Host shifts can lead to ecological speciation and the emergence of new pests and pathogens. However, the mutational events that facilitate the exploitation of novel hosts are poorly understood. Here, we characterize an adaptive walk underpinning the host shift of the aphid Myzus persicae to tobacco, including evolution of mechanisms that overcame tobacco chemical defenses. A series of mutational events added as many as 1.5 million nucleotides to the genome of the tobacco-adapted subspecies, M. p. nicotianae, and yielded profound increases in expression of an enzyme that efficiently detoxifies nicotine, both in aphid gut tissue and in the bacteriocytes housing the obligate aphid symbiont Buchnera aphidicola. This dual evolutionary solution overcame the challenge of preserving 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.

Bayer AG Crop Science Division R and D Alfred Nobel Strasse 50 40789 Monheim Germany

Biology Centre of the Czech Academy of Sciences Institute of Entomology 370 05 České Budějovice Czech Republic

College of Life and Environmental Sciences Biosciences University of Exeter Penryn Campus Penryn Cornwall UK

Department of Biointeractions and Crop Protection Rothamsted Research Harpenden UK

Department of Crop Science Agricultural University of Athens Athens Greece

Department of Sustainable Crop Production Section Sustainable Crop and Food Protection Università Cattolica del Sacro Cuore Piacenza Italy

Institute of Molecular Biology and Biotechnology Foundation for Research and Technology Hellas Crete Greece

University of South Bohemia Faculty of Science 370 05 České Budějovice Czech Republic

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