Into and out of the tropics: global diversification patterns in a hyperdiverse clade of ectomycorrhizal fungi

Abstract

Ectomycorrhizal (ECM) fungi, symbiotic mutualists of many dominant tree and shrub species, exhibit a biogeographic pattern counter to the established latitudinal diversity gradient of most macroflora and fauna. However, an evolutionary basis for this pattern has not been explicitly tested in a diverse lineage. In this study, we reconstructed a mega-phylogeny of a cosmopolitan and hyperdiverse genus of ECM fungi, Russula, sampling from annotated collections and utilizing publically available sequences deposited in GenBank. Metadata from molecular operational taxonomic unit cluster sets were examined to infer the distribution and plant association of the genus. This allowed us to test for differences in patterns of diversification between tropical and extratropical taxa, as well as how their associations with different plant lineages may be a driver of diversification. Results show that Russula is most species-rich at temperate latitudes and ancestral state reconstruction shows that the genus initially diversified in temperate areas. Migration into and out of the tropics characterizes the early evolution of the genus, and these transitions have been frequent since this time. We propose the 'generalized diversification rate' hypothesis to explain the reversed latitudinal diversity gradient pattern in Russula as we detect a higher net diversification rate in extratropical lineages. Patterns of diversification with plant associates support host switching and host expansion as driving diversification, with a higher diversification rate in lineages associated with Pinaceae and frequent transitions to association with angiosperms.

Host shifts enhance diversification of ectomycorrhizal fungi: diversification rate analysis of the ectomycorrhizal fungal genera Strobilomyces and Afroboletus with an 80‐gene phylogeny

“…Although caution is still needed when generalizing the present scenario of evolutionary diversification to other ECM fungal taxa, the scenario may account for patterns in the present global biodiversity of ECM fungi (i.e. a moderate reduction of species richness towards lower latitudes; Tedersoo & Nara, ; Tedersoo et al ., ), which is largely in agreement with previous studies (Sánchez‐Ramírez et al ., ; Looney et al ., ). By applying the methodological and analytical procedures shown in the present study to various ECM taxa, we will be able to test generality in the evolutionary diversification patterns driven by ECM symbioses.…”

“…Our results are partially in agreement with a previous report which suggests host shift‐mediated (i.e. host shift between angiosperms and Pinaceae) diversification of the ECM fungal genus Russula (Looney et al ., ), but they provide a more precise picture of the diversification history of ECM fungi. We consider that an acquisition of novel host plants in Eurasian temperate regions presumably caused the subsequent expansion of geographical ranges that could have led to accelerated diversification of Strobilomyces–Afroboletus , similar to indirect mechanisms of coevolutionary diversification, as suggested in other mutualistic interactions (Payne & Finnegan, ; Gómez & Verdú, ; Joy, ; Althoff et al ., ; Hembry et al ., ).…”

Russulaceae: a new genomic dataset to study ecosystem function and evolutionary diversification of ectomycorrhizal fungi with their tree associates

“…The Russulaceae also comprises one of the most species‐diverse lineages of ectomycorrhizal fungi with an estimated number of some 2000 accepted species (Kirk, ). Given the relatively recent evolutionary age of the group, with a crown group origin of around 55 Myr ago (Ma) (Looney et al ., ), only three other ectomycorrhizal lineages – Cortinarius , Boletaceae and Thelephoraceae – can be said to have gone through as rapid diversification as Russulaceae. A cluster of about five described corticioid species belonging to the genera Boidinia , Pseudoxenasma and Gloeopeniophorella have been recovered as part of Russulaceae (Larsson & Larsson, ).…”

The origin and evolution of mycorrhizal symbioses: from palaeomycology to phylogenomics

“…This paradox may be explained if basal lineages were preferentially conserved in the tropics, whereas a more recent Late Paleogene–Neogene diversification was driven by global cooling and the spread of temperate biomes (Selosse & Le Tacon, ). This diversification of ECMs out of the tropics is exemplified by plant host switching from tropical to temperate observed in various fungi (Looney et al ., ; Sato et al ., ). Other corroborating evidence comes from phylogenetic studies of particular clades.…”