It is often assumed that host specialization is promoted by trade-offs in the performance of parasites on different host species, but experimental evidence for such trade-offs is scant. We studied differences in performance among strains of the anther smut fungus Ustilago violacea from two closely related host plant species, Silene alba and S. dioica, on progeny of (1) the host species from which they originated, (2) the alternative host species, and (3) inter-specific hybrids. Significant intra-specific variation in the pathogen was found for both infection success on a range of host genotypes (virulence) and components of spore production per infected host (aggressiveness) (sensu Burdon 1987). Strains did not have overall higher virulence on conspecifics of their host of origin than on strains from the heterospecific host, but they did have a significantly (c. 3 times) higher spore production per infected male host. This finding suggests that host adaptation may have evolved with respect to aggressiveness rather than virulence. The higher aggressiveness of strains on conspecifics of their host of origin resulted both from higher spore production per infected flower (spores are produced in the anthers), and greater ability to stimulate flower production on infected hosts. The latter indicates the presence of adaptive intraspecific variation in the ability of host manipulation. As transmission of the fungus is mediated by insects that are both pollinators of the host and vectors of the disease, we also assessed the effect of strains on host floral traits. Infection resulted in a reduction of inflorescence height, flower size, and nectar production per flower. Strains did not differ in their effect on nectar production, but infection with strains from S. alba resulted in a stronger reduction of inflorescence height and petal size on both host species. Vectors may therefore in principle discriminate among hosts infected by different strains and affect their efficiency of transmission. Contrary to assumptions of recent hypotheses about the role of host hybrids in the evolution of parasites, hybrids were not generally more susceptible than parental hosts. It is therefore unlikely that the rate of evolution of the pathogen on the parental species is slowed down by selection for specialization on the hybrids.

An important mechanism in stabilizing tightly linked host-parasitoid and prey-predator interactions is the presence of refuges that protect organisms from their natural enemies. However, the presence and quality of refuges can be strongly affected by the environment. We show that infection of the host plant Silene latifolia by its specialist fungal plant pathogen Microbotryum violaceum dramatically alters the enemy-free space of a herbivore, the specialist noctuid seed predator Hadena bicruris, on their shared host plant. The pathogen arrests the development of seed capsules that serve as refuges for the herbivore's offspring against the specialist parasitoid Microplitis tristis, a major source of mortality of H. bicruris in the field. Pathogen infection resulted both in lower host-plant food quality, causing reduced adult emergence, and in twofold higher rates of parasitism of the herbivore. We interpret the strong oviposition preference of H. bicruris for uninfected plants in the field as an adaptive response, positioning offspring on refuge-rich, high-quality hosts. To our knowledge, this is the first demonstration that plant-inhabiting micro-organisms can affect higher trophic interactions through alteration of host refuge quality. We speculate that such interference can potentially destabilize tightly linked multitrophic interactions.

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Summary• In nursery pollination systems, pollinator offspring usually feed on pollinated fruits or seeds. Costs and benefits of the interaction for plant and pollinator, and hence its local outcome (antagonism-mutualism), can be affected by the presence of 'thirdparty' species. Infection of Silene latifolia plants by the fungus Microbotryum violaceum halts the development of fruits that provide shelter and food for larvae of the pollinating moth Hadena bicruris. We investigated whether the moth secures its benefit by selective oviposition on uninfected flowers.• Oviposition was recorded in eight natural populations as a function of plant infection status, local neighbourhood, plant and flower characteristics.• Oviposition was six times lower on flowers from infected than on those from uninfected plants. Oviposition decreased with decreasing flower and ovary size. Moths could use the latter to discriminate against diseased flowers.• Although moths show an adaptive oviposition response, they reduce the future potential of healthy hosts because they still visit infected plants for nectar, vectoring the disease, and they reduce any fitness advantage gained by disease-resistant plants through selective predation of those plants.

-Resistance and tolerance are different strategies of plants to deal with herbivore 29 attack. Since resources are limited and resistance and tolerance serve similar functions for plants, 30 trade-offs between these two strategies have often been postulated. In this study we investigated 31 trade-offs between resistance and one aspect of tolerance, the ability to regrow after defoliation. 32In order to minimize confounding effects of genetic background and selection history, we used 33 offspring derived from artificial selection lines of ribwort plantain (Plantago lanceolata) that 34 differed in their levels of leaf iridoid glycosides (IGs), allelochemicals that confer resistance to 35 generalist herbivores, to study genetic associations with regrowth ability. We tested whether 36 high-IG plants 1) suffer allocation costs of resistance in terms of reduced shoot and root growth, 372) have reduced regrowth ability (tolerance) after defoliation compared to low-IG plants, and 3) 38 whether such costs are more pronounced under nutrient stress. High-IG plants produced fewer 39 inflorescences and side rosettes than low-IG plants and showed a different biomass allocation 40 pattern, but since neither the vegetative, nor the reproductive biomass differed between the lines, 41 there was no evidence for a cost of IG production in terms of total biomass production under 42 either nutrient condition. High-IG plants also did not suffer a reduced capacity to regrow shoot 43 mass after defoliation. However, after regrowth, root mass of high-IG plants grown under 44 nutrient-poor conditions was significantly lower than that of low-IG plants. This suggests that 45 under these conditions shoot regrowth of high-IG plants comes at a larger expense of root growth 46 than in low-IG plants. We speculate therefore that if there is repeated defoliation, high-IG plants 47 may eventually fail to maintain shoot regrowth capacity and that trade-offs between resistance 48 and tolerance in this system will show up after repeated defoliation events under conditions of 49 low resource availability.