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

Coffee Leaf Rust, caused by Hemileia vastatrix (Hv), represents the biggest threat to coffee production worldwide and ranks amongst the most serious fungal diseases in history. Despite a recent series of outbreaks and emergence of hyper-virulent strains, the population evolutionary history and potential of this pathogen remains poorly understood. To address this issue, we used RADseq to generate ~19,000 SNPs across a worldwide collection of 37 Hv samples. Contrarily to the longstanding idea that Hv represents a genetically unstructured and cosmopolitan species, our results 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 (Coffea arabica and tetraploid hybrids) while the other lineages (C1-C2) are severely maladapted to these hosts but successfully infect diploid coffee species. Population dynamic analyses suggest that the C3 group may be a recent “domesticated” lineage that emerged via host-shift from diploid coffee hosts. We also found evidence of recombination occurring within this group, which could explain the high pace of pathotype emergence in face the observed decline of genetic variation. Moreover, genomic footprints of introgression between the C3 and C2 groups were discovered and raise the possibility that virulence factors may be quickly exchanged between groups with different pathogenic abilities. This work advances our understanding on the evolutionary strategies used by plant pathogens in agro-ecosystems with direct and far-reaching implications for disease control.