Evolution of substrate specificity and fungal symbiosis in filmy ferns (Hymenophyllaceae): a Bayesian approach for ambiguous character state reconstruction

Ferns, as landplants in general, originally form a symbiosis involving Arbuscular Mycorrhizal Fungi (AMF), which are prevalent in habitats directly connected to the soil, including low epiphytic sites, but are largely absent in the high epiphytic habitat. High probabilities of AMF should be expected in chiefly terrestrial lineages whereas truly, fully adapted epiphytic lineages should be lacking fungal endophytes or may have switched to other types of fungi; e.g. Dark Septate Endophytes (DSE), a morphological class of mostly unspecified fungi that is often found in epiphytic ferns and may include potentially symbiotic ascomycetes. We used a Bayesian approach for a comparison of the ambiguous character of preferred substrate with the incompletely known mycorrhization status for an ancient lineage of ferns, the Hymenophyllaceae or filmy ferns. The majority of the analysed 167 species prefers either the saxicolous, terrestrial or epiphytic habitat (differentiated into low and high epiphytic), but there are also many generalists without clear preference. For the whole family Hymenophyllaceae and one of the two main clades of the subfamily Trichomanoidae, the terrestrial habitat and AMF received the highest probability for representing the ancestral state. For the subfamily Hymenophylloidae, the low epiphytic habitat and DSE received the highest probability as ancestral state, whereas that for AMF was very low. The other main clade of the subfamily Trichomanoidae as well as the whole subfamily was found most likely to be originally terrestrial; but in both cases the probability values did not differ much from the values for low epiphytism, with all values around 50 ± 5%. The high epiphytic habitat, which in its present condition is thought to be possible only in angiosperm-dominated vegetation, did not receive high probability to be the ancestral state in any clade. This decouples the evolution of epiphytism in filmy ferns in time from the advent of the angiosperms, which is hypothesized to have triggered the radiation of all other major epiphytic fern lineages.