Independent centromeric expansions define giant hornet genomes

Abstract Background The Vespa lineage of hornets demonstrate the potential to displace native species and cause significant damage to US apiculture through predation. In spite of introductions in recent years to North America, eradication efforts have prevented the Northern Giant Hornet, Vespa mandarinia, from establishing. Improved genomic resources could offer insight into the traits that define this lineage: large body size variance, adaptability to new environments, and high potential for invasiveness. 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. 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, indicating active, independent expansion. The intraspecific northern giant hornet genomes exhibit asymmetrical expansion across homologous chromosomal regions localized with Hi-C scaffolding. We leveraged pangenomic alignments of the hornet genomes to identify derived mutations, particularly those that affect repeat content and transposable elements (TEs). We found that TEs do not contribute to the bulk repeat content and show no differential expansion in genic space. Conclusions Large tandemly repetitive DNA account for large structural variations across the Vespa and between V. mandarinia. Localization within the genomes necessitated a suite of tools to support the assembly and identification of those elements. Typical repercussions of long-term reductions in population size – namely, reduced diversity and TE expansion – are not present. The degree to which alternative explanations, such as cell and body size selection or centromeric drive, cause massive, localized repeat amplification will require more extensive sampling.