Population genomics reveals global invasion history of Bursaphelenchus xylophilus based on a high‐quality gap‐free reference genome

BACKGROUND: Bursaphelenchus xylophilus is one of the most destructive invasive alien species in global forestry, causing widespread pine mortality and severe ecological damage. Clarifying its evolutionary patterns, invasion routes and adaptive signatures helps refine the evolutionary theory of plant-parasitic nematodes, and provides practical references for invasion prevention and targeted management. RESULTS: The first chromosome-level gap-free reference genome of B. xylophilus was assembled. The genome spans 78.02 Mb with a contig N50 of 12.60 Mb. All sequences were anchored to six chromosomes, and the BUSCO completeness was estimated at 99.50%. Comparative genomic analysis revealed that B. xylophilus and Bursaphelenchus mucronatus diverged approximately 4.85-24.67 million years ago. Further evolutionary analysis of gene families indicated a striking evolutionary asymmetry between these two species. Population structure analysis revealed that global B. xylophilus populations can be classified into four major genetic groups. Gene flow analyses suggest two potential invasion centers may exist in China. Through the integration of selective sweep analysis, we also identified putative adaptive loci in the two Chinese populations. Due to sampling limitations, the exact geographical origins of some overseas isolates remain unclear, and samples from key regions including South Korea and Europe are not included in this study. Accordingly, the inferences regarding invasion routes need to be further verified with additional population data. CONCLUSION: This study generated a B. xylophilus genome assembly with substantially improved continuity, completeness and accuracy. The resultant high-quality genome provides a fundamental dataset for dissecting its invasion mechanisms and validating gene functions. Furthermore, our findings elucidate the genomic basis underlying the strong invasiveness of this nematode, clarify its global dispersal routes, and identify putative loci associated with adaptive evolution after invasion. © 2026 Society of Chemical Industry.