Host Shift Speciation of the Ectomycorrhizal Genus Suillus (Suillineae, Boletales) and Biogeographic Comparison With Its Host Pinaceae

Abstract

Suillus is a genus of ectomycorrhizal fungi associated almost exclusively with Pinaceae. Lack of sample collections in East Asia and unresolved basal phylogenetic relationships of the genus are the major obstacles for better understanding the Suillus evolution. A resolved phylogeny of Suillus representing global diversity was achieved by sequencing multiple nuclear ribosomal and protein coding genes and extensive samples collected in East Asia. Fungal fossils are extremely rare, and the Eocene ectomycorrhizal symbiosis (ECM) fossil of Pinus root has been widely used for calibration. This study explored an alternative calibration scenario of the ECM fossil for controversy. Ancestral host associations of Suillus were estimated by maximum likelihood and Bayesian Markov chain Monte Carlo (MCMC) analyses, inferred from current host information from root tips and field observation. Host shift speciation explains the diversification of Suillus major clades. The three basal subgenera of Suillus were inferred to be associated with Larix, and diverged in early Eocene or Upper Cretaceous. In the early Oligocene or Paleocene, subgenus Suillus diverged and switched host to Pinus subgenus Strobus, and then switched to subgenus Pinus four times. Suillus subgenus Douglasii switched host from Larix to Pseudotsuga in Oligocene or Eocene. Increased species diversity occurred in subgenus Suillus after it switched host to Pinus but no associated speciation rate shifts were detected. Ancestral biogeographic distributions of Suillus and Pinaceae were estimated under the Dispersal Extinction Cladogenesis (DEC) model. Ancestral distribution patterns of Suillus and Pinaceae are related but generally discordant. Dispersals between Eurasia and North America explain the prevalence of disjunct Suillus taxa.

Soil nutrients and plant diversity affect ectomycorrhizal fungal community structure and functional traits across three subalpine coniferous forests

“…Similar findings were reported by Courty et al (2007) where Lactarius quietus were associated with oak and Suillus sp. with Pinaceae ( Zhang et al, 2022 ). In other study, some common EMF ( Cenococcum geophilum ) depicted wide host range ( Yang et al, 2019 ).…”

Suillus: an emerging model for the study of ectomycorrhizal ecology and evolution

“…To date, there are 112 species of Suillus recognized as valid in the Catalog of Life Database (https://www.catalogueoflife.org/), a number we expect to increase over the coming decade, particularly as new taxa are characterized from understudied areas such as Asia and the Indian subcontinent (Nguyen et al ., 2016b). The Suillus phylogeny is broadly divided into three to five major phylogenetic sections and grouped into corresponding subgenera, including Boletinus , Spectabilis , Larigini , Douglasii , and Suillus (Zhang et al ., 2022). However, this intrageneric classification has not been formally recognized and the exact number of subgenera remains controversial.…”

“…The most significant diversification in the genus occurred during the switch onto Pinus , and it is within this Pinus ‐associated lineage that we find evidence for the active divergence of species complexes. However, the pattern of host switching within Pinus (especially between the host subgenera Pinus and Strobus ) is convoluted and not yet fully resolved (Zhang et al ., 2022). We find notable cases of ongoing evolution associated with host‐switching across the genus, both in clades that are actively diverging and in those that appear relatively stable.…”

“…Suillus diverged from other suilloid fungi between 40.2 and 71.1 million years ago (Ma) (Lepage et al, 1997;Zhang et al, 2022;Fig. 4).…”

“…Both amateur and professional mycologists alike have long targeted the collection of charismatic Suillus mushrooms, with over 46 000 vouchered specimens currently digitized in the MyCoPortal collections database (https://www.mycoportal.org/) and over 62 000 observations of Suillus currently in iNaturalist (https://www.inaturalist.org/). Vouchered collections have facilitated phylogenetic reclassifications across the genus (Nguyen et al ., 2016b), illuminated the association between species diversification and host shifts (Zhang et al ., 2022), clarified species rarity (Kennedy et al ., 2020), and helped to identify the biotic and abiotic factors facilitating range shifts and invasion potential (Pietras et al ., 2018). The collection of Suillus fruit bodies is the first step to obtaining pure cultures, spores for use in bioassays, and preserved specimens for morphological studies or new species descriptions.…”