Independent Expansions Define Giant Hornet Genomes

Background Body size and invasiveness are highly significant ecological and agricultural traits. The Vespa lineage of hornets demonstrates extreme variation in both traits. In addition, many Vespa species destroy beehives and are of great concern to honey producers. The underlying causes of enlarged body sizes are complex, but genome expansion can be an avenue to larger cell size and larger bodies. Emerging long-read technology can overcome many of the limits imparted by large concentrations of repetitive DNA. Results We sequenced and assembled genomes of two lineages of the northern giant hornet, Vespa mandarinia , and one of the European hornet, Vespa crabro , using HiFi long read sequencing technology to ascertain the degree of genomic expansion, if any, in this system. We found centromeric and pericentric satellite repeats account for nearly half the total DNA of the hornet genomes and their identities were largely unique across species. The intraspecific northern giant hornet genomes exhibit asymmetrical expansion across homologous regions localized with Hi-C scaffolding. Further, we leveraged pangenomic alignments of the hornet genomes. Transposable elements do not contribute to the bulk repeat content and show no differential expansion in genic space. Conclusions Though body, population, and genome size are often confounded, the relative lack of transposable element colonization and high genetic diversity of large Vespa suggests selection at the organismal level, potentially acting in concert with centromeric drive. Indeed, two major centromeric polymorphisms in V. mandarinia are bounded by variants bearing hallmarks of selection, disentangling two (population size and genome size) of the three confounded variables.