Genomic analyses of the southern and eastern yellowjacket wasps (Hymenoptera: Vespidae) reveal evolutionary signatures of social life

The evolution of sociality in insects represented a remarkable development in biological history. Social wasps are particularly noteworthy because they display gradations in social behaviors. Here, we sequence the genomes of two highly diverged Vespula wasps to gain greater insight into the evolution of sociality. Both V. squamosa and V. maculifrons Buysson (Hymenoptera: Vespidae) are highly social wasps and live in large colonies characterized by distinct caste systems. 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 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. Next, we found evidence of DNA methylation within the genome of both species directly from PacBio HiFi DNA sequence reads. Patterns of gene expression were correlated with DNA methylation levels within genes; genes that were highly and uniformly expressed were also relatively highly methylated. Finally, we uncovered evidence of differences in patterns of molecular evolution in the two taxa, consistent with V. squamosa showing changes in selective constraint associated with its facultatively parasitic or polygyne life history. Moreover, 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 genomic consequences of social evolution in insects. Keywords: Social Insects, Genetics, Behavior, Population Genetics, Vespidae Entomological Society of America Editorial Office: 170 Jennifer Road, Suite 230, Annapolis, MD 21401, USA. Editorial Office Phone: [phone].

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Methods
Vespula squamosa and Vespula maculifrons transposable elements and methylation coverage files. Transposable element annotation generated from EDTA v2.1.0 and methylation analysis conducted in SeqMonk v1.48.1.