Selective ancestral sorting and de novo evolution in the agricultural invasion of Amaranthus tuberculatus

Abstract

The relative role of hybridization, de novo evolution, and standing variation in weed adaptation to agricultural environments is largely unknown. In Amaranthus tuberculatus, a widespread North American agricultural weed, adaptation is likely influenced by recent secondary contact and admixture of two previously isolated subspecies. We characterized the extent of adaptation and phenotypic differentiation accompanying the spread of A. tuberculatus into agricultural environments and the contribution of subspecies divergence. We generated phenotypic and whole-genome sequence data from a manipulative common garden experiment, using paired samples from natural and agricultural populations. We found strong latitudinal, longitudinal, and sex differentiation in phenotypes, and subtle differences among agricultural and natural environments that were further resolved with ancestry-based inference. The transition into agricultural environments has favoured southwestern var. rudis ancestry that leads to higher biomass and environment-specific phenotypes: increased biomass and earlier flowering under reduced water availability, and reduced plasticity in fitness-related traits. We also detected de novo adaptation to agricultural habitats independent of ancestry effects, including marginally higher biomass and later flowering in agricultural populations, and a time to germination home advantage. Therefore, the invasion of A. tuberculatus into agricultural environments has drawn on adaptive variation across multiple timescales—through both preadaptation via the preferential sorting of var. rudis ancestry and de novo local adaptation.