We investigated genetic diversity in West European populations of the fungal pathogen Microbotryum violaceum in sympatric, parapatric and allopatric populations of the host species Silene latifolia and S. dioica, using four polymorphic microsatellite loci. In allopatric host populations, the fungus was highly differentiated by host species, exhibiting high values of FST and RST, and revealed clear and distinct host races. In sympatric and parapatric populations we found significant population differentiation as well, except for one sympatric population in which the two host species grew truly intermingled. The mean number of alleles per locus for isolates from each of the host species was significantly higher in sympatric/parapatric than in allopatric populations. This suggests that either gene flow between host races in sympatry, or in case of less neutral loci, selection in a more heterogeneous host environment can increase the level of genetic variation in each of the demes. The observed pattern of host‐related genetic differentiation among these geographically spread populations suggest a long‐term divergence between these host races. In sympatric host populations, both host races presumably come in secondary contact, and host‐specific alleles are exchanged depending on the amount of fungal gene flow.

Host fidelity can play an important role in sympatric host race formation of phytophagous insects by providing a mechanism for prezygotic reproductive isolation. Similarly, but less recognized, host fidelity of insects could provide a mechanism for maintaining host-specific differentiation among insect-vectored pathogens. We studied the transfer of fluorescent dye-mimicking spores of the pollinator-transmitted anther smut fungus Microbotryum violaceum in experimental plots of two of its closely related hosts, Silene dioica and Silene latifolia. Mean rates of diurnal interspecific transfer were 26% from S. latifolia to S. dioica and 34% in the reverse direction, suggesting that host fidelity of pollinators per se cannot account for the maintenance of genetically differentiated host races of this fungus observed in sympatry. In a large natural sympatric population of the two hosts, S. dioica flowers experienced a sixfold higher probability of receiving spores from conspecifics than from heterospecifics during the time frame of susceptibility to successful systemic infection due to their earlier onset of flowering. Also, spores from heterospecifics were an order of magnitude farther away than spores from conspecifics. We therefore speculate that the observed sympatric host-specific differentiation is due to a combination of factors, including vector behavior and host spatial and temporal structure.

We studied intraspecific competition and assortative mating between strains of the anther smut fungus Microbotryum violaceum from two of its host species, Silene latifolia and S. dioica. Specifically, we investigated whether strains from allopatric host populations have higher competitive ability on their native host species and show positive assortative mating. In general, strains isolated from S. latifolia outcompeted strains isolated from S. dioica on both host species, but in female hosts, heterotypic dikaryons (i.e., dikaryons composed of a haploid strain originating from S. latifolia and a haploid strain originating from S. dioica) were most successful in competition. Furthermore, the latency period was significantly shorter for heterokaryons that contained at least one strain originating from S. latifolia, compared to heterokaryons that only contained strains originating from S. dioica. The frequencies of conjugations between strains originating from S. latifolia were much higher than conjugation frequencies between strains originating from S. dioica. A significant positive correlation was detected between the relative success of strains in competition and in conjugation, suggesting that success of a strain in competition might be partly determined by its swiftness of mating. In addition, reciprocal differences within heterotypic crosses revealed a significant effect of fungal mating type, with mating type a1 being the main determinant of mating pace. The observed differences in infection success, conjugation rate, and latency period in favor of strains from S. latifolia relative to strains from S. dioica on both host species are discussed in an evolutionary context of opportunities for the maintenance of differentiation between different formae speciales upon secondary contact.

Abstract. We studied intraspecific competition and assortative mating between strains of the anther smut fungus Microbotryum violaceum from two of its host species, Silene latifolia and S. dioica. Specifically, we investigated whether strains from allopatric host populations have higher competitive ability on their native host species and show positive assortative mating. In general, strains isolated from S. latifolia outcompeted strains isolated from S. dioica on both host species, but in female hosts, heterotypic dikaryons (i.e., dikaryons composed of a haploid strain originating from S. latifolia and a haploid strain originating from S. dioica) were most successful in competition. Furthermore, the latency period was significantly shorter for heterokaryons that contained at least one strain originating from S. latifolia, compared to heterokaryons that only contained strains originating from S. dioica. The frequencies of conjugations between strains originating from S. latifolia were much higher than conjugation frequencies between strains originating from S. dioica. A significant positive correlation was detected between the relative success of strains in competition and in conjugation, suggesting that success of a strain in competition might be partly determined by its swiftness of mating. In addition, reciprocal differences within heterotypic crosses revealed a significant effect of fungal mating type, with mating type a 1 being the main determinant of mating pace. The observed differences in infection success, conjugation rate, and latency period in favor of strains from S. latifolia relative to strains from S. dioica on both host species are discussed in an evolutionary context of opportunities for the maintenance of differentiation between different formae speciales upon secondary contact.Key words. Competition success, conjugation, formae speciales, mating success, mating type, smut fungus.Received December 19, 2001. Accepted December 26, 2002 Plant parasites are often capable of infecting more than one host species and show intraspecific variation in host use. Understanding the origin and maintenance of such variation and the conditions under which this may lead to host race formation and speciation are central questions in evolutionary biology. Differences in performance of pathogens on different host species and positive assortative mating are expected to play an active role in processes of divergence between strains or in the maintenance of host related differentiation.