Troubles with mycorrhizal mushroom identification where morphological differentiation lags behind barcode sequence divergence

Abstract

Species of Russula (Russulaceae), a large, cosmopolitan, ectomycorrhizal fungal genus are notoriously difficult to identify. To delimit species and to evaluate their morphology, we sequenced the ~400 bp ITS2 ribosomal DNA region from 713 Pacific Northwest Russula specimens from Benjamin Woo's exceptional collection. As a topological constraint for analysis of the ITS2, we sequenced and inferred a phylogeny from the ITS, LSU, RPB2 and EF1-α regions from 50 European and North American specimens of major clades in Russula. We delimited 72 candidate species from Woo's collection's ITS2 sequences using ABGD, GMYC, PTP, and mothur software. To guide application of names, we sequenced a ~200 bp portion of the ITS from 18 American type specimens. Of the 72 delimited species, 28 matched a type or a currently barcoded European species. Among the remaining 44 are poorly known or undescribed species. We tested the congruence of morphology with delimitations for 23 species represented by 10 or more specimens each. No morphological character alone was consistently diagnostic across all specimens of any of the 23 candidate species. Ordination of combined field characters followed by pairwise multivariate analysis of variance showed that centroids were significantly different in 221 of 253 species pair comparisons. Ordination also showed that specimens from the same species were widely dispersed, overlapping with specimens from other species. This explains why only 48.5% of specimens were correctly assigned to their species in a canonical variates analysis of combined field and spore characters. Based on sequence comparisons, we contribute to correcting the broad and confusing misapplications of European names that have long obscured patterns of Russula's geographical distribution and diversification. Our evidence suggests that morphology in Russula diverges slowly, and that phenotypic plasticity, convergence, or retention of ancestral polymorphisms blur the distinctions among recently derived species.

Over the hills, but how far away? Estimates of mushroom geographic range extents

“…We sequenced the ITS region of 604 mushroom specimens representing 289 species from 75 genera deposited in the Beaty Biodiversity Museum (UBC Herbarium). DNA extraction was as in Bazzicalupo et al (). The Canada Michael Smith Genome Sciences Centre (Vancouver, BC) performed PCR and sequencing using primers ITS1F (Gardes & Bruns, ) and ITS4 (White, Bruns, Lee, & Taylor, ).…”

“…Fungi play essential roles in terrestrial ecosystems by decaying wood, causing diseases of plants, or forming mycorrhizal partnerships. With increasing global CO 2 levels and temperatures, fungal geographic ranges may expand (Pringle, Adams, Cross, & Bruns, 2009) or contract (Ellis, Coppins, Dawson, & Seaward, 2007) potentially altering rates of wood decay (Allison & Treseder, 2008) or increasing plants' susceptibility to fungal infections (Chen et al, 2007). Elucidating distributional ranges is important for predicting shifts in key ecosystem services that may accompany environmental change (Peay, Bidartondo, & Arnold, 2010).…”

Phylogenetic study documents different speciation mechanisms within the Russula globispora lineage in boreal and arctic environments of the Northern Hemisphere

“…Current studies suggest that Russula species reported from multiple continents are mainly boreal-arctic taxa. Bazzicalupo et al (2017) found that 17 of 72 Russula species from the Northwest of the USA (mostly from boreal-arctic areas) matched a sequence of European barcoded taxa. Accordingly, Geml et al (2012) suggested that long distance dispersal and gene flow between boreal-arctic species of the Russulaceae (Russula and Lactarius) was common.…”

The unbearable lightness of sequenced-based identification

“…-Are dependent on the chosen similarity cut-off for species recognition. The often applied 97% similarity cut-off (Lindahl et al 2013;Selosse et al 2016) is certainly too low for most mushrooms as suggested by several recent taxonomic revisions (Bazzicalupo et al 2017;Yuan 2014;Miettinen et al 2018;Ö rstadius et al 2015). -Can be affected by contamination problems, e.g.…”