Male and female Silene latifolia plants differ in per-contact risk of infection by a sexually transmitted disease

1. Behavioural, physiological or immunological constraints often render one sex more susceptible to parasites, thereby potentially generating sex-specific trade-offs between traits associated with infection risk and other life-history characters. 2. The fungal pathogen Microbotryum violaceum systemically infects the dioecious plant Silene latifolia when pollinators deposit fungal spores on the flowers of healthy plants. Male plants produce many short-lived flowers, whereas females produce few flowers that remain connected with the plant after fertilization. We investigated how variation in flower production and flower longevity affects the infection risk for males and females. 3. In glasshouse experiments, we varied the number of flowers inoculated (4 vs. 16 per plant) with spores and the time until these flowers were removed (1 or 2 days for both sexes, 14 days for females only). We also measured the longevity of male flowers receiving simulated visits, with or without spores, to test for an abscission response to visitation and/or contamination. In a field survey, we measured male and female disease prevalence in 17 natural populations. 4. Varying the number of inoculated flowers did not affect infection probability, but females retaining inoculated flowers for 14 days became diseased more often (20.0%) than did plants with flowers removed within 2 days (7.3%). 5. Males that had dropped more inoculated flowers prematurely were more likely to remain uninfected. Spore-bearing visits shortened male flower longevity (38.4 +/- 2.8 h) relative to non-spore visits (47.9 +/- 5.2 h). 6. Female field disease prevalence (19.7 +/- 3.5%) was higher than that of males (14.3 +/- 2.6%), especially in populations with a high disease incidence. 7. Continuing physical connection during fruit ripening appears to increase invasion time and thus the per-contact infection risk in females. This is consistent with higher female field prevalences, although other explanations, unrelated to disease transmission, are possible. These results illustrate how interactions between plant reproductive behaviour and pollinator activity may affect disease spread. Female mating behaviour may evolve towards lower attractiveness to pollinators to minimize infectious contacts, while males can afford to be more promiscuous with an attractive, but disposable, floral display.