Local maladaptation in the anther-smut fungus Microbotryum violaceum to its host plant Silene latifolia: Evidence from a cross-inoculation experiment

Conventional wisdom holds that parasites evolve more rapidly than their hos ts and are therefore locally adapted, that is, better at exploiting sympatr ic than allopatric hosts. We studied local adaptation in the insect-transmi tted fungal pathogen Microbotryum violaceum and its host plant Silene latif olia. Infection success was tested in sympatric (local) and allopatric (for eign) combinations of pathogen and host from 14 natural populations from a metapopulation. Seedlings from, up to 10 seed families from each population were exposed to sporidial suspensions from each of four fungal strains der ived from the same population, from a near-by population (< 10 km distance) , and from two populations at an intermediate (< 30 km) and remote (< 170 k m) distance, respectively. We obtained significant pathogen X plant interac tions in infection success (proportion of diseased plants) at both fungal p opulation and strain level. There was an overall pattern of local maladapta tion of this pathogen: average fungal infection success was significantly l ower on sympatric hosts (mean proportion of diseased plants = 0.32 +/- 0.03 SE) than on allopatric hosts (0.40 +/- 0.02). Five of the 14 fungal popula tions showed no strong reduction in infection success on sympatric hosts, a nd three even tended to perform better on sympatric hosts. This pattern is consistent with models of time-lagged cycles predicting patterns of local a daptation in host-parasite systems to emerge only on average. Several facto rs may restrict the evolutionary potential of this pathogen relative to tha t of its host. First, a predominantly selfing breeding system may limit its ability to generate new virulence types by sexual recombination, whereas t he obligately outcrossing host S. latifolia may profit from rearrangement o f resistance alleles by random mating. Second, populations often harbor onl y a few infected individuals, so virulence variation may be further reduced by drift. Third, migration rates among host plant populations are much hig her than among pathogen populations, possibly because pollinators prefer he althy over diseased plants. Migration among partly isolated populations may therefore introduce novel host plant resistance variants more often than n ovel parasite virulence variants. That migration contributes to the coevolu tionary dynamics in this system is supported by the geographic pattern of i nfectivity. Infection success increased over the first 10-km range of host- pathogen population distances, which is likely the natural range of gene ex change.