Tropic origins, a dispersal model for saprotrophic mushrooms in Agaricus section Minores with descriptions of sixteen new species

Agaricus section Minores contains the richest species diversity within the genus. Its Phylogeny is firstly presented by a Maximum Likelihood tree generated through DNA sequences from four gene regions of 91 species. Furthermore, a molecular dating analysis is conducted used those sequences, and it provided the divergence times of the clades within section Minores. Study showed section Minores has a tropical origin. Four main dispersal routes are proposed: (1) species from South Asia migrated through the Tibetan Plateau and reached Europe ca. 9–13 Ma; (2) species from out of South Asia dispersed to Europe in the earlier time of ca. 22 Ma; (3) species from South Asia dispersed through North Asia to Alaska, and reached West America around ca. 9 Ma; and (4) species from South Asia dispersed south and reached Oceania by at least three invading events about ca. 9, 12 and 16–18 Ma respectively. Those routes excepting the second route coincide with those of ectomycorrhizal mushrooms. To know whether the second route existed in the saprotrophic mushrooms requires further studies, and the fourth route may explain why the secotioid species occurring in Australia are morphologically similar but cluster in different phylogenetic clades. This study also demonstrates a great biodiversity of A. section Minores in China. Sixteen new species and three new records are introduced from China with morphological descriptions, illustrations, color photographs and phylogenetic analyses.

[1]  R. Halling Ectomycorrhizae: Co-Evolution, Significance, and Biogeography , 2001 .

[2]  Zhao Rui-Lin,et al.  A new species of Agaricus section Minores from China , 2015, Mycology.

[3]  D. J. Lodge,et al.  Out of the Palaeotropics? Historical biogeography and diversification of the cosmopolitan ectomycorrhizal mushroom family Inocybaceae , 2009 .

[4]  A. Bawadekji,et al.  First Report of Agaricus aridicola in Saudi Arabia and Ecological Notes on Agaricus bisporus , 2015 .

[5]  S. Redhead A biogeographical overview of the Canadian mushroom flora , 1989 .

[6]  J. Geml,et al.  Molecular diversity assessment of arctic and boreal Agaricus taxa , 2008, Mycologia.

[7]  H. Thiers The secotioid syndrome , 1984 .

[8]  K. Hyde,et al.  Towards standardizing taxonomic ranks using divergence times – a case study for reconstruction of the Agaricus taxonomic system , 2016, Fungal Diversity.

[9]  K. Hyde,et al.  Fungal diversity notes 1–110: taxonomic and phylogenetic contributions to fungal species , 2015, Fungal Diversity.

[10]  G. Liti,et al.  Surprisingly diverged populations of Saccharomyces cerevisiae in natural environments remote from human activity , 2012, Molecular ecology.

[11]  Jaa Nylander,et al.  MrModeltest 2.2. Program Distributed by the Author , 2004 .

[12]  R. Stockey,et al.  Cretaceous and Eocene poroid hymenophores from Vancouver Island, British Columbia , 2004, Mycologia.

[13]  B. Cui,et al.  Phylogeny and biogeography of the remarkable genus Bondarzewia (Basidiomycota, Russulales) , 2016, Scientific Reports.

[14]  Ronald,et al.  Megacollybia ( Agaricales ) , 2008 .

[15]  Andrew W. Wilson,et al.  Diversity and evolution of ectomycorrhizal host associations in the Sclerodermatineae (Boletales, Basidiomycota). , 2012, The New phytologist.

[16]  J. Geml,et al.  Evidence for strong inter- and intracontinental phylogeographic structure in Amanita muscaria, a wind-dispersed ectomycorrhizal basidiomycete. , 2008, Molecular phylogenetics and evolution.

[17]  N. Lennon,et al.  An arctic community of symbiotic fungi assembled by long‐distance dispersers: phylogenetic diversity of ectomycorrhizal basidiomycetes in Svalbard based on soil and sporocarp DNA , 2012 .

[18]  H. Ashton Ainsworth and Bisby's Dictionary of the Fungi (10th edition) , 2009 .

[19]  F. Martin,et al.  Genetic diversity of Pisolithus in New Zealand indicates multiple long-distance dispersal from Australia. , 2003, The New phytologist.

[20]  K. Hyde,et al.  Mycosphere Essay 8: A review of genus Agaricus in tropical and humid subtropical regions of Asia , 2016 .

[21]  R. Kerrigan,et al.  New and rare taxa in Agaricus section Bivelares (Duploannulati) , 2008, Mycologia.

[22]  T. Henkel,et al.  Molecular phylogenetics of porcini mushrooms (Boletus section Boletus). , 2010, Molecular phylogenetics and evolution.

[23]  John P. Huelsenbeck,et al.  MrBayes 3: Bayesian phylogenetic inference under mixed models , 2003, Bioinform..

