Systematic Biology Advance Access originally published online on June 4, 2009
Systematic Biology 2009 58(2):224-239; doi:10.1093/sysbio/syp020
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© Society of Systematic Biologists
The Ascomycota Tree of Life: A Phylum-wide Phylogeny Clarifies the Origin and Evolution of Fundamental Reproductive and Ecological Traits
1 Department of Botany and Plant Pathology, Oregon State University, Corvallis, OR 97331, USA
2 Department of Ecology and Evolutionary Biology, Yale University, 165 Prospect Street, New Haven, CT 06520, USA
3 Department of Biology, Duke University, Durham, NC 27708, USA
4 Swiss Federal Research Station for Plant Production of Changins (RAC), PO Box 254, CH-1260 Nyon 1, Switzerland
5 Biology Department, Clark University, Worcester, MA 01610, USA
6 Department of Ecology and Evolutionary Biology, University of Tennessee, 569 Dabney Hall, Knoxville, TN 37996, USA
7 Molecular Phylogenetics, FB Biologie, 13/276, TU Kaiserslautern, Postfach 3049, 67653 Kaiserslautern, Germany
8 Centraalbureau voor Schimmelcultures, Fungal Biodiversity Centre, PO Box 85167, 3508 AD, Utrecht, the Netherlands
9 Department of Zoology, Copenhagen University Institute for Ecology, Thorvaldsensvej 40, 1871 Frederiksberg, Copenhagen, Denmark
10 Department of Organismic and Evolutionary Biology, Harvard University, 22 Divinity Avenue, Cambridge, MA 021 38, USA
11 Forestry & Agricultural Biotechnology Institute, University of Pretoria, Pretoria 0002, South Africa
12 Adviesbureau voor Bryologie en Lichenologie, G.v.d.Veenstraat 107, NL-3762 XK Soest, the Netherlands
13 Mycology Program, American Type Culture Collection, 10801 University Boulevard, Manassas, VA 20110, USA
14 Department of Biological Sciences, Louisiana State University, Baton Rouge, LA 70803, USA
15 Section of Integrative Biology, University of Texas, Austin, TX 78712, USA
16 Institute of Biological, Environmental and Rural Sciences, Aberystwyth University, Aberystwyth, Ceredigion SY23 3DD, Wales, UK
17 United States Department of Agriculture, Agricultural Research Service, Systematic Mycology and Microbiology Laboratory, 10300 Baltimore Avenue, Beltsville, MD 20705, USA
18 Department of Botany, The Field Museum, 1400 South Lake Shore Drive, Chicago, IL 60605, USA
19 Fachbereich Biologie, Abteilung Pflanzenökologie und Systematik, 67653 Kaiserslautern, Germany
20 Musée National d'Histoire Naturelle, L-2160 Luxembourg, Luxembourg
21 Department of Cryptogamy (BT), National Botanical Garden of Belgium, Domaine de Bouchout, B-1860 Meise, Belgium
22 Department of Plant Pathology, Pennsylvania State University, University Park, PA 16802, USA
23 Department of Botany, National Museum of Nature and Science, Tsukuba-shi, Ibaraki 305-0005, Japan
24 University of California, Kearney Agricultural Center, 9240 South Riverbend Avenue, Parlier, CA 93648, USA
25 Institute of Marine Sciences, University of North Carolina at Chapel Hill, Morehead City, NC 28557, USA
26 Department of Plant Pathology, University of Stellenbosch, Private Bag X1, Matieland 7602, South Africa
27 Microbial Genomics Research Unit, National Center for Agricultural Utilization Research, U.S. Department of Agriculture, Agricultural Research, Service, Peoria, IL 61604, USA
28 Botanischer Garten und Botanisches Museum Berlin-Dahlem, Freie Universität Berlin, Königin-Luise-Straße, 6-8, D-14195 Berlin, Germany
29 Department of Plant Pathology, Washington State University, Pullman, WA 99164, USA
30 Biodiversity (Mycology and Botany), Agriculture and Agri-Food Canada, Ottawa, Ontario K1A 0C6, Canada
31 TechnoSuruga Laboratory Co. Ltd., Tokyo Office, Chiyoda-ku, Tokyo 101-0052, Japan
32 27 Hillcrest Park, Toronto, Ontario M4X 1E8, Canada
33 Department of Biology, Brandon University, Brandon, Manitoba R7A 6A9, Canada
34 Herbarium PDD, Landcare Research, Private Bag 92170, Auckland, New Zealand
35 Botanical Museum, Finnish Museum of Natural History, PO Box 7, FI-00014 University of Helsinki, Finland
36 Institute of Phytopathology and Applied Zoology, University of Giessen, D-35392 Giessen, Germany
37 School of Biology, University of Nottingham, Nottingham NG7 2RD, UK
38 2017 Thure Avenue, St. Paul, Minnesota 55116, USA
39 Department of Cryptogamic Botany, Swedish Museum of Natural History, Box 50007, SE-10405 Stockholm, Sweden
40 Department of Forest Science, Oregon State University, Corvallis, Oregon 97331, USA
41 Royal Botanic Garden Edinburgh, 20A Inverleith Row, Edinburgh, EH3 5LR, UK
42 Plant Protection Department, Agriculture Faculty, University of Tabriz, PO Box: 5166614766, Tabriz, Iran
* Correspondence to be sent to: National Center for Biotechnology Information, National Library of Medicine, National Institutes of Health, 45 Center Drive, Bethesda, MD 20892, USA; E-mail: schoch2{at}mail.nih.gov.
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Abstract |
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We present a 6-gene, 420-species maximum-likelihood phylogeny of Ascomycota, the largest phylum of Fungi. This analysis is the most taxonomically complete to date with species sampled from all 15 currently circumscribed classes. A number of superclass-level nodes that have previously evaded resolution and were unnamed in classifications of the Fungi are resolved for the first time. Based on the 6-gene phylogeny we conducted a phylogenetic informativeness analysis of all 6 genes and a series of ancestral character state reconstructions that focused on morphology of sporocarps, ascus dehiscence, and evolution of nutritional modes and ecologies. A gene-by-gene assessment of phylogenetic informativeness yielded higher levels of informativeness for protein genes (RPB1, RPB2, and TEF1) as compared with the ribosomal genes, which have been the standard bearer in fungal systematics. Our reconstruction of sporocarp characters is consistent with 2 origins for multicellular sexual reproductive structures in Ascomycota, once in the common ancestor of Pezizomycotina and once in the common ancestor of Neolectomycetes. This first report of dual origins of ascomycete sporocarps highlights the complicated nature of assessing homology of morphological traits across Fungi. Furthermore, ancestral reconstruction supports an open sporocarp with an exposed hymenium (apothecium) as the primitive morphology for Pezizomycotina with multiple derivations of the partially (perithecia) or completely enclosed (cleistothecia) sporocarps. Ascus dehiscence is most informative at the class level within Pezizomycotina with most superclass nodes reconstructed equivocally. Character-state reconstructions support a terrestrial, saprobic ecology as ancestral. In contrast to previous studies, these analyses support multiple origins of lichenization events with the loss of lichenization as less frequent and limited to terminal, closely related species.
Keywords: Ancestral character reconstruction; Fungi; large data sets; lichenization; phylogeny
Received April 21, 2008; Revised July 7, 2008; Accepted February 12, 2009