Historical genomics reveals the evolutionary mechanisms behind multiple outbreaks of the host-specific coffee wilt pathogen Fusarium xylarioides

Nearly 50% of crop yields are lost to pests and disease, with plants and pathogens locked in an amplified co-evolutionary process of disease outbreaks. Coffee wilt disease, caused by Fusarium xylarioides, decimated coffee production in west and central Africa following its initial outbreak in the 1920s. After successful management, it later re-emerged and by the 2000s comprised two separate epidemics on arabica coffee in Ethiopia and robusta coffee in east and central Africa. Here, we use genome sequencing of six historical culture collection strains spanning 70 years to identify the evolutionary processes behind these repeated outbreaks. The robusta population arose from the initial outbreak, whilst the arabica population is divergent and emerged independently. We show that the two populations evolved similar pathologies on the different hosts by separately acquiring different effector genes horizontally. Horizontal transfer occurred by movements of genes linked to transposable elements rather than by the transfer of whole pathogenicity chromosomes. Potential donors comprised other Fusarium taxa, including F. oxysporum, which is known to share coffee as a host as well as other plants intercropped with coffee in the same region. Our results show how historical genomics can help reveal mechanisms that allow fungal pathogens to keep pace with our efforts to resist them. Our list of putative effector genes identifies possible future targets for fungal control. In turn, knowledge of horizontal transfer mechanisms and putative donor taxa might help to design future intercropping strategies that minimize the risk of transfer of effector genes between closely-related Fusarium taxa.