Effects of Gasteroid Fruiting Body Morphology on Diversification Rates in Three Independent Clades of Fungi Estimated Using Binary State Speciation and Extinction Analysis

Abstract

Gasteroid fungi include puffballs, stinkhorns, and other forms that produce their spores inside the fruiting body. Gasteroid taxa comprise about 8.4% of the Agaricomycetes (mushroom-forming fungi) and have evolved numerous times from nongasteroid ancestors, such as gilled mushrooms, polypores, and coral fungi, which produce spores on the surface of the fruiting body. Nongasteroid Agaricomycetes have a complex mechanism of forcible spore discharge that is lost in gasteroid lineages, making reversals to nongasteroid forms very unlikely. Our objective was to determine whether gasteromycetation affects the rate of diversification of lineages "trapped" in the gasteroid state. We assembled four datasets (the Sclerodermatineae, Boletales, Phallomycetidae, and Lycoperdaceae), representing unique origins of gasteroid fungi from nongasteroid ancestors and generated phylogenies using BEAST. Using the program Diversitree, we analyzed these phylogenies to estimate character-state-specific rates of speciation and extinction, and rates of transitions between nongasteroid and gasteroid forms. Most optimal models suggest that the net diversification rate of gasteroid forms exceeds that of nongasteroid forms, and that gasteroid forms will eventually come to predominate over nongasteroid forms in the clades in which they have arisen. The low frequency of gasteroid forms in the Agaricomycetes as a whole may reflect the recent origins of many gasteroid lineages.

How do Agaricomycetes shape their fruiting bodies? 1. Morphological aspects of development

“…Gasteroid evolutions tend to be terminal positions of development (Thiers, 1984;Lebel et al, 2012;Oberwinkler, 2012). Evolution of angiocarpous fruiting bodies from non-gasteroid clades correlates with loss of ballistospory (Thiers, 1984;Hibbett et al, 1997;Wilson et al, 2011), which is the active spore discharge mechanism employing Buller's drops at the proximal tips of basidiospores that is innate to the basidiomycetes (Buller, 1909;Pringle et al, 2005). Indeed, loss of ballistospory appears to be the only criterion shared between the diverse evolutionary lineages of gasteroid species (Reijnders, 2000).…”

Dating the emergence of truffle-like fungi in Australia, by using an augmented meta-analysis

“…Wilson et al (2011) did examine extinction in gasteroid fungi (again a broader definition than the sequestrate fungi defined here). Although noting that the low occurrence of gasteroid forms was consistent with the idea that these fungi are at a heightened risk of extinction, their results suggested that gasteroid fungi may be diversifying more rapidly (or at least no less rapidly) than their non-gasteroid counterparts (Wilson et al 2011). Persistence for millions of years to the current day by sequestrate fungi across several lineages suggests some degree of stability.…”

“…For the other nine lineages, datasets were compiled from sets of GenBank sequences as utilised in published studies, and, in two cases, these were augmented with further sequences from GenBank. The published Sclerodermataceae phylogeny (Wilson et al 2011) was augmented to include 'Pisolithus sp. MURU' (Pisolithus hypogaeus) and its closest five BLAST matches on GenBank.…”

Molecular techniques revolutionize knowledge of basidiomycete evolution

“…Binder et al 2010). However, taxonomy, including fungal taxonomy, faces serious challenges (Agnarsson and Kuntner 2007), and thus, fungal taxonomists should consider adopting new modes of working (Hibbett et al 2011), in order to accelerate the discovery and documentation of the world's fungal heritage.…”

“…Binder and Hibbett 2007;Hosaka et al 2007). Newly most optimal models suggest that the net diversifica- tion rate of gasteroid forms exceeds that of non-gasteroid forms, and that gasteroid forms will eventually come to predominate over non-gasteroid forms in the clades in which they have arisen (Wilson et al 2011). …”