title: Evolution of complex symbiotic relationships in a morphologically derived family of lichen-forming fungi.
abstract: We studied the evolutionary history of the Parmeliaceae (Lecanoromycetes, Ascomycota), one of the largest families of lichen-forming fungi with complex and variable morphologies, also including several lichenicolous fungi. We assembled a six-locus data set including nuclear, mitochondrial and low-copy protein-coding genes from 293 operational taxonomic units (OTUs). The lichenicolous lifestyle originated independently three times in lichenized ancestors within Parmeliaceae, and a new generic name is introduced for one of these fungi. In all cases, the independent origins occurred c. 24 million yr ago. Further, we show that the Paleocene, Eocene and Oligocene were key periods when diversification of major lineages within Parmeliaceae occurred, with subsequent radiations occurring primarily during the Oligocene and Miocene. Our phylogenetic hypothesis supports the independent origin of lichenicolous fungi associated with climatic shifts at the Oligocene-Miocene boundary. Moreover, diversification bursts at different times may be crucial factors driving the diversification of Parmeliaceae. Additionally, our study provides novel insight into evolutionary relationships in this large and diverse family of lichen-forming ascomycetes.
authors: Departamento de Biología Vegetal II, Facultad de Farmacia, Universidad Complutense de Madrid, Plaza de Ramón y Cajal s/n, 28040, Madrid, Spain.
authors: Pradeep K
authors: PK
authors: Divakar
authors: Departamento de Biología Vegetal II, Facultad de Farmacia, Universidad Complutense de Madrid, Plaza de Ramón y Cajal s/n, 28040, Madrid, Spain.
authors: Ana
authors: A
authors: Crespo
authors: Department of Botany, Swedish Museum of Natural History, PO Box 50007, SE-104 05, Stockholm, Sweden.
authors: Mats
authors: M
authors: Wedin
authors: Science & Education, The Field Museum, 1400 S. Lake Shore Drive, Chicago, IL, 60605, USA.
authors: Steven D
authors: SD
authors: Leavitt
authors: Departamento de Biología Vegetal II, Facultad de Farmacia, Universidad Complutense de Madrid, Plaza de Ramón y Cajal s/n, 28040, Madrid, Spain.
authors: David L
authors: DL
authors: Hawksworth
authors: Botanical Museum, Finnish Museum of Natural History, University of Helsinki, PO Box 7, Helsinki, FI-00014, Finland.
authors: Leena
authors: L
authors: Myllys
authors: Department of Botany and Plant Pathology, Oregon State University, Corvallis, OR, 97331-2902, USA.
authors: Bruce
authors: B
authors: McCune
authors: Institute of Ecology & Earth Sciences, University of Tartu, Lai Street 38, Tartu, 51005, Estonia.
authors: Tiina
authors: T
authors: Randlane
authors: Norwegian Institute for Nature Research (NINA), FRAM - High North Research Centre for Climate and the Environment, NO-9296, Tromsø, Norway.
authors: Jarle W
authors: JW
authors: Bjerke
authors: National Museum of Nature and Science, 4-1-1 Amakubo, Tsukuba, Ibaraki, 305-0005, Japan.
authors: Yoshihito
authors: Y
authors: Ohmura
authors: Biodiversity and Climate Research Centre BiK-F, Senckenberganlage 25, 60325, Frankfurt am Main, Germany.|Department of Biological Sciences, Institute of Ecology, Evolution and Diversity, Goethe Universität, Max-von-Laue-Str. 13, 85 D-60438, Frankfurt, Germany.
authors: Imke
authors: I
authors: Schmitt
authors: Departamento de Biología Vegetal II, Facultad de Farmacia, Universidad Complutense de Madrid, Plaza de Ramón y Cajal s/n, 28040, Madrid, Spain.
authors: Carlos G
authors: CG
authors: Boluda
authors: Departamento de Biología Vegetal II, Facultad de Farmacia, Universidad Complutense de Madrid, Plaza de Ramón y Cajal s/n, 28040, Madrid, Spain.
authors: David
authors: D
authors: Alors
authors: Departamento de Biología Vegetal II, Facultad de Farmacia, Universidad Complutense de Madrid, Plaza de Ramón y Cajal s/n, 28040, Madrid, Spain.
authors: Beatriz
authors: B
authors: Roca-Valiente
authors: Departamento de Biología Vegetal II, Facultad de Farmacia, Universidad Complutense de Madrid, Plaza de Ramón y Cajal s/n, 28040, Madrid, Spain.
authors: Ruth
authors: R
authors: Del-Prado
authors: Departamento de Biología Vegetal II, Facultad de Farmacia, Universidad Complutense de Madrid, Plaza de Ramón y Cajal s/n, 28040, Madrid, Spain.
