strongest selection pressures inP. fuscatus’ recent evolutionary history. Detailed analyses of selective sweeps containing candidate cognition loci reveal multiple cases of hard selective sweeps within the last few thousand years on de novo mutations, mainly in noncoding regions. These data provide unprecedented insight into some of the processes by which cognition evolves. 

Abstract Natural history collections (NHCs) are important resources for a diverse array of scientific fields. Recent digitization initiatives have broadened the user base of NHCs, and new technological innovations are using materials generated from collections to address novel scientific questions. Simultaneously, NHCs are increasingly imperiled by reductions in funding and resources. Ensuring that NHCs continue to serve as a valuable resource for future generations will require the scientific community to increase their contribution to and acknowledgement of collections. We provide recommendations and guidelines for scientists to support NHCs, focusing particularly on new users that may be unfamiliar with collections. We hope that this perspective will motivate debate on the future of NHCs and the role of the scientific community in maintaining and improving biological collections.