The genetic architecture of an aphid (Myzus persicae) host shift: an adaptive walk protected an aphid (Myzus p. nicotianae) and its endosymbiont from plant chemical defences. Myzus persicae

Host shifts can lead to ecological speciation and the formation of new pests and pathogens. However, the mutational events that facilitate the exploitation of a novel host are poorly understood. Here we characterise, at fine resolution, an adaptive walk underpinning the host shift of the aphid Myzus persicae to tobacco which overcame the chemical defences of this plant. We uncover a continuum of mutational events that added up to 1.5 million nucleotides to the tobacco-adapted subspecies, M. p. nicotianae. These led to profound increases in the expression of an enzyme that efficiently detoxifies nicotine in the gut and in bacteriocytes, specialised aphid cells which house the obligate symbiont Buchnera aphidicola. This dual evolutionary solution overcame the challenge of preserving the fitness of a mutualistic symbiosis during adaptation to a toxic novel host. Our results reveal the intricate processes by which genetic novelty can arise and drive the evolution of key innovations required for ecological adaptation.