Biogeographic history of a large clade of ectomycorrhizal fungi, the Russulaceae, in the Neotropics and adjacent regions

Abstract

The biogeography of neotropical fungi remains poorly understood. Here, we reconstruct the origins and diversification of neotropical lineages in one of the largest clades of ectomycorrhizal fungi in the globally widespread family Russulaceae.We inferred a supertree of 3285 operational taxonomic units, representing worldwide internal transcribed spacer sequences. We reconstructed biogeographic history and diversification and identified lineages in the Neotropics and adjacent Patagonia.The ectomycorrhizal Russulaceae have a tropical African origin. The oldest lineages in tropical South America, most with African sister groups, date to the mid-Eocene, possibly coinciding with a boreotropical migration corridor. There were several transatlantic dispersal events from Africa more recently. Andean and Central American lineages mostly have northtemperate origins and are associated with North Andean uplift and the general north-south biotic interchange across the Panama isthmus, respectively. Patagonian lineages have Australasian affinities. Diversification rates in tropical South America and other tropical areas are lower than in temperate areas.Neotropical Russulaceae have multiple biogeographic origins since the mid-Eocene involving dispersal and co-migration. Discontinuous distributions of host plants may explain low diversification rates of tropical lowland ectomycorrhizal fungi. Deeply diverging neotropical fungal lineages need to be better documented.

Phylogenomics, biogeography, and trait evolution of the Boletaceae (Boletales, Agaricomycetes, Basidiomycota)

“…Subsequent diversification was likely facilitated by vicariance events correlated with continental drift and possible long-distance dispersal. These results support the emerging consensus that numerous lineages of ECM fungi originated in Gondwana or more recently in paleotropical regions (Hosaka et al 2008, Matheny et al 2009, Dentinger et al 2010, Ryberg & Matheny 2011, Kennedy et al 2012, Sanchez-Ramirez et al 2015, Han et al 2018Hackel et al 2022;Codjia et al 2023).…”

“…Subsequent divergence was likely facilitated by continental drift-based vicariance events and possible long-distance dispersals. Other recent studies have shown that lineages of ECM fungi originated in Gondwana or more recently in paleotropical regions (Hosaka et al 2008, Matheny et al 2009, Dentinger et al 2010, Ryberg and Matheny 2011, Kennedy et al 2012, Sanchez-Ramirez et al 2015, Han et al 2018; Hackel et al 2022; Codjia et al 2023). Phytogeographic endemism was implied with our biogeographic reconstruction.…”

“…Long-distance dispersals may have occurred, albeit rarely. While long-distance dispersal is demonstrably possible in the Boletaceae and other ECM lineages the likelihood of its frequent occurrence is low (Geml et al 2012; Hackel et al 2022; Tremble et al 2022). Most basidiospores do not travel far from the parental sporocarp (Galante et al 2011), and the probability of two airborne basidiospores landing in close-enough proximity to mate is negatively correlated with increasing distance from sporocarps (Peay et al 2012; Golan and Pringle 2017).…”

“…It follows that long-distance dispersals may have occurred, albeit rarely. While long-distance dispersal is demonstrably possible in the Boletaceae (Tremble et al 2022), and has been documented in diverse ECM lineages (Gelm et al 2012; Hackel et al 2022), it is obvious that successful long-distance dispersal is difficult. Most basidiospores do not travel far from the sporocarp (Galante et al 2011), and the probability of two basidiospores landing in proximity to mate becomes highly unlikely with increasing distance from sporocarps (Peay et al 2012; Golan and Pringle 2017).…”

Two new Asian species of Russula sect. Ingratae with unique basidiospore features for subg. Heterophyllidiae

“…Russula Pers. has a nearly cosmopolitan distribution with species occurring from tropical to arctic ecosystems where they form symbiotic relationships with a diversity of plant species in broad-leaved and coniferous forests, scrubland and meadows (Adamčík et al 2019;Hackel et al 2022). Agaricoid members of this genus frequently have a colourful fragile pileus, amyloid spore ornamentation, a brittle context with abundant sphaerocytes and presence of gloeoplerous elements in various parts of their fruiting bodies, but they lack a branching lactiferous system ending in pseudocystidia at the basidiome surface as in the genera Lactarius Pers.…”