Sexual reproduction facilitates the adaptation of parasites to antagonistic host environments: Evidence from empirical study in the wheat-Mycosphaerella graminicola system

Most eukaryotes use sexual reproduction to transmit genetic information from generation to generation despite the advantages offered by asexual reproduction. One theory to explain the origin and maintenance of sexual reproduction hypothesises that sexual recombination generates genetic variation that allows faster adaptation to fluctuating and/or stressful environments. We used a combination of ecological, molecular genetic, statistical and experimental evolution approaches to test this hypothesis in an agricultural plant-pathogen system. We inoculated wheat hosts with 10 strains of the fungal pathogen Mycosphaerella graminicola in a field experiment and estimated the contributions of sexual reproduction, asexual reproduction and immigration to the genetic composition of fungal populations sampled from moderately resistant and susceptible hosts through the course of an epidemic cycle. We found that a significant proportion of the M. graminicola population in the late phase of the epidemic originated from sexual reproduction among isolates that had been introduced into the field plots at the beginning of the epidemic. Recombinants were recovered at a higher frequency on the moderately resistant plant host Madsen than on the susceptible host Stephens. By the end of the growing season, we estimated that ∼13% of the strains sampled from the resistant host were recombinants, compared with 9% in the samples collected from the susceptible host. We also found that pathogen strains originating from the resistant cultivar displayed higher levels of fitness, virulence and fungicide tolerance than those originating from the susceptible cultivar. Our results provide empirical support for the hypothesis that sexual reproduction facilitates the evolution of parasites to overcome host resistance.