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Cophylogeny of the anther smut fungi and their caryophyllaceous hosts: prevalence of host shifts and importance of delimiting parasite species for inferring cospeciation.

ABSTRACT: BACKGROUND: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. RESULTS: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. CONCLUSION: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.

SUBMITTER: Refregier G

PROVIDER: S-EPMC2324105 | biostudies-literature | 2008 Mar

REPOSITORIES: biostudies-literature

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Cophylogeny of the anther smut fungi and their caryophyllaceous hosts: prevalence of host shifts and importance of delimiting parasite species for inferring cospeciation.

Refrégier Guislaine G Le Gac Mickaël M Jabbour Florian F Widmer Alex A Shykoff Jacqui A JA Yockteng Roxana R Hood Michael E ME Giraud Tatiana T

BMC evolutionary biology 20080327

<h4>Background</h4>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, an ...[more]

PMID: 18371215

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Project description:The first taxonomic treatment of the smut fungi in Greenland is provided. A total of 43 species in 11 genera are treated and illustrated by photographs of sori, microphotographs of spores in LM and SEM, and distribution maps. Two species, Anthracoidea pseudofoetidae and Urocystis tothii, are recorded as new from North America. Thirteen species, Anthracoidea altera, A. capillaris, A. limosa, A. liroi, A. pseudofoetidae, A. scirpoideae, A. turfosa, Microbotryum lagerheimii, M. stellariae, Schizonella elynae, Stegocintractia luzulae, Urocystis fischeri, and U. tothii, are reported for the first time from Greenland. Three new fungus-host combinations, Anthracoidea capillaris on Carex boecheriana, Anthracoidea pseudofoetidae on Carex maritima, and Urocystis tothii on Juncus biglumis, are given. Five plant species are reported as new hosts of smut fungi in Greenland, namely, Carex nigra for Anthracoidea heterospora, C. canescens for Anthracoidea karii, C. fuliginosa subsp. misandra for Anthracoidea misandrae, C. maritima for Orphanomyces arcticus, and C. fuliginosa subsp. misandra for Schizonella melanogramma. Three species, Microbotryum violaceum s. str. (recorded as 'Ustilago violacea'), Urocystis anemones, and U. junci, which were previously reported from Greenland, are considered wrongly identified. Additional distribution records are given for 12 species from Greenland: Anthracoidea bigelowii, A. caricis, A. elynae, A. lindebergiae, A. misandrae, A. nardinae, A. rupestris, A. scirpi, Schizonella melanogramma, Stegocintractia hyperborea, Urocystis agropyri, and U. sorosporioides. The most numerous distribution groups are the following: circumpolar-alpine and Arctic-alpine species - 14; circumboreal-polar species - 10; and circumpolar and Arctic species - 6. The most widely distributed smut fungi in Greenland were Anthracoidea bigelowii, A. elynae, Microbotryum bistortarum, and M. vinosum. Most species were found in the High Arctic zone (29 species), while from the Low Arctic zone and the Subarctic zone, 26 and 19 species were known, respectively. Ten species, Anthracoidea bigelowii, A. capillaris, A. elynae, Microbotryum bistortarum, M. koenigiae, M. pustulatum, M. silenes-acaulis, M. vinosum, Schizonella elynae, and Urocystis sorosporioides, were recorded from all three zones. Only plants belonging to six families, Cyperaceae, Poaceae, Juncaceae, Ranunculaceae, Caryophyllaceae, and Polygonaceae, out of a total of 55 in the flora of Greenland, hosted smut fungi. Cyperaceae was the plant family with most host species (23). Carex was the genus with the highest number of host species (22). The total number of the host plants (45 species) was 8.5 % out of a total of 532 vascular plants in the flora of Greenland. A new combination in Carex, C. macroprophylla subsp. subfilifolia, is proposed for Kobresia filifolia subsp. subfilifolia.

Dataset Information

Cophylogeny of the anther smut fungi and their caryophyllaceous hosts: prevalence of host shifts and importance of delimiting parasite species for inferring cospeciation.

Publications

Cophylogeny of the anther smut fungi and their caryophyllaceous hosts: prevalence of host shifts and importance of delimiting parasite species for inferring cospeciation.

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