Range expansion compromises adaptive evolution in an outcrossing plant

Neutral genetic diversity gradients have long been used to infer the colonization history of species, but range expansion may also influence the efficacy of natural selection and patterns of non-synonymous polymorphism in different parts of a species’ range. Recent theory predicts both an accumulation of deleterious mutations and a reduction in the efficacy of positive selection as a result of range expansion. These signatures have been sought in a number of studies of the human range expansion out of Africa, but with contradictory results. We analyzed the polymorphism patterns of 578,125 SNPs (17,648 genes) in the European diploid plant Mercurialis annua, which expanded its range from an eastern Mediterranean refugium into western habitats with contrasted climates. Our results confirmed strong signatures of bottlenecks and revealed the accumulation of mildly to strongly deleterious mutations in range-front populations. A significantly higher number of these mutations were homozygous in individuals in range-front populations, pointing to increased genetic load and reduced fitness under a model of recessive deleterious effects. We also inferred a reduction in the number of selective sweeps in range-front versus core populations. These signatures have persisted even in a dioecious herb subject to substantial interpopulation gene flow. Our results extend support from humans to plants for theory on the dynamics of mutations under selection during range expansion, showing that colonization bottlenecks can compromise adaptive potential.