Genetic and epigenetic variation separately contribute to range expansion and local metalliferous habitat adaptation during invasions of Chenopodium ambrosioides into China.

BACKGROUND AND AIMS: Invasive plants often colonize wide-ranging geographical areas with various local microenvironments. The specific roles of epigenetic and genetic variation during such expansion are still unclear. Chenopodium ambrosioides is a well-known invasive alien species in China that can thrive in metalliferous habitats. This study aims to comprehensively understand the effects of genetic and epigenetic variation on the successful invasion of C. ambrosioides. METHODS: We sampled 367 individuals from 21 heavy metal-contaminated and uncontaminated sites with a wide geographical distribution in regions of China. We obtained environmental factors of these sampling sites, including 13 meteorological factors and the contents of four heavy metals in soils. Microsatellite markers were used to investigate the demographic history of C. ambrosioides populations in China. We also analysed the effect of epigenetic variation on metalliferous microhabitat adaptation using methylation-sensitive amplified polymorphism (MSAP) markers. A common garden experiment was conducted to compare heritable phenotypic variations among populations. KEY RESULTS: Two distinct genetic clusters that diverged thousands of years ago were identified, suggesting that the eastern and south-western C. ambrosioides populations in China may have originated from independent introduction events without recombination. Genetic variation was shown to be a dominant determinant of phenotypic differentiation relative to epigenetic variation, and further affected the geographical distribution pattern of invasive C. ambrosioides. The global DNA unmethylation level was reduced in metalliferous habitats. Dozens of methylated loci were significantly associated with the heavy metal accumulation trait of C. ambrosioides and may contribute to coping with metalliferous microenvironments. CONCLUSIONS: Our study of C. ambrosioides highlighted the dominant roles of genetic variation in large geographical range expansion and epigenetic variation in local metalliferous habitat adaptation.