The coexistence of generalist and specialist clonal lineages in natural populations of the Irish Famine pathogen Phytophthora infestans explains local adaptation to potato and tomato

Phytophthora infestans, causing late blight on Solanaceae, is a serious threat to potato and tomato crops worldwide. P.infestans populations sampled on either potato or tomato differ in genotypes and pathogenicity, suggesting niche exclusion in the field. We hypothesized that such niche separation can reflect differential host exploitation by different P.infestans genotypes. We thus compared genotypes and phenotypes in 21 isolates sampled on potato (n=11) or tomato (n=10). Typing at 12 microsatellite loci assigned potato isolates to the 13_A2, 6_A1 and 1_A1 lineages, and tomato isolates to the 23_A1, 2_A1 and unclassified multilocus genotypes. Cross-inoculations on potato and tomato leaflets showed that all isolates were pathogenic on both hosts. However, tomato isolates performed much better on tomato than did potato isolates, which performed better on potato than did tomato isolates, thus revealing a clear pattern of local adaptation. Potato isolates were significantly fitter on potato than on tomato, and are best described as potato specialists; tomato isolates appear to be generalists, with similar pathogenicity on both hosts. Niche separation in the field may thus result mainly from the large fitness gap on tomato between generalists and unadapted potato specialists, while the small, but significant fitness difference on potato between both types of isolates may prevent population invasion by generalists. Extreme specialization to potato seems very costly relative to performance loss on the alternative host. This study therefore shows that local adaptation and niche separation, commonly expected to involve and generate specialists, can occur with generalists.