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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 wasp Polistes 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 in P. fuscatus contain 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 in P. 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.

Transgenic crops producing crystalline (Cry) proteins from the bacterium Bacillus thuringiensis (Bt) have been used extensively to control some major crop pests. However, many populations of the noctuid moth Helicoverpa zea, one of the most important crop pests in the United States, have evolved practical resistance to several Cry proteins including Cry1Ac. Although mutations in single genes that confer resistance to Cry proteins have been identified in lab-selected and gene-edited strains of H. zea and other lepidopteran pests, the genetic basis of field-evolved resistance to Cry proteins in H. zea has remained elusive. We used a genomic approach to analyze the genetic basis of field-evolved resistance to Cry1Ac in 937 H. zea derived from 17 sites in seven states of the southern United States. We found evidence for extensive gene flow among all populations studied. Field-evolved resistance was not associated with mutations in 20 single candidate genes previously implicated in resistance or susceptibility to Cry proteins in H. zea or other lepidopterans. Instead, resistance in field samples was associated with increased copy number of a cluster of nine trypsin genes. However, trypsin gene amplification occurred in a susceptible sample and not in all resistant samples, implying that this amplification does not always confer resistance and mutations in other genes also contribute to field-evolved resistance to Cry1Ac in H. zea. The mismatch between lab-generated and field-evolved resistance in H. zea is unlike other cases of Bt resistance and reflects challenges for managing this pest. [ABSTRACT FROM AUTHOR]

Paper wasps (genus Polistes) are one of the most species-rich genera of social insect. Prior studies have found that male coloration, male colour pattern, territory choice and female caste are potential drivers of intraspecific mate choice in paper wasps. However, there has been no formal assessment of interspecific mate choice in this group; therefore, the mechanism driving diversification in paper wasps remains an open question. In this study, we measured interspecific and intraspecific mating behaviour between two closely related species of paper wasps, Polistes fuscatus and Polistes metricus. These two species have ample opportunity to interbreed because P. fuscatus and P. metricus forage, nest and mate in the same habitats. We tested the strength of reproductive isolation between these species using no-choice and choice mating trials. Our results show strong, symmetric, prezygotic isolation between P. fuscatus and P. metricus. Males discriminated between conspecifics and heterospecifics but attempted to mate with females of the other species in ~10% of heterospecific mating trials. Female wasps were more discriminating than males and probably evaluated species identity and male quality through visual or olfactory cues. We additionally report sexual dimorphism in P. metricus body size. [ABSTRACT FROM AUTHOR]

Olfaction mediates many behaviors in social Hymenoptera, with sexual dimorphism in antennal transcription associated with different behaviors between sexes. Females display coordinated social behaviors within colonies, while males exhibit limited social behavior but are selected for finding mates. The expanded "9-exon" odorant receptor (OR) gene subfamily is associated with chemical communication and exhibits strongly female biased antennal transcription in ants and honey bees. Polistine wasps represent an independent evolution of sociality and associated expansion of 9-exon ORs, though antennal expression patterns are unknown. Here, we report distinct patterns of sexually dimorphic OR transcription in Polistes fuscatus compared to ants and bees. Most P. fuscatus 9-exon transcripts were detected at similar levels in males and females, and some were male biased. We also report differential antennal transcription of cytochromes P450 and muscle-related genes between sexes. We discuss these patterns in the context of the unique sexual and social behaviors of Polistes wasps, including prolonged male mating aggregations and male antennal tapping and curling during courtship and copulation. These results call attention to the lineage-specific selective pressures shaping sexually dimorphic antennal transcription in social insects.