Evolution of marine mushrooms.

Fungi make up one of the most diverse, ecologically important groups of eukaryotes. The vast majority of fungi are terrestrial, but the chytridiomycetes, a basal group of fungi, includes flagellated, unicellular, aquatic forms, and it is likely that this was the ancestral condition of the group (1). The more derived groups of fungi—zygomycetes, ascomycetes, and basidiomycetes—are all predominantly filamentous and terrestrial, and lack flagellated cells at any stage of the life cycle. Within the basidiomycetes, the most conspicuous group is the homobasidiomycetes, which includes about 13,000 described species of mushrooms and related forms. Eleven species of homobasidiomycetes (in eight genera) occur in marine or freshwater habitats. To resolve the relationships among terrestrial and aquatic homobasidiomycetes, we assembled a data set of ribosomal DNA (rDNA) sequences that includes 5 aquatic species and 40 terrestrial species. Phylogenetic trees obtained using parsimony and maximum likelihood (ML) methods suggest that there have been three or four independent transitions from terrestrial to aquatic habitats within the homobasidiomycetes. Three of the marine taxa in our data set are associated with mangroves, suggesting that these ecosystems provide a common evolutionary stepping-stone by which homobasidiomycetes have reinvaded aquatic habitats. One of the major themes in the evolution of eukaryotes is the repeated transition from aquatic to terrestrial habitats that has occurred in several major clades, including fungi, plants, and animals. In a classic paper, Pirozynski and Malloch (2) suggested that fungi and plants were the first eukaryotes to colonize the land, and that this ecological shift was made possible by the establishment of mycorrhizal symbioses (associations involving fungal hyphae and plant roots). This hypothesis has been bolstered by the recent discovery of spores of putatively mycorrhizal fungi from the Ordovician (3). Fungi have radiated extensively in terrestrial habitats, where they play pivotal ecological roles, as decayers, pathogens, and symbionts of plants and animals. One group of fungi that is elegantly adapted to life on the land is the homobasidiomycetes. Adaptations to terrestrial habitats displayed by some homobasidiomycetes include rootlike rhizomorphs that allow the fungi to forage along the forest floor, drought-resistant sclerotia, and tough, perennial fruiting bodies. Aerial spore dispersal in homobasidiomycetes is accomplished by a forcible discharge mechanism termed ballistospory. However, several lineages of terrestrial homobasidiomycetes have lost ballistospory, including puffballs and other forms with enclosed spore-bearing structures. Aquatic homobasidiomycetes include four species that have retained ballistospory and seven species that have lost ballistospory. The ballistosporic forms can be tentatively assigned to certain terrestrial groups on the basis of the morphology of spores and fruiting bodies (4–12). However, the aquatic homobasidiomycetes that have lost ballistospory have no obvious close relatives among terrestrial groups. This taxonomically enigmatic assemblage includes several marine genera that have elongate or appendaged spores, which superficially resemble the spores of many aquatic ascomycetes (4, 5; Fig. 1). To resolve the relationships among terrestrial and aquatic homobasidiomycetes, we assembled a data set that includes 4 marine species, 1 freshwater species, and 40 diverse terrestrial species (Fig. 2). The heterobasidiomycete “jelly fungus” Auricularia auricula-judae was included for rooting purposes. The data set contains sequences of four rDNA regions, including nuclear and mitochondrial small and large subunit rDNA (3.8 kb total). Four species in the data set lack the mitochondrial large subunit rDNA sequence (Fig. 2). Sequences from 38 terrestrial species and one marine species, Nia vibrissa, were drawn from earlier studies (13, 14). Received 19 July 2001; accepted 30 August 2001. * To whom correspondence should be addressed. E-mail: dhibbett@ black.clarku.edu Reference: Biol. Bull. 201: 319–322. (December 2001)