Whole Genome Resequencing Reveals Origins and Global Invasion Pathways of the Japanese Beetle Popillia japonica

Invasive species are an increasing global threat given their ability to rapidly spread and adapt to novel environments. The adverse ecological and economic impacts of invasive species highlight the critical need to understand the mechanisms that underpin invasion processes and success. The Japanese beetle, Popillia japonica, is an invasive pest of remarkable interest, as it feeds on hundreds of economically valuable plant species. It has been expanding outside of its native range in Japan since the first decades of the 20th century, colonising large areas of North America and, more recently, Europe. Here, we compared whole-genome resequencing data from individuals encompassing the entire species distribution to study the geographic differentiation of P. japonica populations and reconstruct expansion routes from Japan to the USA and Europe. We found six genomically distinguishable clusters, corresponding to the approximate colonisation areas at a continental scale. Our analysis supported an ancestral divergence between South and North/Central Japan, with the latter being the source of the initial invasion to the USA. Coalescent simulations supported independent bridgehead events from the USA to the Azores and Italy. We also investigated possible signals of selection to better understand the adaptive mechanisms that underlie the invasion success of P. japonica. However, the absence of strong selection signatures suggested that the beetle's adaptive ability might be embedded in pre-existing genomic features. Our comprehensive genome-wide dataset allowed a detailed inference of the invasion process and may be useful in determining the origin of P. japonica individuals in future invasion events.