Trade-off between intra- and interannual scales in the evolution of aggressiveness in a local plant pathogen population

The efficiency of plant resistance to a fungal pathogen population is expected to decrease over time, due to the selection of virulent or highly aggressive strains. This dynamics may differ depending on the scale investigated (annual or pluriannual), particularly for annual crop pathogens with both sexual and asexual reproduction cycles. We assessed this time-scale effect, by comparing aggressiveness changes in a local Zymoseptoria tritici population over an eight-month cropping season and a six-year period of wheat monoculture. We collected two pairs of subpopulations to represent the annual and pluriannual scales: collected from leaf lesions at the beginning and end of a single annual epidemic (annual), and collected from crop debris at the beginning and end of a six-year period (pluriannual). We assessed two aggressiveness traits – latent period and lesion size – on sympatric and allopatric host varieties. Average aggressiveness increased during the course of the annual epidemic, but not over the six-year period. Furthermore, a significant cultivar effect (sympatric vs. allopatric) on the average aggressiveness of the isolates revealed host (mal)adaptation, suggesting that the observed patterns resulted from selection. We thus provide experimental evidence of a trade-off between the intraand interannual scales in the evolution of aggressiveness in a local plant pathogen population. More aggressive isolates were collected from upper leaves, on which disease severity is usually lower than on the lower part of the plants then left in the field as crop debris after harvest. We suggest that these isolates play little role in sexual reproduction, due to an Allee effect (difficulty finding mates at low pathogen densities), particularly as the upper parts of the plant are removed from the field, explaining the lack of transmission of increases in aggressiveness between epidemics.