authors: Constantino
authors: C
authors: Ruibal
authors: Departamento de Biología Vegetal II, Facultad de Farmacia, Universidad Complutense de Madrid, Plaza de Ramón y Cajal s/n, 28040, Madrid, Spain.|Department of Biology, Faculty of Science, Ramkhamhaeng University, Bangkok, 10240, Thailand.
authors: Kawinnat
authors: K
authors: Buaruang
authors: Departamento de Biología Vegetal II, Facultad de Farmacia, Universidad Complutense de Madrid, Plaza de Ramón y Cajal s/n, 28040, Madrid, Spain.
authors: Jano
authors: J
authors: Núñez-Zapata
authors: Departamento de Biología Vegetal II, Facultad de Farmacia, Universidad Complutense de Madrid, Plaza de Ramón y Cajal s/n, 28040, Madrid, Spain.
authors: Guillermo
authors: G
authors: Amo de Paz
authors: Departamento de Biología Vegetal II, Facultad de Farmacia, Universidad Complutense de Madrid, Plaza de Ramón y Cajal s/n, 28040, Madrid, Spain.
authors: Víctor J
authors: VJ
authors: Rico
authors: Área de Biodiversidad y Conservación, Universidad Rey Juan Carlos, c/ Tulipón s/n., 28933, Móstoles, Madrid, Spain.
authors: M Carmen
authors: MC
authors: Molina
authors: Research School of Chemistry, Australian National University, Building 137, Canberra, ACT, 2601, Australia.
authors: John A
authors: JA
authors: Elix
authors: Department of Biological Sciences Dept. 2715, North Dakota State University, PO Box 6050, Fargo, ND, 58108-6050, USA.
authors: Theodore L
authors: TL
authors: Esslinger
authors: Tromsø University Museum, University of Tromsø - The Arctic University of Norway, PO Box 6050, Langnes, NO-9037, Tromsø, Norway.
authors: Inger Kristin K
authors: IK
authors: Tronstad
authors: Botanical Museum, Finnish Museum of Natural History, University of Helsinki, PO Box 7, Helsinki, FI-00014, Finland.
authors: Hanna
authors: H
authors: Lindgren
authors: Department of Bryophytes-Thallophytes, Domaine de Bouchout, National Botanic Garden of Belgium, 1860, Meise, Belgium.
authors: Damien
authors: D
authors: Ertz
authors: Department of Botany, The Natural History Museum, Cromwell Road, London, SW7 5BD, UK.
authors: Cécile
authors: C
authors: Gueidan
authors: Institute of Ecology & Earth Sciences, University of Tartu, Lai Street 38, Tartu, 51005, Estonia.
authors: Lauri
authors: L
authors: Saag
authors: Institute of Ecology & Earth Sciences, University of Tartu, Lai Street 38, Tartu, 51005, Estonia.
authors: Kristiina
authors: K
authors: Mark
authors: Biodiversity and Climate Research Centre BiK-F, Senckenberganlage 25, 60325, Frankfurt am Main, Germany.
authors: Garima
authors: G
authors: Singh
authors: Biodiversity and Climate Research Centre BiK-F, Senckenberganlage 25, 60325, Frankfurt am Main, Germany.
authors: Francesco
authors: F
authors: Dal Grande
authors: Science & Education, The Field Museum, 1400 S. Lake Shore Drive, Chicago, IL, 60605, USA.|Department of Medical Sciences, Ministry of Public Health, Tivanon Road, Nonthaburi, 11000, Thailand.
authors: Sittiporn
authors: S
authors: Parnmen
authors: Department of Lichenology and Bryology, Botanische Staatssammlung, Menzinger Str. 67 D-80638, München, Germany.
authors: Andreas
authors: A
authors: Beck
authors: Instituto de Botânica, Núcleo de Pesquisa em Micologia, Caixa Postal 68041, 04045-972, São Paulo, SP, Brazil.
authors: Michel Navarro
authors: MN
authors: Benatti
authors: Biodiversity and Animal Welfare Research Group, Department of Natural Sciences, Unitec Institute of Technology, Private Bag 92025, Auckland, 1142, New Zealand.
authors: Dan
authors: D
authors: Blanchon
authors: Department of Biology, Faculty of Science, Anadolu University, EskiŞehir, Turkey.
authors: Mehmet
authors: M
authors: Candan
authors: Conservatoire et Jardin botaniques de la Ville de Genève, CP 60, 1292, Chambésy, Switzerland.
authors: Philippe
authors: P
authors: Clerc
authors: UBC Herbarium, Beaty Museum, University of British Columbia, Vancouver, BC, V6T 1Z4, Canada.
