Human-Mediated Dispersal Drives Global Invasion of Halyomorpha halys: A COI Haplotype and Mantel Test Analysis

The brown marmorated stink bug, Halyomorpha halys (Hemiptera: Pentatomidae), is a globally invasive agricultural pest that has rapidly expanded across North America, Europe, and Asia over the past three decades. Understanding the drivers of its invasion success is critical for predicting future spread and informing management. In this study, we assembled a comprehensive mitochondrial COI dataset comprising 1039 sequences from 15 countries across the species' native and introduced ranges, including 119 newly obtained sequences. We identified 65 haplotypes, including eight novel variants, and performed genetic diversity analysis, haplotype network reconstruction, and Mantel tests to quantitatively assess whether patterns of genetic differentiation are consistent with isolation by distance (IBD) or isolation by environment (IBE). Native populations, particularly China and Japan, exhibited high haplotype diversity and pronounced genetic differentiation, suggesting long-term independent evolution. Introduced populations generally showed reduced diversity consistent with founder effects, with two notable exceptions: Greece and Belgium displayed high haplotype diversity and positive Fu's Fs values, identifying them as potential genetic admixture zones resulting from multiple introductions. The haplotype network revealed two dominant lineages, H1 and H3, with distinct geographic distributions. Mantel tests detected no significant correlations between genetic distance and either geographic distance or climatic dissimilarity (p > 0.05). While the limited resolution of a single mitochondrial marker precludes definitive conclusions about the absence of IBD/IBE, these findings are consistent with the hypothesis that frequent and large-scale human-mediated dispersal may have overwhelmed signals of natural population structure. By quantitatively decoupling genetic structure from biogeographic templates, this study advances our understanding of invasion mechanisms and underscores the need for biosecurity strategies that target human-mediated dispersal pathways.