Novel insights on colonization routes and evolutionary potential of Colletotrichum kahawae, a severe pathogen of Coffea arabica

Pathogenic fungi are emerging at an increasing rate on a wide range of host plants, leading to tremendous threats to global economy and food safety. Several plant pathogens have been considered invasive species, rendering large-scale population genomic analyses crucial to better understand their demographic history and evolutionary potential. Colletotrichum kahawae (Ck) is a highly aggressive and specialized pathogen, causing Coffee Berry Disease in Arabica coffee in Africa. This pathogen leads to severe production losses and its dissemination out of Africa is greatly feared. To address this issue, a population genomic approach using thousands of SNPs spaced throughout the genome was used to unveil its demographic history and evolutionary potential. The current study supports that Ck is a true clonal pathogen, perfectly adapted to green coffee berries, with three completely differentiated populations (Angola, Cameroon and East African). Two independent clonal lineages were found within Angola as opposed to the remaining single-clonal populations. The most probable colonization scenario suggests that this pathogen has emerged in Angola and immediately dispersed to East Africa, where these two populations began to differentiate, followed by the introduction in Cameroon from an Angola population. However, the differentiation between the two Angola clonal lineages masks the mechanism for the emergence of the Cameroon population. Our results suggest that Ck is completely differentiated from the ancestral lineage, has a low evolutionary potential and dispersion ability, being human transport the mostly likely scenario for its potential dispersion, which makes the fulfilment of the quarantine measures and management practices implemented crucial.