Convergent evolution of highly reduced fruiting bodies in Pezizomycotina suggests key adaptations to the bee habitat

BACKGROUND: Among the understudied fungi found in nature are those living in close association with social and solitary bees. The bee-specialist genera Bettsia, Ascosphaera and Eremascus are remarkable not only for their specialized niche but also for their simple fruiting bodies or ascocarps, which are morphologically anomalous in Pezizomycotina. Bettsia and Ascosphaera are characterized by a unicellular cyst-like cleistothecium known as a spore cyst, while Eremascus is characterized by completely naked asci, or asci not formed within a protective ascocarp. Before molecular phylogenetics the placement of these genera within Pezizomycotina remained tentative; morphological characters were misleading because they do not produce multicellular ascocarps, a defining character of Pezizomycotina. Because of their unique fruiting bodies, the close relationship of these bee-specialist fungi and their monophyly appeared certain. However, recent molecular studies have shown that Bettsia is not closely related to Ascosphaera. In this study, I isolated the very rare fungus Eremascus fertilis (Ascomycota, Pezizomycotina) from the bee bread of honey bees. These isolates represent the second report of E. fertilis both in nature and in the honey bee hive. To establish the systematic position of E. fertilis and Bettsia alvei, I performed phylogenetic analyses of nuclear ribosomal LSU + SSU DNA sequences from these species and 63 additional ascomycetes. RESULTS: The phylogenetic analyses revealed that Eremascus is not monophyletic. Eremascus albus is closely related to Ascosphaera in Eurotiomycetes while E. fertilis belongs in Myxotrichaceae, a putative member of Leotiomycetes. Bettsia is not closely related to Ascosphaera and like E. fertilis apparently belongs in Leotiomycetes. These results indicate that both the naked ascus and spore cyst evolved twice in the Pezizomycotina and in distantly related lineages. The new genus Skoua is described to accommodate E. fertilis. CONCLUSIONS: The naked ascus and spore cyst are both shown to have evolved convergently within the bee habitat. The convergent evolution of these unusual ascocarps is hypothesized to be adaptive for bee-mediated dispersal. Elucidating the dispersal strategies of these fungal symbionts contributes to our understanding of their interaction with bees and provides insight into the factors which potentially drive the evolution of reduced ascocarps in Pezizomycotina. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12862-015-0401-6) contains supplementary material, which is available to authorized users.