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Abstract Insects have evolved remarkably complex social systems. Social wasps are particularly noteworthy because they display gradations in social behaviors. Here, we sequence the genomes of two highly diverged Vespula wasps, V. squamosa and V. maculifrons Buysson (Hymenoptera: Vespidae), to gain greater insight into the evolution of sociality. Both V. squamosa and V. maculifrons are social wasps that live in large colonies characterized by distinct queen and worker castes. However, V. squamosa is a facultative social parasite, and V. maculifrons is its frequent host. We found that the genomes of both species were ~200 Mbp in size, similar to the genome sizes of congeneric species. Analyses of gene expression from members of different castes and developmental stages revealed similarities in expression patterns among immature life stages. We also found evidence of DNA methylation within the genome of both species by directly analyzing DNA sequence reads. Moreover, genes that were highly and uniformly expressed were also relatively highly methylated. We further uncovered evidence of differences in patterns of molecular evolution in the two taxa, consistent with V. squamosa exhibiting alterations in evolutionary pressures associated with its facultatively parasitic or polygyne life history. Finally, rates of gene evolution were correlated with variation in gene expression between castes and developmental stages, as expected if more highly expressed genes were subject to stronger levels of selection. Overall, this study expands our understanding of how social behavior relates to genome evolution in insects. 

Abstract The study of social parasitism faces numerous challenges arising from the intricate and intranidal host–parasite interactions and the rarity of parasites compared to their free-living counterparts. As a result, our understanding of the ecology and evolution of most social parasites remains limited. Using whole-genome and reduced-representation sequence data, we conducted a study to fill knowledge gaps on host use, colony social structure, and population genetics of the facultative dulotic ant Formica aserva Forel. Our study reveals the remarkable ability of F. aserva to exploit at least 20 different host species across its wide geographic distribution. In some cases, one social parasite colony exploits multiple hosts simultaneously, suggesting a high degree of generalization even at a local spatial scale. Approximately 80% of the colonies were monogyne (with a single queen), with many exhibiting higher rates of polyandry compared to most Formica ants. Although we identified a supergene on chromosome 3, its association with colony structure remains uncertain due to the rarity of polygyny in our sample. Population genetic analyses reveal substantial geographic population structure, with the greatest divergence between California populations and those from the rest of the range. Mitochondrial population structure differs from structure inferred from the nuclear genome on a broad geographic scale, suggesting a possible role of adaptive introgression or genetic drift. This study provides valuable insights into the ecology and evolution of F. aserva, underscoring the need for further research to decipher the complexities of host interactions and the genetic mechanisms that regulate social structure.