Co-phylogenetic constraints on host breadth within an emerging fungal pathogen complex of global concern

Emerging fungal infectious diseases constitute the largest pathogen threat to plants. However, the factors influencing fungal-plant interactions, host shifts, and the emergence of pathogens on a novel host are still not well understood. Evolutionary relationships among hosts appear to be important, with closely related hosts often sharing pathogens and pests, but we typically lack information on the evolutionary history of the pathogens. Here, we gather over 27,000 sequences to construct a comprehensive phylogenetic tree for Botryosphaeriaceae, a fungal family including many emerging pathogens of global concern, and explore the evolutionary conservatism in fungal-plant associations across host and pathogen phylogenies. We reveal a significant influence of both phylogenies in constraining fungal-plant associations. However, we also show that most fungal pathogens are generalists, able to infect multiple hosts, and demonstrate an evolutionary trend toward increased generalism, contrary to theory that suggests that pathogens should evolve toward increased host specialization. We suggest that the anthropogenic movement of plant species and agricultural practices might have allowed some Botryosphaeriaceae to escape phylogenetic constraints on host range via increasing the ecological opportunities for host shifts. Understanding the factors influencing fungal-plant interaction and host breadth of pathogenic fungi could help identify emerging threats, prevent spillover onto naïve plants, and reduce the risk of further host range expansion.