The saprotrophic Pleurotus ostreatus species complex: late Eocene origin in East Asia, multiple dispersal, and complex speciation

Abstract

The Pleurotus ostreatus species complex is saprotrophic and of significant economic and ecological importance. However, species delimitation has long been problematic because of phenotypic plasticity and morphological stasis. In addition, the evolutionary history is poorly understood due to limited sampling and insufficient gene fragments employed for phylogenetic analyses. Comprehensive sampling from Asia, Europe, North and South America and Africa was used to run phylogenetic analyses of the P. ostreatus species complex based on 40 nuclear single-copy orthologous genes using maximum likelihood and Bayesian inference analyses. Here, we present a robust phylogeny of the P. ostreatus species complex, fully resolved from the deepest nodes to species level. The P. ostreatus species complex was strongly supported as monophyletic, and 20 phylogenetic species were recognized, with seven putatively new species. Data from our molecular clock analyses suggested that divergence of the genus Pleurotus probably occurred in the late Jurassic, while the most recent common ancestor of the P. ostreatus species complex diversified about 39 Ma in East Asia. Species of the P. ostreatus complex might migrate from the East Asia into North America across the North Atlantic Land Bridge or the Bering Land Bridge at different times during the late Oligocene, late Miocene and late Pliocene, and then diversified in the Old and New Worlds simultaneously through multiple dispersal and vicariance events. The dispersal from East Asia to South America in the middle Oligocene was probably achieved by a long-distance dispersal event. Intensification of aridity and climate cooling events in the late Miocene and Quaternary glacial cycling probably had a significant influence on diversification patterns of the complex. The disjunctions among East Asia, Europe, North America and Africa within Clade IIc are hypothesized to be a result of allopatric speciation. Substrate transitions to Apiaceae probably occurred no earlier than 6 Ma. Biogeographic analyses suggested that the global cooling of the late Eocene, intensification of aridity caused by rapid uplift of the QTP and retreat of the Tethys Sea in the late Miocene, climate cooling events in Quaternary glacial cycling, and substrate transitions have contributed jointly to diversification of the species complex.

Phylogeny, Divergence Time Estimation and Biogeography of the Genus Onnia (Basidiomycota, Hymenochaetaceae)

“…Biogeographic studies of macrofungi have been very successful for ectomycorrhizal fungi, such as Amanita (see Sánchez-Ramírez et al, 2015;Truong et al, 2017), saprotrophic Lentinula (see Hibbett et al, 1998), and pathogenic fungi, e.g., Heterobasidion (Chen et al, 2015) based on molecular analyses. Our results suggest that the species distribution of Onnia has a distinct biogeographical pattern, similar to other wood-decaying fungi (Sato et al, 2017;Han et al, 2018;Li et al, 2020). Species of Onnia appear to have originated in Asia, especially in the Hengduan-Himalayan region which is a global biodiversity hotspot, and this conclusion supports previous studies on the origination of wood-decaying fungi (Song et al, 2016;Li et al, 2020;Wang X. W. et al, 2022).…”

“…Our results suggest that the species distribution of Onnia has a distinct biogeographical pattern, similar to other wood-decaying fungi (Sato et al, 2017;Han et al, 2018;Li et al, 2020). Species of Onnia appear to have originated in Asia, especially in the Hengduan-Himalayan region which is a global biodiversity hotspot, and this conclusion supports previous studies on the origination of wood-decaying fungi (Song et al, 2016;Li et al, 2020;Wang X. W. et al, 2022). Three species, O. himalayana, O. tibetica, and O. tomentosa, occur in the Hengduan-Himalayan region.…”

“…Smith et al (2004) and Berbee and Taylor (2010) representing a minimum age of 125 Mya for Hymenochaetaceae. Meanwhile, the molecular dating studies of macrofungi widely pay attention to ectomycorrhizal fungi, saprotrophic fungi, and pathogenic fungi (Hibbett and Matheny, 2009;Chen et al, 2015;Song et al, 2016;Truong et al, 2017;Li et al, 2020;Liu et al, 2022;Wang X. W. et al, 2022). A series of studies related to the divergence time of pathogenic fungi, such as Coniferiporia L.W.…”

“…In the study of biogeography, the evolution of species is an important issue requiring reconstructing the origin, speciation, and distribution patterns of organisms (Page, 2003;Seehausen et al, 2014). To date, macrofungi, especially wood-inhabiting fungi, being closely interacted with host plants, are an interesting subject in biogeographic research (Chen et al, 2015;Song et al, 2016;Varga et al, 2019;Li et al, 2020;Wang X. W. et al, 2022). For example, the ancestral geographic origin analyses suggested that coniferous pathogenic fungal Coniferiporia originated in Asia and then extend to Europe and North America (Wang X. W. et al, 2022).…”

Taxonomy, Phylogenetic and Ancestral Area Reconstruction in Phyllachora, with Four Novel Species from Northwestern China

“…Ancestor state reconstruction currently requires inferring phenotypes of ancestral species using observations from present-day species [ 55 , 56 ]. As new classical and molecular methods for identifying fungi continue to develop [ 57 ], ancestor state reconstruction analysis of fungal taxonomy is at the forefront of a new trend [ 8 , 58 , 59 , 60 ]. Future studies on species diversity and evolution of Phyllachora species require more extensive sampling and high-quality molecular data.…”