Evolutionary divergence in sympatric populations of the fungal pathogen Alternaria alternata across wild tomato hosts

Abstract

Alternaria alternata is a globally distributed fungal pathogen with a broad host range, increasingly affecting both tomato crops and wild tomato relatives. The genomic basis of this ecological breadth in A. alternata remains poorly understood. Here we leverage the opportunity of wild pathosystems to study pathogen evolution and diversity beyond agricultural settings. We sampled isolates from wild tomato species across a 2,500 km range in South America, producing highly contiguous genomes, to investigate population structure. Our comparative genomics analyses reveal that A. alternata sensu stricto consists of two divergent clades. Strikingly, this divergence is not linked to host species, geography, or habitat type. Transposable elements contribute to variation within clades but do not explain their separation. Although some signs of recombination are present, reproductive mode appears stable across clades. Notably, global reference isolates cluster with one clade, while the other, more diverse clade is only found in wild populations. We hypothesize that these wild populations may act as reservoirs of evolutionary potential. These findings challenge prevailing assumptions about the population structure of necrotrophic pathogens and raise new questions about how genetic divergence can persist without ecological or geographic isolation. Media summary (lay abstract)The fungus Alternaria alternata is an emerging threat on tomato and potato crops. In a previous study, we found that it also infects wild tomato plants over a large range in Chile and Peru. Here we sequenced and compared full genomes of the fungi. Surprisingly, they formed two distinct groups that do not reflect different host plant species, geographical locations, or environments. One of those groups is related more closely to global reference samples, while the other group is more diverse. This suggests wild plants may quietly harbour forms of the fungus that could affect crops in the future.