Mushrooms are not only tasty, but also provide numerous examples of evolutionary convergence...

Mushrooms are probably the most familiar group of fungi and celebrated for their tastiness (and, if misidentified, their potential lethality). Strictly speaking, a mushroom is the fleshy fruiting body of about 8000 species of fungus in the Agaricomycotina, one of three subphyla in the phylum Basidiomycota (the other two being the rusts (Pucciniomycotina) and the smuts (Ustilaginomycotina)). The fruiting body serves to disperse the spores, sometimes involving the extraordinary process of ballistospory. Mushrooms come in a variety of shapes, and their classification had long been based on the form of the fruiting body. Work on the airflow across these structures, however, has suggested that they both facilitate spore dispersal and reflect adaptive needs. It is therefore not surprising that the shapes of fruiting bodies show extensive convergence. This has, of course, had implications for mushroom classification, although many guide books still use the old system. There are some interesting trends in that some transformations from one fruiting body shape to another tend to be more common than others, while in certain cases the shift seems to be irreversible (as in the gasteroids, best known as puffballs and earthstars). The tendencies and trends are quite complex, and only a brief outline is given here.

Resupinate forms

These forms, as their name suggests, tend to lie flat on the surface. The fruiting bodies can be thin and cobweb-like or more robust and crustose. More than 2000 species of fungus show this morphology. It is highly polyphyletic with at least twelve independent evolutionary origins. Not only does it occur in every major clade of the Homobasidiomycetes (a large and diverse group of macrofungi), with some clades containing almost exclusively resupinate forms, but also in some heterobasidiomycete clades (Auriculariales, Dacrymycetales and Tremellales). Comparative analyses indicated that there is a greater tendency to go from resupinate to non-resupinate forms than vice versa. This has been interpreted as reflecting an evolutionary trend towards increased morphological complexity, as the resupinate forms are relatively simple. A more recent analysis, however, has not supported the conclusion that the resupinate morphology is an evolutionarily labile one.

Cyphelloids

Cyphelloid fungi are characterised by tiny (1-2 mm) cup-shaped fruiting bodies with smooth spore-bearing surfaces. These fruiting bodies typically grow on dead or decaying wood and occur in clusters. It has been estimated that there might be 400-500 species of cyphelloid fungi, but their actual diversity remains mysterious. Those species that have been described so far show a cosmopolitan distribution, but are better known from northern temperate regions. Intriguingly, two cyphelloid species, Calathella mangrovei and Halocyphina villosa, are salt-tolerant and found on mangroves, where they are periodically submerged in seawater. Molecular phylogenetic analyses have suggested that there are at least ten to twelve (probably more) independent evolutionary origins of the cyphelloid form, representing cases of a reduction from morphologically more complex agaricoid ancestors.

Aquatic mushrooms

The two cyphelloid species that are associated with mangroves are not the only mushrooms that occur in an aquatic environment. Within the homobasidiomycetes, about a dozen species are found in marine or freshwater habitats and have evolved unique morphological adaptations. The marine gasteroid Nia vibrissa, for example, grows on fully submerged substrates and produces spores equipped with hairs that might help them to float and disperse successfully. Another marine species, Mycaureola dilseae, which is a parasite of a red alga, is not at all closely related to N. vibrissa. According to a molecular phylogenetic analysis, the move from terrestrial to aquatic habit has occurred three or four times independently. Mangroves might have represented a stepping-stone in this transition.

Gasteroids

These closed, bag-shaped forms are amongst the most striking of the fungi and include the puffballs, earthstars (Geastrales), bird’s nest fungi (Nidulariaceae) and false truffles (Hymenogastrales). They have evolved at least four times and, as explained below, often materialise via a secotioid intermediate (although there are other possible evolutionary routes). Gasteroids show great diversity in the form of the fruiting body and the mechanism of spore dispersal. Unlike most other homobasidiomycetes, they produce their spores internally and have lost the ability to forcibly discharge them. It has been suggested that this loss of ballistospory has constrained the evolution of other forms from the gasteroids. The remarkable Sphaerolobus, however, has reinvented a method of spore dispersal that is akin to a cannon.

Secotioid syndrome

The secotioid arrangement (or syndrome) involves the loss of the characteristic gills and the transformation of the fungus into a contorted mass of tissue. Whilst this is a dramatic morphological shift, it is genetically trivial and in some cases may depend on only a single gene. Hence, we can hardly be surprised that it has occurred numerous times. The secotioid arrangement does, however, appear to be functionally unsatisfactory, especially for the all-important release and dispersal of spores (which now largely relies on animals rather than air currents). So most secotioid “experiments” might in fact be short-lived. However, there are also possible advantages of a more closed form, such as moisture retention. Furthermore, it seems to be the best route to become gasteroid, which is why the secotioid syndrome has attracted a great deal of attention amongst mycologists. No wonder gasteroid fungi turn out to be polyphyletic as well – even if the great majority of secotioids fail, there are more than enough that pull through to ensure a continuous supply of new gasteroids.

Bracket and coralloid fungi

Within the Homobasidiomycetes, pileate-sessile and coralloid-clavarioid forms have evolved multiple times. They are considered the evolutionarily most labile fruiting body morphologies, meaning that they commonly evolve into other forms, while reverse transformations are rare. Pileate-sessile forms have a cap but lack a stalk. This group includes the bracket or shelf fungi, such as the beefsteak fungus (Fistulina hepatica). Most of these tough, sturdy fungi grow on trees, where they are parasitic or saprotrophic and can cause considerable damage. The erect fruiting bodies of coralloid-clavarioid forms (e.g. Ramaria) are club-shaped or branched, resembling a coral. These saprotrophic fungi, which can be very colourful, grow in leaf litter on the ground or on decaying wood or vegetation.

Smut fungi

Smut fungi are a very important group of multicellular plant parasites, which can do serious damage to crops, particularly cereal grasses. Whilst the corn smut (Ustilago maydis) is probably best known, there are more than a thousand species of smut fungus. For infection to occur, cells of compatible mating types have to fuse. They then form galls on the plant, which burst to release vast numbers of dark, dust-like teliospores. Teliospores are ornamented, and it has been shown that particular types of ornamentation (e.g. warts) can arise through different developmental pathways in different genera. This independent evolution of similar structures might be due to constraints acting on spore morphology to ensure successful dispersal. Several genera form so-called spore balls consisting of both spores and sterile cells, which have evolved as an adaptation to parasitize water plants. The ultrastructure of these spore balls differs between Doassansiopsis and other genera, again suggesting convergent evolution.