A phylogenetic study of the Cantharellales supports recognition of four families and independent gains of biotrophic nutritional modes.

PREMISE

The agaricomycete order Cantharellales contains approximately 1000 species of fungi characterized by diverse morphological forms, ecological guilds, and nutritional modes. Examples include coralloid lichens that form symbioses with unicellular green algae, bulbil-forming lichenicolous species, corticioid free-living fungi that degrade dead sources of organic carbon, pathogens that cause plant disease, orchid root endosymbionts, and ectomycorrhizal fungi including popular edible mushrooms. However, evolutionary relationships in the Cantharellales remain poorly understood due to conflicting estimates based on ribosomal DNA loci.

METHODS

We constructed a five-gene phylogeny of the Cantharellales using data from 301 specimens to evaluate family-level relationships. We used penalized likelihood to estimate divergence times and ancestral state reconstruction to test the hypothesis of multiple independent origins of biotrophic ecologies in the order and whether those transitions are younger than the divergence times of associated plant or lichen hosts.

RESULTS

Four monophyletic families were recovered with strong support: Botryobasidiaceae, Ceratobasidiaceae, Hydnaceae s.l., and Tulasnellaceae, with Hydnaceae containing the greatest species richness and morphological diversity. Our results suggest the Cantharellales diverged during the Carboniferous period with subsequent diversification following the Permian-Triassic extinction. Ancestral state reconstruction supports a saprotrophic most recent common ancestor with at least three transitions to an ectomycorrhizal ecology, multiple transitions to a lichenicolous habit with one or more subsequent transitions to mutualistic nutritional modes, four transitions to an orchid mycorrhizal ecology, and two transitions to a lichenized lifestyle.

CONCLUSIONS

This study represents the first comprehensive examination of the evolution of form and function across this ecologically and morphologically diverse order of fungi.