In many organisms, males and females differ in one or other of development, morphology, physiology, life history and behaviour. Such sexual dimorphism is often considered to be the direct or indirect result of intra- and intersexual selection (Darwin 1871; Andersson 1994; Short & Balaban 1994) for traits that maximize the acquisition of mates or mating opportunities.
However, complications may arise if sexual selection produces conflicts with other aspects of the life history of an organism, particularly if such conflicts are different for males and females. Constraints or trade-offs may explain the sexual dimorphism in disease susceptibility that is found in certain host–parasite systems in vertebrates (Poulin 1996; Schalk & Forbes 1997; Møller et al. 1998) and invertebrates (Wedekind & Jakobsen 1998). In vertebrates, susceptibility to parasites may be higher in males due to the presence of secondary sexual characteristics associated with negative effects on the immune system, produced as a result of stronger sexual selection on males (Alexander & Stimson 1988; Zuk 1990; Folstad & Karter 1992; Zuk & McKean 1996). However, susceptibility bias is not always the result of an impaired immune system, and not always towards males. In humans, for example, women may become infected with sexually transmitted diseases more easily than men because of the retention of the ejaculate in their reproductive organs (Hook & Handsfield 1990; Ewald 1994). Furthermore, differences between the sexes in their behaviour or ecology may lead to higher parasite encounter, and thus higher infection rates, of one or other sex (Bundy 1988; Zuk & McKean 1996; Schalk & Forbes 1997).
In both animals and plants, sexual dimorphism in susceptibility to disease may influence epidemiology as well as the evolutionary trajectories of traits involved in sexual selection and/or host–parasite interactions. Recent theoretical work has suggested that optimal mating strategies in the presence of sexually transmitted disease may not necessarily be those which minimize the risk of infection and disease spread in a population (Guldbrandtsen 1997; Thrall et al. 1997). Although monogamy may reduce infection risk (Loehle 1995), limited promiscuity can generate similar or even higher reproductive success, despite the higher chance of becoming infected (Thrall et al. 1997). Moreover, if males and females differ in their probabilities of encountering disease and becoming infected thereafter, varying constraints and trade-offs between selection for minimizing disease risk and selection for maximizing reproductive success may lead to different optimal mating strategies in the two sexes.
We investigated differences in infection probability for males and females of the dioecious plant Silene latifolia (Caryophyllaceae) to the anther-smut disease, Microbotryum violaceum. This fungal pathogen sporulates in the flowers of infected hosts, thereby sterilizing the host, and is mainly transmitted by pollinating insects (Roche et al. 1995), thus having the features of a sexually transmitted disease (Alexander & Antonovics 1988; Thrall et al. 1993; Lockheart et al. 1996).
Sexual activity, i.e. flowering behaviour, influences the probability of disease contact and subsequent infection in S. latifolia. Plants producing more flowers, flowering earlier or longer in the season (Alexander & Antonovics 1988; Alexander 1989; Thrall & Jarosz 1994b; Biere & Antonovics 1996; Biere & Honders 1996b), or presenting more receptive surface (Elmqvist et al. 1993) are more likely to become infected, partly because some of these traits are negatively correlated with biochemical resistance (Biere & Antonovics 1996), but also because such plants receive more visits (Shykoff & Bucheli 1995) and thus become contaminated with fungal spores more often. Hence, evolution of floral traits and breeding systems in such cases may be determined by the interaction with this pathogen as well as by sexual selection (Elmqvist et al. 1993; Skogsmyr 1993; Thrall et al. 1993; Meagher 1994; Shykoff et al. 1997).
Because male plants of S. latifolia produce more flowers (e.g. Gross & Soule 1981; Delph & Meagher 1995; Carroll & Delph 1996) with more nectar sugar (Shykoff & Bucheli 1995; Shykoff & Kaltz 1998; but see Biere & Honders 1996a) and receive more pollinator visits than do females (Shykoff & Bucheli 1995; Altizer et al. 1998), exposure, and hence infection, is likely to be more frequent in males than in females. Indeed, male-biased infection rates have been documented (Alexander 1989; Thrall & Jarosz 1994b; Alexander & Antonovics 1995; Biere & Antonovics 1996; Biere & Honders 1998), but are not universal. Sometimes there is no sex difference in disease prevalence (Zillig 1921; Alexander 1990; Thrall & Jarosz 1994b), and a recent survey across several natural populations of S. latifolia and its close relative S. dioica even found, on average, higher disease prevalence in females (Shykoff et al. 1996; see also Lee 1981; Alexander & Antonovics 1988; Alexander 1989). This may result from a higher per-contact infection risk (Alexander 1989; Shykoff et al. 1996) because females retain physical connections with fertilized flowers during fruit development, whereas male flowers drop within a short time. Thus fungal spores deposited on female flowers may have more time to initiate an infection than spores deposited on male flowers.
We tested the effects of frequency of infectious contacts and per-contact infection risk on infection rates in males and females in two glasshouse experiments. In the first, we inoculated a variable number of flowers, which were removed from the plant after a range of times. In the second, we measured flower longevity following artificial visits that did or did not deposit fungal spores, to test whether males potentially reduce the per-contact infection risk by dropping visited and/or contaminated flowers. In addition, we measured disease prevalence of males and females in 17 natural populations of S. latifolia.