TL;DR: Local adaptation in the insect‐transmitted fungal pathogen Microbotryum violaceum and its host plant Silene latifolia is studied and it is found that migration among partly isolated populations may introduce novel host plant resistance variants more often than novel parasite virulence variants.
Abstract: Conventional wisdom holds that parasites evolve more rapidly than their hosts and are therefore locally adapted, that is, better at exploiting sympatric than allopatric hosts. We studied local adaptation in the insect-transmitted fungal pathogen Microbotryum violaceuin and its host plant Silene latifolia. Infection success was tested in sympatric (local) and allopatric (foreign) combinations of pathogen and host from 14 natural populations from a metapopulation. Seedlings from up to 10 seed families from each population were exposed to sporidial suspensions from each of four fungal strains derived from the same population, from a near-by population (< 10 km distance), and from two populations at an intermediate (< 30 km) and remote (< 170 km) distance, respectively. We obtained significant pathogen X plant interactions in infection success (proportion of diseased plants) at both fungal population and strain level. There was an overall pattern of local maladaptation of this pathogen: average fungal infection success was significantly lower on sympatric hosts (mean proportion of diseased plants = 0.32 + 0.03 SE) than on allopatric hosts (0.40 + 0.02). Five of the 14 fungal populations showed no strong reduction in infection success on sympatric hosts, and three even tended to perform better on sympatric hosts. This pattern is consistent with models of time-lagged cycles predicting patterns of local adaptation in host-parasite systems to emerge only on average. Several factors may restrict the evolutionary potential of this pathogen relative to that of its host. First, a predominantly selfing breeding system may limit its ability to generate new virulence types by sexual recombination, whereas the obligately outcrossing host S. latifolia may profit from rearrangement of resistance alleles by random mating. Second, populations often harbor only a few infected individuals, so virulence variation may be further reduced by drift. Third, migration rates among host plant populations are much higher than among pathogen populations, possibly because pollinators prefer healthy over diseased plants. Migration among partly isolated populations may therefore introduce novel host plant resistance variants more often than novel parasite virulence variants. That migration contributes to the coevolutionary dynamics in this system is supported by the geographic pattern of infectivity. Infection success increased over the first 10-km range of host-pathogen population distances, which is likely the natural range of gene exchange.
TL;DR: To show phylogenetic relationships among the smut fungi and their relatives, a part of the nuclear LSU rDNA from 43 different species of smut fungus and related taxa was sequenced and two groups of smUT fungi appeared.
Abstract: To show phylogenetic relationships among the smut fungi and their relatives, we sequenced a part of the nuclear LSU rDNA from 43 different species of smut fungi and related taxa. Our data were combined with the existing sequences of seven further smut fungi and 17 other basidiomycetes. Two sets of sequences were analyzed. The first set with a representative number of simple septate basidiomycetes, complex septate basidiomycetes, and smut fungi was analyzed with the neighbor-joining method to estimate the general topology of the basidiomycetes phylogeny and the positions of the smut fungi. The tripartite subclassification of the basidiomycetes into the Urediniomycetes, Ustilaginomycetes, and Hymenomycetes was confirmed and two groups of smut fungi appeared. The smut genera Aurantiosporium, Microbotryum, Fulvisporium, and Ustilentyloma are members of the Urediniomycetes, whereas the other smut species tested are members of the Ustilaginomycetes with Entorrhiza as a basal taxon. The second set of 46 Ustilagi...
TL;DR: Genetic similarity underlying the host-parasite interactions appeared to have the most important influence on specialization and host-shifts: generalist multi-host parasite species were found on closely related plant species, and related species in the Microbotryum phylogeny were associated with members of the same host clade.
