Short‐range clinal variation in the prevalence of a sexually transmitted fungus associated with urbanisation

Sexually transmitted pathogens and parasites have attracted much recent attention by virtue of differences in epidemiology and biology from classical pathogens and parasites (Getz & Pickering, 1983; Anderson & May, 1991; Lockhart et al., 1996). Epidemiologically, the rate of transmission of a sexually transmitted parasite is likely to be less dependent on host density than for ordinary infectious diseases, copulation frequency being generally less affected by density than by gross contact rate (Anderson & May, 1991). While work on the dynamics of sexually transmitted diseases in mammals, especially humans, has been intense (Anderson & May, 1991), study of these diseases in insects is rare. Where studies have been carried out, they have gone little beyond the observation that certain parasites and pathogens of insects are sexually transmitted, with some note of their virulence but little or no information about the dynamics of infection (e.g. Hurst et al., 1995). This is unfortunate, as the dynamics of these diseases in insects are likely to differ from those of their better understood mammalian analogues because of the short lifespan of most adult insects and the voltinism of many insect populations. Study of the factors affecting the dynamics, and therefore prevalence and incidence, of sexually transmitted disease in insects is therefore timely. One interaction that bears inspection is that between Laboulbeniales fungi and their hosts. The Laboulbeniales is a group of Ascomycete fungi where species grow on the cuticle of their host, are generally specialised on one or two host species, and cause little pathology beyond increased melanisation of the cuticle around the point of infection (Weir & Beakes, 1995). They are frequently, but not exclusively, transmitted during sexual contact (Benjamin & Shalor, 1952; Whisler, 1968; Strandberg & Tucker, 1974; De Kesel, 1995). The interaction between a coccinellid beetle, Adalia bipunctata, and the laboubenialian fungus Hesperomyces virescens presents a potentially useful case study for aiding understanding of disease dynamics, where incidence appears to vary over fairly short distances. The fungus was originally described on A. bipunctata in the London area (Weir & Beakes, 1996) but earlier examination of the host outside London failed to reveal the presence of infection (G. D. D. Hurst, pers. obs.), suggesting an effect of urbanisation on disease incidence and dynamics. The work reported here had two objectives: (1) To examine whether transmission during host copulation is important for this parasite. This was attained by testing whether males were more likely to be infected on their ventral surface and females on their dorsum, paralleling the position of the sexes during copulation, and echoing observations of other sexually transmitted fungi (Benjamin & Shalor, 1952; Whisler, 1968; De Kesel, 1995). (2) To quantify systematically the extent of variation in prevalence over space, the extent to which this variation altered with time, and the potential role of variation in host phenology in producing the observed changes. Extreme variation in prevalence over a remarkably short distance was observed, with high prevalence in urban areas of London but absence outside these areas. The possible causes of this shortrange variation in prevalence in terms of the effect of urbanisation on host phenology are discussed.