Evolution of ectomycorrhizas as a driver of diversification and biogeographic patterns in the model mycorrhizal mushroom genus Laccaria.

Andrew W Wilson,Kentaro Hosaka,Gregory M Mueller

doi:10.1111/nph.14270

Abstract

Summary A systematic and evolutionary ecology study of the model ectomycorrhizal (ECM) genus Laccaria was performed using herbarium material and field collections from over 30 countries covering its known geographic range.A four‐gene (nrITS, 28S, RPB2, EF1α) nucleotide sequence dataset consisting of 232 Laccaria specimens was analyzed phylogenetically. The resulting Global Laccaria dataset was used for molecular dating and estimating diversification rates in the genus. Stable isotope analysis of carbon and nitrogen was used to evaluate the origin of Laccaria's ECM ecology.In all, 116 Laccaria molecular species were identified, resulting in a near 50% increase in its known diversity, including the new species described herein: Laccaria ambigua. Molecular dating indicates that the most recent common ancestor to Laccaria existed in the early Paleocene (56–66 million yr ago), probably in Australasia. At this time, Laccaria split into two lineages: one represented by the new species L. ambigua, and the other reflecting a large shift in diversification that resulted in the remainder of Laccaria. L. ambigua shows a different isotopic profile than all other Laccaria species.Isotopes and diversification results suggest that the evolution of the ECM ecology was a key innovation in the evolution of Laccaria. Diversification shifts associated with Laccaria's dispersal to the northern hemisphere are attributed to adaptations to new ecological niches.

Highlights

Ectomycorrhizal (ECM) fungi are symbiotic associates of dominant plant species found in most forest ecosystems (Smith & Read, 2008)
The current study provides a thorough evaluation of Laccaria’s systematic diversity and is one of the most taxonomically comprehensive studies of any group of Agaricomycetes
The results have identified > 50% more Laccaria species, the cryptic nature of fungi makes it likely that undescribed taxa remain to be discovered

Summary

Introduction

Ectomycorrhizal (ECM) fungi are symbiotic associates of dominant plant species found in most forest ecosystems (Smith & Read, 2008). While arbuscular mycorrhizal fungi associate with the greater proportion of terrestrial plant species (> 70% vs 2%)(Brundrett, 2009), the diversity of ECM fungal species is much greater (> 7000 vs 230) (Rinaldi et al, 2008). This diversity is partly the result of as many as 80 independent evolutions of the ECM ecology among Agaricomycetes (mushrooms and allies) (Tedersoo & Smith, 2013), but understanding how this ecology functions as a driver of diversification in fungal lineages continues as a subject of interest in the study of ECM fungi (Bonito et al, 2013; Sanchez-Ramırez et al, 2015). There is currently no evidence that directly correlates a shift in fungal diversification rates with a switch to the ECM ecology

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Discussion

Conclusion