Abstract: Using phylogenetic approaches, the expectation that parallel cladogenesis should occur between parasites and hosts has been validated in some studies, but most others provided evidence for frequent host shifts. Here we examine the evolutionary history of the association between Microbotryum fungi that cause anther smut disease and their Caryophyllaceous hosts. We investigated the congruence between host and parasite phylogenies, inferred cospeciation events and host shifts, and assessed whether geography or plant ecology could have facilitated the putative host shifts identified. For cophylogeny analyses on microorganisms, parasite strains isolated from different host species are generally considered to represent independent evolutionary lineages, often without checking whether some strains actually belong to the same generalist species. Such an approach may mistake intraspecific nodes for speciation events and thus bias the results of cophylogeny analyses if generalist species are found on closely related hosts. A second aim of this study was therefore to evaluate the impact of species delimitation on the inferences of cospeciation. We inferred a multiple gene phylogeny of anther smut strains from 21 host plants from several geographic origins, complementing a previous study on the delimitation of fungal species and their host specificities. We also inferred a multi-gene phylogeny of their host plants, and the two phylogenies were compared. A significant level of cospeciation was found when each host species was considered to harbour a specific parasite strain, i.e. when generalist parasite species were not recognized as such. This approach overestimated the frequency of cocladogenesis because individual parasite species capable of infecting multiple host species (i.e. generalists) were found on closely related hosts. When generalist parasite species were appropriately delimited and only a single representative of each species was retained, cospeciation events were not more frequent than expected under a random distribution, and many host shifts were inferred. Current geographic distributions of host species seemed to be of little relevance for understanding the putative historical host shifts, because most fungal species had overlapping geographic ranges. We did detect some ecological similarities, including shared pollinators and habitat types, between host species that were diseased by closely related anther smut species. Overall, genetic similarity underlying the host-parasite interactions appeared to have the most important influence on specialization and host-shifts: generalist multi-host parasite species were found on closely related plant species, and related species in the Microbotryum phylogeny were associated with members of the same host clade. We showed here that Microbotryum species have evolved through frequent host shifts to moderately distant hosts, and we show further that accurate delimitation of parasite species is essential for interpreting cophylogeny studies.
TL;DR: Studies on the process of disease emergence by host shifts using the model system of anther‐smut disease (Microbotryum violaceum) on the plant genus Silene are presented, indicating the potential for rapid evolution of resistance.
Abstract: The need to prevent and cure emerging diseases often precludes their continuing study in situ. We present studies on the process of disease emergence by host shifts using the model system of anther‐smut disease (Microbotryum violaceum) on the plant genus Silene (Caryophyllaceae). This system has little direct social impact, and it is readily amenable to experimental manipulation. Our microevolutionary studies have focused on the host shift of Microbotryum from Silene alba (=latifolia; white campion) onto Silene vulgaris (bladder campion) in a population in Virginia. Karyotypic variation shows that the host shift is recent and originates from the disease on sympatric S. alba. Analysis of the spatial pattern of disease shows that the host shift has been contingent on the co‐occurrence of the two species at a local scale. Cross‐inoculation studies show that families of the new host differ greatly in their susceptibility to the pathogen, indicating the potential for rapid evolution of resistance. Di...
TL;DR: The effect of limited gene flow in this parasite on its coevolutionary interaction with its host, and its potential for local adaptation on sympatric host populations are discussed.
Abstract: We investigated the genetic population structure in a metapopulation of the plant Silene latifolia (Caryophyllaceae) and its fungal pathogen Microbotryum violaceum (Ustilaginales), a pollinator-borne disease. Population structure of the host plant was estimated using allozyme markers and that of the fungus by microsatellites. Both host and parasite showed significant differentiation, but parasite populations were 12 times more strongly differentiated than those of the hosts. We found significant isolation by distance for host populations but not for parasite populations. Higher population differentiation for the parasite may result from small effective population size, high selfing rates, or low migration rate. In this system, hosts are obligate outcrossers and they migrate by seeds and pollen, whereas parasites can self-fertilize and migrate only on pollinating insects. We discuss the effect of limited gene flow in this parasite on its coevolutionary interaction with its host, and its potential for local adaptation on sympatric host populations.