Long-distance gene flow and recombination shape the evolutionary history of a maize pathogen

The evolutionary history of crop pathogens is shaped by a complex interaction of natural and anthropogenic factors. The fungus Colletotrichum graminicola causes maize anthracnose which results in significant yield losses worldwide. We conducted a comprehensive investigation into the evolutionary genomics of C. graminicola using a collection of 212 isolates from 17 countries across five continents. Genomic analyses supported the existence of three geographically isolated genetic lineages, with a significant pattern of isolation by distance. We identified two distinct gene flow patterns, driven by short- and long-distance dispersal, likely resulting from the natural spread of the pathogen and the exchange of contaminated seeds. We present evidence of genetic introgression between lineages, suggesting a long history of recombination. We identified significant recombination events coalescing at distinct points in time, with the North American lineage displaying evidence of the most ancient recombination. Demographic modelling has indicated that North America is an intermediate between Brazil, Europe and an ancestral, unsampled source population, which is hypothesised to be Mesoamerican. Our analyses revealed that the global genomic structure of C. graminicola is shaped by geographic differentiation driven by long-distance migration and a long history of recombination and introgression. We show historical relationships amongst these lineages, identifying a potential route for fungal spread, with the North American population emerging ancestrally, followed sequentially by the Brazilian and European populations. Our research indicates that the European lineage is more virulent, which has implications for the potential emergence of new outbreaks of maize anthracnose in Europe.