Historical Biogeography and Diversification of Truffles in the Tuberaceae and Their Newly Identified Southern Hemisphere Sister Lineage

Abstract

Truffles have evolved from epigeous (aboveground) ancestors in nearly every major lineage of fleshy fungi. Because accelerated rates of morphological evolution accompany the transition to the truffle form, closely related epigeous ancestors remain unknown for most truffle lineages. This is the case for the quintessential truffle genus Tuber, which includes species with socio-economic importance and esteemed culinary attributes. Ecologically, Tuber spp. form obligate mycorrhizal symbioses with diverse species of plant hosts including pines, oaks, poplars, orchids, and commercially important trees such as hazelnut and pecan. Unfortunately, limited geographic sampling and inconclusive phylogenetic relationships have obscured our understanding of their origin, biogeography, and diversification. To address this problem, we present a global sampling of Tuberaceae based on DNA sequence data from four loci for phylogenetic inference and molecular dating. Our well-resolved Tuberaceae phylogeny shows high levels of regional and continental endemism. We also identify a previously unknown epigeous member of the Tuberaceae – the South American cup-fungus Nothojafnea thaxteri (E.K. Cash) Gamundí. Phylogenetic resolution was further improved through the inclusion of a previously unrecognized Southern hemisphere sister group of the Tuberaceae. This morphologically diverse assemblage of species includes truffle (e.g. Gymnohydnotrya spp.) and non-truffle forms that are endemic to Australia and South America. Southern hemisphere taxa appear to have diverged more recently than the Northern hemisphere lineages. Our analysis of the Tuberaceae suggests that Tuber evolved from an epigeous ancestor. Molecular dating estimates Tuberaceae divergence in the late Jurassic (∼156 million years ago), with subsequent radiations in the Cretaceous and Paleogene. Intra-continental diversification, limited long-distance dispersal, and ecological adaptations help to explain patterns of truffle evolution and biodiversity.

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

“…A more recent study of the Myrtaceae places the crown node between 84 and 88 million years ago (Thornhill et al 2012), and the crown node for the ECM Hysterangiales is estimated here at c. 65 million years ago, thus supporting the prediction of Hosaka et al (2008). Although the Hysterangiales is the oldest lineage in the present analysis, the true-truffle ascomycete genus, Tuber, not known to occur in Australia, is also ECM and diverged even earlier, at about the same time as did the Eudicots in the late Cretaceous (c. 142 million years ago; Bonito et al 2013).…”

“…This hypothesis is supported by the high diversity of sequestrate fungi in the dry continent of Australia (Bougher and Lebel 2001;Danks et al 2010;Trappe et al 2010;Castellano et al 2011;Lebel and Syme 2012;Lebel et al 2015) as well as seasonally dry western North America States 2001, 2002;Trappe et al 2009). Alternatively, the stimulus may be related to an association with plant hosts because most sequestrate taxa are ectomycorrhizal (Tedersoo et al 2010), and distributions and diversity of sequestrate fungi are thought to be driven more generally by plant host availability and diversity (Jumpponen et al 2004;Bonito et al 2013). In addition to the dependence of ectomycorrhizal fungi on their plant hosts, sequestrate fungi also rely on animals (insects, reptiles, birds and mammals) to disperse their spores (Claridge and May 1994;.…”

Certainties and uncertainties about the life cycle of the Périgord black truffle (Tuber melanosporum Vittad.)

“…It comprises at least 180 species (Bonito et al 2013). Index Fungorum recognizes 290 species, subspecies and varieties.…”

The role of wild boars in spore dispersal of hypogeous fungi

“…Hypogeous fungi comprise species belonging to several genera of Ascomycota (true truffles), Basidiomycota and Muromycotina (false truffles) (Trappe et al 2009;Bonito et al 2013). The hypogeous lifestyle comported several morphological changes, as the loss of the ability to discard spores actively .…”