[24]  D. Geiser,et al.  Molecular evolution of Agaricus species based on ITS and LSU rDNA sequences , 2004, Mycological Progress.

[25]  A. Mitchell,et al.  PHYLOGENETIC RELATIONSHIPS OF AGARICUS SPECIES BASED ON ITS-2 AND 28S RIBOSOMAL DNA SEQUENCES , 1999 .

[26]  S. Sánchez-Ramírez,et al.  Palaeotropical origins, boreotropical distribution and increased rates of diversification in a clade of edible ectomycorrhizal mushrooms (Amanita section Caesareae) , 2015 .

[27]  K. Hyde,et al.  Study in Agaricus subgenus Minores and allied clades reveals a new American subgenus and contrasting phylogenetic patterns in Europe and Greater Mekong Subregion , 2017, Persoonia.

[28]  K. Hyde,et al.  Major clades in tropical Agaricus , 2011, Fungal Diversity.

[29]  T. Lebel,et al.  Sequestrate species of Agaricus and Macrolepiota from Australia: new species and combinations and their position in a calibrated phylogeny , 2012, Mycologia.

[30]  Z. Yang,et al.  Molecular phylogeny of eastern Asian species of Amanita (Agaricales, Basidiomycota): taxonomic and biogeographic implications , 2004 .

[31]  R. Vilgalys,et al.  Assessing biogeographic relationships between North American and Chinese macrofungi , 2001 .

[32]  M. Suchard,et al.  Bayesian Phylogenetics with BEAUti and the BEAST 1.7 , 2012, Molecular biology and evolution.

[33]  Andrew W. Wilson,et al.  Contributions of rpb2 and tef1 to the phylogeny of mushrooms and allies (Basidiomycota, Fungi). , 2007, Molecular phylogenetics and evolution.

[34]  S. Ho,et al.  Relaxed Phylogenetics and Dating with Confidence , 2006, PLoS biology.

[35]  K. Hyde,et al.  Agaricus megalosporus: A New Species in Section Minores , 2012 .

[36]  Robert C. Edgar,et al.  MUSCLE: multiple sequence alignment with high accuracy and high throughput. , 2004, Nucleic acids research.

[37]  Chengshu Wang,et al.  Phylogeography and evolution of a fungal–insect association on the Tibetan Plateau , 2014, Molecular ecology.

[38]  F. Bai,et al.  Evidence for a Far East Asian origin of lager beer yeast , 2014, Current Biology.

[39]  Rc Dai Characterization of four species including one new species of Agaricus subgenus Spissicaules from Eastern China , 2016 .

[40]  D. L. Largent,et al.  How to identify mushrooms to genus , 1973 .

[41]  New species and distinctive geographical divergences of the genus Sparassis (Basidiomycota): evidence from morphological and molecular data , 2013, Mycological Progress.

[42]  V. K. Bhatt,et al.  Fungal diversity notes 253–366: taxonomic and phylogenetic contributions to fungal taxa , 2016, Fungal diversity.

[43]  K. Hyde,et al.  Agaricus section Brunneopicti: a phylogenetic reconstruction with descriptions of four new taxa , 2015 .

[44]  D. Silvestro,et al.  raxmlGUI: a graphical front-end for RAxML , 2011, Organisms Diversity & Evolution.

[45]  H. Nusbaum,et al.  Beringian origins and cryptic speciation events in the fly agaric (Amanita muscaria) , 2005, Molecular ecology.

[46]  T. White Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics , 1990 .

[47]  P. Heinemann Quelques Agaricus de Nouvelle-Zelande , 1974 .

[48]  R. Vilgalys,et al.  Multilocus sequence typing suggests the chytrid pathogen of amphibians is a recently emerged clone , 2003, Molecular ecology.

[49]  ZHU-LIANG Yang,et al.  Phylogenetic and biogeographic relationships of Chroogomphus species as inferred from molecular and morphological data , 2009 .

[50]  ZHU-LIANG Yang,et al.  DNA Sequence Analyses Reveal Abundant Diversity, Endemism and Evidence for Asian Origin of the Porcini Mushrooms , 2012, PloS one.

[51]  M. Donoghue,et al.  Fossil mushrooms from Miocene and Cretaceous ambers and the evolution of Homobasidiomycetes. , 1997, American journal of botany.

[52]  T. Lebel Two new species of sequestrate Agaricus (section Minores) from Australia , 2012, Mycological Progress.

[53]  R. Singer The Agaricales in modern taxonomy , 1949 .

[54]  K. Hyde,et al.  Inter- and intra stream variation of lignicolous freshwater fungi in tropical Australia , 2006 .

[55]  D. Bryant,et al.  A general comparison of relaxed molecular clock models. , 2007, Molecular biology and evolution.