Global invasion history and genomic signatures of adaptation of a highly invasive lace bug

Invasive species cause enormous economic and ecological damage. Climate change has resulted in an unprecedented increase in the number and impact of invaders. The mechanisms underlying invasions, however, are largely unclear. The sycamore lace bug, Corythucha ciliata , is a highly invasive species that originated in North America. Its population has expanded over the Northern Hemisphere since the 1960s. In this study, we assemble the lace bug’s genome using high-coverage PacBio, Illumina, and Hi-C sequencing. We identify 15,278 protein-coding genes and expansion of gene families with oxidoreductase and metabolic activities. In-depth resequencing of 402 samples collected from native and nine invasive countries across three continents identified 2.74 million single nucleotide polymorphisms. We resolve two major invasion routes of this lace bug from North America through both Europe and Japan, forming a contact zone in East Asia. Genomic signatures of selection associated with invasion and long-term balancing selection in native ranges are identified. These genomic signatures overlap with each other and the expanded genes, suggesting an improvement in the oxidative stress and thermal tolerance of this species. Our findings offer valuable insights into the genomic architecture and adaptive evolution underlying the invasive capabilities of species in the face of rapid environmental changes.