1. Evolution of fungicide resistance in agricultural and natural ecosystems is associated with the biology of pathogens, the chemical property and application strategies of the fungicides. The influence of ecological factors such as host diversity on the evolution of fungicide resistance has been largely overlooked but is highly relevant to social and natural sustainability. In this study, we used an experimental evolution approach to understand how host population heterogeneity may affect the evolution of fungicide resistance in the associated pathogens.

2. Potato populations with six levels of genetic heterogeneity were grown in the same field and naturally infected by Phytophthora infestans. Pathogen isolates (~1200) recovered from the field experiment were molecularly genotyped. Genetically distinct isolates were selected form each population and 142 isolates were assayed for their tolerance to two fungicides differing in the mode of action. Tolerance was determined by calculating the relative growth rate of the isolates in the presence and absence of fungicides and the effective concentration for 50% inhibition.

3. The evolution of fungicide resistance in P. infestans was affected by the genetic variation of host populations. Higher potato diversification increased the sensitivity of P. infestans to both fungicides and reduced genetic variation of the pathogen available for the development of fungicide resistance. These mitigating effects are independent of biochemical properties of fungicides and are likely caused by host selection for pathogen strains differing in the ability of fungicide influxes, effluxes or detoxification rather than mutations in fungicide target genes.

4. Synthesis and applications: Increased fungicide sensitivity and diminished evolutionary potential of fungicide resistance associated with higher host diversification reduce the fungicide dose and application frequency needed to achieve the same extent of disease control, relaxing the selection pressure acting on the pathogen populations and retarding the evolution of fungicide resistance. Together with benefits documented in other studies, our results indicate that host diversification is an eco-friendly approach that not only ameliorate fungicide resistance but also help achieve social and ecological sustainability by balancing the interaction among food security, socioeconomic development and ecological resilience.

See details in the materials and methods of the paper.