A radical shift in the taxonomy of Lepraria s.l.: Molecular and morphological studies shed new light on the evolution of asexuality and lichen growth form diversification

Abstract

A combination of molecular phylogenetic analyses of ITS and mtSSU sequences, morphological and chemical analyses were used to investigate the lineages nominally included in the sterile lichen genus Lepraria. A core group (Lepraria s. str.) was resolved as sister to Stereocaulon. Species producing the secondary compounds argopsin, pannarin and usnic acid were found to belong to other lineages of lichen-forming ascomycetes. Study of Leprocaulon revealed that all species, except the type, likely represent members of Lepraria s. str. that have evolved a fruticose growth form. The correct name for the type species of Leprocaulon is shown to be L. quisquiliare, not L. microscopicum, and the genus is redefined to include several species previously placed in Lepraria. Leprocaulon quisquiliare is also shown to comprise two morphologically convergent species. The name is lectotypified and epitypified on material from the type region (Germany) and its application restricted to Old World populations. New World populations of L. quisquiliare are described as L. americanum. Leprocaulon, in its revised sense, is recognized in a new family (Leprocaulaceae) and order (Leprocaulales) sister to the Caliciales and including the genus Halecania. A new genus of Pilocarpaceae, Nelsenium, is introduced to accommodate Lepraria usnica. The status of Lepraria ecorticata is discussed in the context of usnic acid-producing Lecanora species. These nomenclatural novelties are proposed: (i) transfers from Leprocaulon to Lepraria: Lepraria albicans comb. nov., L. arbuscula comb. nov., L. congestum comb. nov., L. gracilescens comb. nov., L. pseudoarbuscula comb. nov., L. subalbicans comb. nov., L. tenellum comb. nov.; (ii) transfers from Lepraria to Leprocaulon: Leprocaulon adhaerens comb. nov., L. coriense, L. santamonicae comb. nov., L. terricola comb. nov. and L. textum comb. nov.; (iii) new taxa: Leprocaulales ord. nov., Leprocaulaceae fam. nov., Nelsenium gen. nov., Leprocaulon americanum sp. nov. and L. knudsenii sp. nov.

• asexual reproduction
• evolutionary placement algorithm
• Halecania
• polyphyly
• Speerschneidera

Acknowledgments

Thanks to the reviewers for their constructive comments that significantly improved the manuscript. Bill Buck, Richard Harris and Kerry Knudsen also are thanked for reviewing drafts of the manuscript before submission and for their extensive discussion of various problems associated with this study. Kerry Knudsen is specifically thanked for encouraging the first author to pursue studies of the taxa now placed in Leprocaulon. Teuvo Ahti and Leena Myllys (H) are thanked for locating and digitizing the lectotype of Leprocaulon nanum. David Hawksworth is thanked for providing a copy of his 1974 publication in a difficult to obtain British serial. Fieldwork carried out by the first author, during which specimens used in this study were collected, was financially supported in part by the City University of New York (CUNY), the National Park Service (Great Smoky Mountains National Park), the National Science Foundation (NSF), the Southern Appalachian Botanical Society (SABS), the Torrey Botanical Society (TBS) and the Western Pennsylvania Conservancy (WPC). Laboratory work and loan handling was facilitated by The New York Botanical Garden (NYBG) and financially supported in part by a grant from the California Lichen Society (CALS). In addition to the above financial sources, supplementary fieldwork and laboratory studies were made possible by a Doctoral Dissertation Improvement Grant from the National Science Foundation ( NSF-DDIG Award DEB-1110433). During research, BPH was supported by the National Science Foundation under awards EF-1115086 (North American lichens and bryophytes), DEB-1011504 (A phylogenetic characterization of the lichen microbiome) and EF-0832858 (NIMBioS). Sean Beeching, Ernie and Fenja Brodo, Colin Freebury, Malcolm Hodges, Rob E. Lee, Jennifer Staniforth, Michael Sundue, and Signa and Floyd Williams are thanked for facilitating permitting and other aspects of the first author’s fieldwork. The Humboldt Research Institute in Steuben, Maine, hosted the first author during his study there in summer 2010. Finally, the curators and collections staff of the institutions cited in Materials and methods are thanked for loaning specimens and answering information queries.