authors: Trevor
authors: T
authors: Goward
authors: Institute of Plant Sciences, Karl-Franzens-University Graz, Holteigasse 6, 8010, Graz, Austria.
authors: Martin
authors: M
authors: Grube
authors: Grice Lab, Department of Dermatology, University of Pennsylvania, BRB 1046A, 421 Curie Blvd, Philadelphia, PA, 19104, USA.
authors: Brendan P
authors: BP
authors: Hodkinson
authors: Korean Lichen Research Institute, Sunchon National University, Sunchon, 540-742, Korea.
authors: Jae-Seoun
authors: JS
authors: Hur
authors: Tasmanian Herbarium, Private Bag 4, Hobart, Tas., 7001, Australia.
authors: Gintaras
authors: G
authors: Kantvilas
authors: Botany Department, National Museums of Kenya, PO Box 45166-00100, Nairobi, Kenya.
authors: Paul M
authors: PM
authors: Kirika
authors: Institute of Systematic Botany, The New York Botanical Garden, Bronx, NY, 10458-5126, USA.
authors: James
authors: J
authors: Lendemer
authors: School of Life Sciences, Södertörn University, SE-141 89, Huddinge, Sweden.
authors: Jan-Eric
authors: JE
authors: Mattsson
authors: Instituto de Investigaciones en Biodiversidad y Medioambiente (INIBIOMA) - CONICET, Universidad del Comahue, Quintral 1250, 8400, Sán Carlos de Bariloche, Río Negro, Argentina.
authors: María Inés
authors: MI
authors: Messuti
authors: Department of Biology, Duke University, 27708-0338, Durham, NC, 27708, USA.
authors: Jolanta
authors: J
authors: Miadlikowska
authors: Science & Education, The Field Museum, 1400 S. Lake Shore Drive, Chicago, IL, 60605, USA.
authors: Matthew
authors: M
authors: Nelsen
authors: Department of Bioinformatics and Genetics, Swedish Museum of Natural History, PO Box 50007, SE-104 05, Stockholm, Sweden.
authors: Jan I
authors: JI
authors: Ohlson
authors: Departamento de Biogeoquímica y Ecología Microbiana, Museo Nacional de Ciencias Naturales, CSIC, c/ Serrano 115, E-28006, Madrid, Spain.
authors: Sergio
authors: S
authors: Pérez-Ortega
authors: Institute of Ecology & Earth Sciences, University of Tartu, Lai Street 38, Tartu, 51005, Estonia.
authors: Andres
authors: A
authors: Saag
authors: Botanischer Garten und Botanisches Museum Berlin-Dahlem, Freie Universität Berlin, Königin-Luise-Straße 6-8, 14195, Berlin, Germany.
authors: Harrie J M
authors: HJ
authors: Sipman
authors: Iranian Research Organization for Science and Technology (IROST), 15815-115, Tehran, Iran.
authors: Mohammad
authors: M
authors: Sohrabi
authors: Biologal Museum, Lund University, Box 117, SE-22100, Lund, Sweden.
authors: Arne
authors: A
authors: Thell
authors: Department of Ecology, Swedish University of Agricultural Sciences, Box 7044, SE-750 07, Uppsala, Sweden.
authors: Göran
authors: G
authors: Thor
authors: Conservatoire et Jardin botaniques de la Ville de Genève, CP 60, 1292, Chambésy, Switzerland.
authors: Camille
authors: C
authors: Truong
authors: Royal Botanic Garden Edinburgh, 20A Inverleith Row, Edinburgh, EH3 5LR, UK.
authors: Rebecca
authors: R
authors: Yahr
authors: National Botanical Research Institute (CSIR), Rana Pratap Marg, Lucknow, 226001, Uttar Pradesh, India.
authors: Dalip K
authors: DK
authors: Upreti
authors: Departamento de Biología Vegetal II, Facultad de Farmacia, Universidad Complutense de Madrid, Plaza de Ramón y Cajal s/n, 28040, Madrid, Spain.
authors: Paloma
authors: P
authors: Cubas
authors: Science & Education, The Field Museum, 1400 S. Lake Shore Drive, Chicago, IL, 60605, USA.
authors: H Thorsten
authors: HT
authors: Lumbsch
mesh_terms: D005075:Biological Evolution; D002965:Classification; D005800:Genes, Fungal; D008011:Lichens / Q000235:genetics*; D000068837:Parmeliaceae / Q000235:genetics*; D010802:Phylogeny; D013559:Symbiosis
keywords: Ascomycota; Parmeliaceae; Raesaenenia; ancestral character reconstruction; lichenicolous fungi; mutualism; phylogeny