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Towards standardizing taxonomic ranks using divergence times – a case study for reconstruction of the Agaricus taxonomic system

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Abstract

The recognition of taxonomic ranks in the Linnean classification system is largely arbitrary. Some authors have proposed the use of divergence time as a universally standardized criterion. Agaricus (Agaricaceae, Agaricales) is a mushroom genus that contains many species of high commercial value. Recent studies using ITS sequence data discovered 11 new phylogenetic lineages within the genus, however their taxonomic ranks were uncertain due to the lack of criteria to define them within traditional taxonomy. In this study, we analyzed ITS sequence data from 745 collections (nearly 600 being newly generated) including 86 from type specimens of previously recognized subgenera and sections. Many monophyletic groups were recognized, but most basal relationships were unresolved. One hundred and fourteen representatives of the identified ITS clades were selected in order to produce a multi-gene phylogeny based on combined LSU, tef-1α, and rpb2 sequence data. Divergence times within the multi-gene phylogeny were estimated using BEAST v1.8. Based on phylogenetic relationships and with respect to morphology, we propose a revised taxonomic system for Agaricus that considers divergence time as a standardized criterion for establishing taxonomic ranks. We propose to segregate Agaricus into five subgenera and 20 sections. Subgenus Pseudochitonia is substantially emended; circumscription of the subgenera Agaricus and Flavoagaricus is restricted to taxa of sections Agaricus and Arvenses, respectively; and two new subgenera (Minores and Spissicaules) are introduced. Within Pseudochitonia, sections Bivelares, Brunneopicti, Chitonioides, Nigrobrunnescentes, Sanguinolenti and Xanthodermatei are maintained, but the latter two are reduced because we raise subsection Bohusia to sectional rank and a clade within section Xanthodermatei is formally introduced as section Hondenses; and sections Rubricosi, Crassispori, Flocculenti, and Amoeni are introduced. Section Laeticolores is placed in the subgenus Minores and sections Rarolentes and Subrutilescentes are placed in the subgenus Spissicaules. Twenty-two new species belonging to various sections are described. This work exemplifies that ITS data, while useful at lower taxonomic levels (i.e., detection of species and species groups), are of limited value for inferring deeper phylogenetic relationships. Finally, we suggest that the establishment of a standardized taxonomic system based on divergence times could result in a more objective, and biologically more meaningful, taxonomic ranking of fungi.

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Acknowledgments

This work was supported by grants from the National Natural Science Foundation of China to RLZ (Project IDs 31000013, 31360014 and 31470152), the Thailand Research Fund to KDH (grant BRG 5580009), and the Natural Sciences and Engineering Research Council of Canada and the ROM Governors to JMM. Dr. Richard Kerrigan made valuable comments and suggestions to improve this paper. Drs. Wang Xiang-Hua, Su Hong-Yang, István Nagy, Samantha C. Karunarathna and Phongeun Sysouphanthong lended specimens.

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Authors and Affiliations

  1. State Key Laboratory of Mycology, Institute of Microbiology, Chinese Academy of Sciences, Beijing, 100101, China

    Rui-Lin Zhao & Guo-Jie Li

  2. Institute of Microbiology and Beijing Key Laboratory for Forest Pest Control, Beijing Forestry University, Beijing, 100083, China

    Jun-Liang Zhou

  3. Center of Excellence in Fungal Research, Mae Fah Luang University, Chiang Rai, 57100, Thailand

    Jie Chen & Kevin D Hyde

  4. School of Science, Mae Fah Luang University, Chiang Rai, 57100, Thailand

    Jie Chen & Kevin D Hyde

  5. Department of Natural History, Royal Ontario Museum, Toronto, ON, M5S 2C6, Canada

    Simona Margaritescu, Santiago Sánchez-Ramírez & Jean-Marc Moncalvo

  6. Department of Ecology and Evolutionary Biology, University of Toronto, Toronto, ON, M5S 3B2, Canada

    Santiago Sánchez-Ramírez & Jean-Marc Moncalvo

  7. Key Laboratory of Economic Plants and Biotechnology, Kunming Institute of Botany, Chinese Academy of Sciences, 132 Lanhei Road, Kunming, 650201, China

    Kevin D Hyde

  8. INRA-UR1264, Mycologie et Sécurité des Aliments, CS 20032, 33882, Villenave d’Ornon cedex, France

    Philippe Callac

  9. Avda. Padre Claret n°7, 5°G, 09400, Aranda de Duero, Burgos, Spain

    Luis A. Parra

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  1. Rui-Lin Zhao
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Zhao, RL., Zhou, JL., Chen, J. et al. Towards standardizing taxonomic ranks using divergence times – a case study for reconstruction of the Agaricus taxonomic system. Fungal Diversity 78, 239–292 (2016). https://doi.org/10.1007/s13225-016-0357-x

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