And the nasty ones lose in the end: foliar pathogenicity trades off with asexual transmission in the Irish famine pathogen Phytophthora infestans.

A trade-off between pathogenicity and transmission is often postulated to explain the persistence of pathogens over time. If demonstrated, it would help to predict the evolution of pathogenicity across cropping seasons, and to develop sustainable control strategies from this prediction. Unfortunately, experimental demonstration of such trade-offs in agricultural plant pathogens remains elusive. We measured asexual transmission of Phytophthora infestans isolates differing in pathogenicity in two sets of artificial infection experiments under controlled, semi-outdoor conditions. Higher foliar pathogenicity decreased mean daughter tuber weight, increased infection severity in daughter tubers, and increased stem mortality before emergence. The most pathogenic isolates thus suffer a double penalty for asexual transmission: a lower survival probability within small and severely infected tubers; and a lower infection probability of neighbouring healthy plants due to fewer infected stems produced by surviving tubers. Moderate tuber resistance favoured transmission of the least pathogenic isolates, while high levels of resistance almost abolished transmission of all isolates. These data demonstrate a trade-off between foliar pathogenicity and asexual transmission over seasons in P. infestans, which should stabilise pathogenicity over time in the potato late blight pathosystem and possibly favour clone replacement by less pathogenic lineages after demographic bottlenecks.

Long-distance gene flow outweighs a century of local selection and prevents local adaptation in the Irish famine pathogen Phytophthora infestans.

Sustainably managing plant resistance to epidemic pathogens implies controlling the genetic and demographic changes in pathogen populations faced with resistant hosts. Resistance management thus depends upon the dynamics of local adaptation, mainly driven by the balance between selection and gene flow. This dynamics is best investigated with populations from locally dominant hosts in islands with long histories of local selection. We used the unique case of the potato late blight pathosystem on Jersey, where a monoculture of potato cultivar 'Jersey Royal' has been in place for over a century. We also sampled populations from the coasts of Brittany and Normandy, as likely sources for gene flow. The isolation by distance pattern and the absence of genetic differentiation between Jersey and the closest French sites revealed gene flow at that spatial scale. Microsatellite allele frequencies revealed no evidence of recombination in the populations, but admixture of two genotypic clusters. No local adaptation in Jersey was detected from pathogenicity tests on Jersey Royal and on French cultivars. These data suggest that long-distance gene flow (∼ 50/100 km) prevents local adaptation in Jersey despite a century of local selection by a single host cultivar and emphasize the need for regional rather than local management of resistance gene deployment.