Using herbarium genomics to understand the history of a global plant invasion

Abstract

Invasive plants are dynamic eco-evolutionary systems characterized by rapid spread and evolutionary change. Herbarium genomics offers a powerful way to study these processes across broad spatial and temporal scales. We generated low-coverage shotgun-sequencing data from 152 herbarium specimens of the invasive Japanese knotweed species complex (Reynoutria), collected across its native range in Japan and China, and its introduced ranges in Europe and North America, spanning 200 years of global spread. Introduced populations of R. japonica, R. japonica var. compacta and R. sachalinensis showed reduced genetic diversity compared to native populations and were genetically most similar to Japanese specimens, indicating Japan as the source of all three introductions. European and North American R. japonica were genetically highly similar and closely related to local R. x bohemica hybrids, suggesting that these hybrids originated post-introduction, through hybridization and subsequent introgression from the R. japonica parent. A few R. x bohemica hybrids in the UK and France shared a multilocus lineage with R. sachalinensis, indicating an independent but ecologically less successful hybridization event involving introgression from R. sachalinensis. A genetically distinct R. x bohemica from Japan was closely related to a Japanese R. sachalinensis specimen, suggesting that hybridization also occurs in the native range. Introduced R. japonica has remained genetically uniform for [~]200 years reflecting long-term founder effects. The dominance of a single R. japonica lineage supports the general-purpose genotype hypothesis and the importance of vegetative reproduction in its spread. Herbarium genomics thus uncovers the origin and global spread of Japanese knotweed, providing direct molecular evidence of long-term plant invasions.