Giraud, Tatiana*; Le Gac, Mickael ; Hood, Michael. Reproductive isolation in the Microbotryum violaceum species complex, anther smut of the Caryophyllaceae. In: International Meeting on "Population and Evolutionary Biology of Fungal Symbionts", Ascona, Switzerland, 2007. AB-01. Click here to download the presentation on pdf format.

Detecting the cryptic structure of species complexes is essential for an accurate accounting of the biological diversity in natural systems, especially as the different sibling species have often evolved very different life history traits. Microbotryum violaceum is a fungus that causes the sterilizing anther-smut disease in many species of Caryophyllaceae. The degree of specialization and the extent of gene flow between strains on different host species (host races) were controversial in the literature. In order to settle these issues, we conducted molecular phylogenetic analyses on 23 host races of M. violaceum from different geographic origins using three single-copy nuclear genes (ß-tub, γ-tub and Ef1α). The congruence between the gene phylogenies allowed identification of several lineages that seem to evolve independently for several millions of years. These lineages were highly specialized on different host species and had largely overlapping geographic ranges. The coexistence of these lineages in sympatry without gene flow indicates the existence of strong reproductive isolation barriers. These results thus suggest that M. violaceum is a complex of highly specialized sibling species. Two incongruencies between the individual gene phylogenies and one intra-gene recombination event were detected at basal nodes, suggesting some ancient introgression or speciation events via hybridizations. Neither incongruences nor recombination were however detected among terminal branches of different lineages, indicating that the demonstrated potential for cross-infection and experimental mating among some lineages is not sufficient to allow introgressions.

We then investigated the evolution reproductive isolation among the identified sympatric species of the complex M. violaceum. The relative importance of pre- and post-mating reproductive isolation remains an unresolved and critical gap in our understanding of speciation processes. Previous work, primarily involving animal systems, indicates that pre-mating isolation is most strongly favoured among close species in sympatry. In M. violaceum, we found no evidence of pre-mating isolation associated with assortative mating. In contrast, post-mating isolation in the form of hybrid inviability increased with the genetic distance between mating partners, both when measured as hyphal growth or the ability to cause disease. The surprising lack of significant assortative mating among sympatric species despite the existence of a strong post-mating isolation may be due to the life cycle of M. violaceum. Ecological barriers in association with the disease have indeed been suggested, which may limit local interactions between pathogen strains adapted to different hosts, such as habitat isolation and vector specialization. The propensity of M. violaceum for selfing probably also contributes to an effective pre-mating isolation in sympatry without the need of specific genetic mechanisms of assortative mating.

Keywords: multiple gene genealogies, Ustilago violacea, specialization, cryptic species, sibling species, Phylogenies, sympatry, adaptation

*Institution: ESE Univ Paris Sud

Email: Tatiana.Giraud@u-psud.fr