A two-step adaptive walk rewires nutrient transport in a novel edaphic environment

Most well-characterized cases of adaptation involve single genetic loci. Theory suggests multi-locus adaptive walks should be common, but these are challenging to identify in natural populations. Here, we combine trait mapping with population genetic modeling to show that a two-step process rewired nutrient homeostasis in a population of Arabidopsis as it colonized the base of an active stratovolcano characterized by extremely low soil manganese (Mn). First, a variant that disrupted the primary iron (Fe) uptake transporter (IRT1) swept quickly to fixation in a hard selective sweep, increasing Mn but limiting Fe in the leaves. Second, multiple independent tandem duplications occurred at NRAMP1 and together rose to near-fixation in the island population, compensating the loss of IRT1 by improving Fe homeostasis. This study provides a clear case of a multi-locus adaptive walk and reveals how genetic variants reshaped a phenotype and spread over space and time.