Palaeotropical origins, boreotropical distribution and increased rates of diversification in a clade of edible ectomycorrhizal mushrooms (Amanita section Caesareae)

Abstract

Aim The geographical distributions of most fungal species are still poorly known; consequently, their origins and historical distributions remain largely understudied. High levels of cryptic diversity, scarce fossil records and poorly sampled regions can explain some of these shortcomings. We extensively sampled an iconic group of edible ectomycorrhizal (EM) fungi, Amanita caesarea and its allies, in order to infer evolutionary patterns on a global scale.Location Worldwide.Methods DNA sequences from three nuclear genes were derived for 120 collections. Divergence times were estimated using fossil calibrations within the Agaricomycetes, followed by more inclusive (A. sect. Caesareae + outgroup) root-recalibrated estimations. Ultrametric trees from beast were used in ancestralarea reconstructions and to infer geodispersal models. They were further used in diversification-rate analyses using maximum-likelihood and Bayesian methods.Results Molecular dating and ancestral-area reconstruction indicated a Palaeotropical origin of A. sect. Caesareae between the Palaeocene and Eocene. Dispersal events to temperate regions in Mediterranean Europe, eastern Australia and North and Central America, occurred mostly during the late Miocene and Pliocene. A boreotropical model was supported as the most likely mode of geodispersal. Diversification rates were significantly higher in the New World than in the Old World. Main conclusionsWe present evidence that this group of edible EM mushrooms was ancestrally Palaeotropical from around the Eocene to the late Miocene, reaching temperate insular and continental areas during the late Miocene and Pliocene. The mode of dispersal is largely consistent with Wolfe's boreotropical hypothesis. We also found that the overall diversification rate has been rather constant, but has increased relatively recently in the New World, possibly as a result of the well-documented Plio-Pleistocene climatic fluctuations.

A new species and four new records of Amanita (Amanitaceae; Basidiomycota) from Northern Thailand

“…Amanita sect. Caesareae (Sánchez-Ramírez et al 2014, 2015, A. sect. Validae series Mappae (Drehmel et al 1999, Hughes et al 2013, Tulloss & Yang 2016d, A. sect.…”

“…Phalloideae . A possible set of four protein-coding loci was proposed by Sánchez-Ramírez et al (2014) and utilized in (Sánchez-Ramírez et al 2015).…”

“…Caesareae") the separation of apparently earlier diverging white-, gray-, and brown-capped taxa from those with brighter colors as in the large sample, multilocus study of Sánchez-Ramírez et al (2014). In the latter study, an isotype of A. rubromarginata was included in the sample.…”

Dimensions of biodiversity in the Earth mycobiome

“…Instead, dispersal limitation seems to have a crucial role in producing the patterns of fungal diversity and community structure that are observed across a range of spatial (see the figure, solid lines (or, where speculative, dashed lines)) and temporal scales (see the figure, y-axis). Evolution of unique bio-geographical assemblages [48][49][50][51] Limited gene flow leads to population differentiation 47,52 Introduction of invasive species disrupts local communities 109 Dispersal limitation may affect species richness and colonization rate for isolated habitats 37 Priority effects increase spatial heterogeneity of assemblages 66,67,68 Dispersal traits influence community assembly 37 Dispersal distance of most spores 37,114,116 Nature Reviews | Microbiology…”

A review on the diversity, phylogeography and population genetics ofAmanitamushrooms

“…A study based on phylogenetic analysis and ancestral area reconstructions suggested that lethal amanitas (Section Palloideae ) probably originated in the palaeotropical zone in the Palaeocene, migrated from the Eurasian continent to North America through the Beringian Land Bridge, and then extended to Central America during Oligocene to Miocene (Cai et al 2014). Similarly, a recent study on edible amanitas (Section Caesareae ) indicated that this group probably originated between the Palaeocene and Eocene in a Palaeotropical setting, most likely in Africa, subsequently dispersed into other temperate and tropical areas during the Miocene and Pliocene (Sánchez-Ramírez et al 2015). The results of these studies are in agreement with the Eurasia-North America disjunct distribution pattern or the Eurasia-North/Central America distribution pattern for some species or sister species in this genus.…”