Population genomic footprints of host adaptation, introgression and recombination in Coffee Leaf Rust

Coffee Leaf Rust, caused by Hemileia vastatrix (Hv), represents the biggest threatto coffee production worldwide and ranks amongst the most serious fungal diseasesin history. Despite a recent series of outbreaks and emergence of hyper-virulentstrains, the population evolutionary history and potential of this pathogen remainspoorly understood. To address this issue, we used RADseq to generate 19 000SNPs across a worldwide collection of 37 Hv samples. Contrarily to the longstandingidea that Hv represents a genetically unstructured and cosmopolitan species, ourresults reveal the existence of a cryptic species complex with marked host tropism.Using phylogenetic and pathological data, we show that one of these lineages (C3)infects almost exclusively the most economically valuable coffee species (tetraploidsthat include Coffea arabica and inter-specific hybrids) while the other lineages (C1-C2) are severely maladapted to these hosts but successfully infect diploid coffeespecies. Population dynamic analyses suggest that the C3 group may be a recent“domesticated” lineage that emerged via host-shift from diploid coffee hosts. We alsofound evidence of recombination occurring within this group, which could explainthe high pace of pathotype emergence despite the low genetic variation. Moreover,genomic footprints of introgression between the C3 and C2 groups were discoveredand raise the possibility that virulence factors may be quickly exchanged betweengroups with different pathogenic abilities. This work advances our understanding onthe evolutionary strategies used by plant pathogens in agro-ecosystems with directand far-reaching implications for disease control.