Pangenome analyses reveal divergence and extensive introgression in two global corn pests

Introgression between closely related species can profoundly influence evolutionary trajectories, yet how genomic divergence interacts with introgression, especially in invasive hybridization, remains insufficiently understood. Structural variants (SVs), particularly chromosomal inversions, are key contributors to divergence and may modulate patterns of gene flow. The Asian corn borer (ACB) and European corn borer (ECB), two globally important agricultural pests, provide an excellent system to investigate these processes.

We construct a graph-based pangenome from 23 high-quality genome assemblies to characterize genome-wide SVs and introgression between ACB and ECB. We identify over 216,000 SVs, most of which are associated with transposable elements and contribute to interspecific divergence. Population genomic analyses reveal widespread yet asymmetric introgression, predominantly from ACB into ECB populations in China. Introgressed regions are more prevalent in autosomes than in sex chromosomes and are enriched for genes involved in adaptive pathways. In contrast, large inversion regions on the Z chromosome exhibit strong genetic differentiation and reduced introgression, suggesting a role in maintaining species barriers. Notably, a highly divergent region containing the circadian clock gene period (per) shows signatures of selection. Functional validation using CRISPR/Cas9 demonstrates that per significantly influences diapause regulation, linking genomic divergence to adaptive phenotypic variation.

Our results demonstrate that introgression and structural variation jointly shape genomic divergence in these species. While introgression facilitates the spread of adaptive variation, chromosomal inversions restrict gene flow and maintain species integrity. This study provides new insights into the evolutionary mechanisms underlying divergence, adaptation, and invasion in major agricultural pests.