Host adaptation in the anther smut fungus Ustilago violacea (Microbotryum violaceum): infection success, spore production and alteration of floral traits on two host species and their F1-hybrid

Abstract

It is often assumed that host specialization is promoted by trade-offs in the performance of parasites on different host species, but experimental evidence for such trade-offs is scant. We studied differences in performance among strains of the anther smut fungus Ustilago violacea from two closely related host plant species, Silene alba and S. dioica, on progeny of (1) the host species from which they originated, (2) the alternative host species, and (3) inter-specific hybrids. Significant intra-specific variation in the pathogen was found for both infection success on a range of host genotypes (virulence) and components of spore production per infected host (aggressiveness) (sensu Burdon 1987). Strains did not have overall higher virulence on conspecifics of their host of origin than on strains from the heterospecific host, but they did have a significantly (c. 3 times) higher spore production per infected male host. This finding suggests that host adaptation may have evolved with respect to aggressiveness rather than virulence. The higher aggressiveness of strains on conspecifics of their host of origin resulted both from higher spore production per infected flower (spores are produced in the anthers), and greater ability to stimulate flower production on infected hosts. The latter indicates the presence of adaptive intraspecific variation in the ability of host manipulation. As transmission of the fungus is mediated by insects that are both pollinators of the host and vectors of the disease, we also assessed the effect of strains on host floral traits. Infection resulted in a reduction of inflorescence height, flower size, and nectar production per flower. Strains did not differ in their effect on nectar production, but infection with strains from S. alba resulted in a stronger reduction of inflorescence height and petal size on both host species. Vectors may therefore in principle discriminate among hosts infected by different strains and affect their efficiency of transmission. Contrary to assumptions of recent hypotheses about the role of host hybrids in the evolution of parasites, hybrids were not generally more susceptible than parental hosts. It is therefore unlikely that the rate of evolution of the pathogen on the parental species is slowed down by selection for specialization on the hybrids.

Patterns of within population dispersal and mating of the fungus Microbotryum violaceum parasitising the plant Silene latifolia

“…This is in agreement with previous studies showing strong differentiation between host races of M. violaceum, which might be considered as different species (Biere and Honders, 1996;Shykoff et al, 1999;Bucheli et al, 2000). Among amplifiable microsatellites, only 6.7% were polymorphic.…”

“…Each of these cells buds off yeast-like sporidia and new infectious dikaryons are produced by conjugation of two cells of opposite mating types. M. violaceum has been studied as an experimental model species in genetics (reviewed in Garber and Ruddat, 2002), host-race differentiation (eg Biere and Honders, 1996;Shykoff et al, 1999;Bucheli et al, 2000), and sex-ratio distortion (Kaltz and Shykoff, 1997;Oudemans et al, 1998;Hood and Antonovics, 2000;Thomas et al, 2003). M. violaceum has also been the basis for theoretical models on transmission dynamics (eg Thrall et al, 1993;Antonovics et al, 1994Antonovics et al, , 1995Thrall and Antonovics, 1995).…”

Performance of Lychnis Flos-Cuculi From Fragmented Populations Under Experimental Biotic Interactions

“…Moreover, some populations are infected by the anther smut fungus Microbotryum violaceum, which may systemically infect plants and sterilize flowers and thus may have profound effects on plant fitness. The Silene-Microbotryum plant-pathogen system is one of the best studied plant-pathogen systems in natural populations (e.g., Antonovics et al 1994, Alexander and Antonovics 1995, Biere and Honders 1996, Shykoff and Kaltz 1997, Bucheli et al 2001). In the field, larger populations of Silene alba were more likely to be diseased than smaller populations (Antonovics et al 1994), and among our sampling populations we observed a similar trend (Galeuchet 2003).…”

LOCAL MALADAPTATION IN THE ANTHER-SMUT FUNGUSMICROBOTRYUM VIOLACEUMTO ITS HOST PLANTSILENE LATIFOLIA: EVIDENCE FROM A CROSS-INOCULATION EXPERIMENT

“…Under natural conditions, passive transmission of spores by wind or rain and infection of plants at the vegetative stage is a possible, but relatively rare option occurring only over short distances (Roche et al 1995). Inoculation of plants at the seedling or rosette stage has been widely used to investigate variation in resistance or infectivity (e.g., Baird and Garber 1979;Alexander 1989;Biere and Honders 1996;Shykoff and Kaltz 1997), and plant crosses more resistant to artificial inoculation are also more resistant when exposed to spores by insect transmission in the field (Alexander et al 1993).…”