ANTHER SMUT DISEASE IN DIANTHUS SILVESTER (CARYOPHYLLACEAE): NATURAL SELECTION ON FLORAL TRAITS.

Mating opportunities, pollination intensity, and pollen dispersal ability may vary with variation in floral traits such as color, size, and shape. Where these traits are selected by pollinators for enhanced elaboration, they should evolve toward the equilibrium between selection for further elaboration and selection against this through reduced fecundity or vitality. Here we show that pollinator-borne fungal diseases of plants may be a factor influencing the position of this equilibrium. Populations of the rock pink, Dianthus silvester often contain individuals infected with the anther smut fungus Microbotryum violaceum (= Ustilago violacea). In a naturally infected population in the Alps of eastern Switzerland we investigated how intrapopulation variation in flower size and nectar rewards influenced spore deposition and how floral traits varied with disease status. We found that spore deposition increased with increasing petal size, suggesting that large-flowered plants were at a greater risk of disease. Spore deposition was also higher for plants growing in patches with many or a high proportion of diseased neighbors. Multiple regression analyses showed that petal size or nectar reward influenced spore deposition when the effects of neighborhood disease abundance were controlled statistically. In sequential analyses, after removing the effects of disease density or frequency and plant gender, petal length explained significant variation in spore deposition. Diseased plants had reduced female reproductive organs, but calyx size was intermediate between that of healthy perfect and female flowers of this gynodioecious-gynomonoecious species, and diseased plants bore flowers with the largest petals. This may reflect a symptom of this disease or the cause, if larger-flowered plants are more likely to become infected. We conclude that investment to pollinator attraction may bring an enhanced risk of contracting this sterilizing pollinator-borne disease, so natural selection by the fungus M. violaceum acts to lower attractiveness to pollinators.