DNA methylation is associated with genomic architecture, genetic variation and dispersal-related traits in an expanding invasion

The importance of epigenetics in invasion biology is debated. In particular, the role of epigenetic mechanisms, such as DNA methylation, as potential drivers of rapid adaptation compensating for reduced genetic diversity remains an open question. Introduced to Australia 90 years ago, cane toads (Rhinella marina) are spreading at an ever-increasing rate. Across the invasion range, toads display overall low genetic diversity, yet paradoxically show high phenotypic variation in dispersal-related traits. Here, we use a common-garden experiment to investigate the role of DNA methylation in fostering rapid evolution in this system. We show that toads from newly established populations show distinct DNA methylation profiles to toads from long-colonized areas, particularly in genes putatively involved in dispersal. Epigenetic changes were strongly associated with genetic variation and often overlapped with transposable elements. Our results indicate that epigenetic changes following environmental perturbations have the potential to generate phenotypic variation at ecologically relevant traits in genetically depauperate invasive populations, their molecular interplay with gene activity being complex and probably context-dependent. This article is part of the theme issue 'Ecological epigenetics at the intersection of behaviour and life history variation in non-model animals'.