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(<I>Helvella</I>: <I> Ascomycota</I>) in Europe ÂŒ Persoonia 39, 2017: 201–253 ISSN (Online) 1878-9080 www.ingentaconnect.com/content/nhn/pimj RESEARCH ARTICLE https://doi.org/10.3767/persoonia.2017.39.09 A synopsis of the saddle fungi (Helvella: Ascomycota) in Europe – species delimitation, taxonomy and typification I. Skrede1,*, T. Carlsen1, T. Schumacher1 Key words Abstract Helvella is a widespread, speciose genus of large apothecial ascomycetes (Pezizomycete: Pezizales) that are found in terrestrial biomes of the Northern and Southern Hemispheres. This study represents a beginning on molecular phylogeny assessing species limits and applying correct names for Helvella species based on type material and specimens in the Pezizales university herbaria (fungaria) of Copenhagen (C), Harvard (FH) and Oslo (O). We use morphology and phylogenetic systematics evidence from four loci – heat shock protein 90 (hsp), translation elongation factor alpha (tef), RNA polymerase II (rpb2) and the nuclear large subunit ribosomal DNA (LSU) – to assess species boundaries in an expanded sample of Helvella specimens from Europe. We combine the morphological and phylogenetic information from 55 Helvella species from Europe with a small sample of Helvella species from other regions of the world. Little intraspecific variation was detected within the species using these molecular markers; hsp and rpb2 markers provided useful barcodes for species delimitation in this genus, while LSU provided more variable resolution among the pertinent species. We discuss typification issues and identify molecular characteristics for 55 European Helvella species, designate neo- and epitypes for 30 species, and describe seven Helvella species new to science, i.e., H. alpicola, H. alpina, H. carnosa, H. danica, H. nannfeldtii, H. pubescens and H. scyphoides. Article info Received: 10 November 2016; Accepted: 7 April 2017; Published: 14 September 2017. INTRODUCTION (Quélet 1886, Nannfeldt 1932, 1937, Dissing 1966a, b, Weber 1972, 1975, Häffner 1987, Abbott & Currah 1997). In its widest Helvella is a widespread, speciose genus of apothecial ascomy- circumscription over the last century, Helvella encompassed the cetes (Pezizomycetes: Pezizales) whose members are found in monotypic genera Underwoodia (Peck 1890, Eckblad 1968, terrestrial biomes of the Northern and Southern Hemispheres. Harmaja 1974), Wynnella (Boudier 1885, 1907, Harmaja 1974, The genus contains many of the larger and charismatic spe- Abbott & Currah 1997), Pindara (Velenovský 1934, Landvik cies of the order Pezizales and comprises a range of elaborate et al. 1999) and the hypogeous Helvella astieri (Korf 1973a). apothecia, from cupulate to saddle-shaped, and convex to cam- A number of Helvella taxa dating from late 18th (pre-Friesian) panulate, including species with folded and lobed caps seated and early 19th century taxonomic works, have been variously on a simple, ribbed or furrowed stipe. interpreted over time. Most taxonomists, including Fries himself, Although easily separated from other macrofungi by conspicu- applied a broad species concept allowing for a lot of morphologi- ous polymorphic apothecia, it is surprisingly difficult to distin- cal variation among the Helvella species that were accepted guish between Helvella species. Historically, the shape and in their monumental works (Afzelius 1783, Fries 1822, Dissing colour and outer surface characters have been emphasized 1966a, b, Weber 1972, 1975, Abbott & Currah 1997). These in species discrimination, whilst microanatomy of the sterile works also listed a number of heterotypic synonyms for many and fertile structures has added few characters of value in Helvella species, mostly assessed based on similarities of pu- species recognition. Weber (1972), after extensive studies of blished descriptions rather than as a result of comparative Michigan collections of Helvella, concluded that: “in summary, studies of type specimens. Furthermore, the iconic European most morphological and anatomical characters exhibit nearly Helvella species names, e.g., H. lacunosa, H. corium, H. elas- continuous variation in the genus as a whole. Each species, tica and H. acetabulum have been applied to specimens be- however, represents only one area on the spectrum of variation longing to a number of phylogenetically related or unrelated for each character, and several species may share a given part Helvella taxa in regional or local reports on the genus, and of the spectrum for a character. Thus a group of characters misidentifications of Helvella spp. in the literature and on the must be used to delimit species”. web are common. The more comprehensive 20th and 21st cen- Linnaeus (1737, 1753) proposed the genus Elvela (= Helvella, tury taxonomic works on the genus Helvella in Europe include orth. var.) for Elvela mitra (= Helvella crispa ss. Fries (1822)). the works of Dissing (1966a, b, 2000), Harmaja (1977b, 1979), Fries (1822) erected the family Elvellaceae, which was later re- Häffner (1987) and Van Vooren (2010, 2014). Dissing (1966b) ferred to as Helvellaceae (Corda 1842). Generic delimitation of recognised 26 species of Helvella in Europe, a list which was the morphologically diverse Helvella has varied. Fuckel (1870) later expanded to 28 (Dissing 1972) and to 38 in a later survey segregated two new genera, i.e., Macroscyphus and Paxina, of the species confined to the restricted area of the Nordic and Boudier (1907a) recognized altogether five genera, i.e., countries (Dissing 2000). Häffner (1987) accepted altogether 41 Leptopodia, Cyathipodia, Acetabula, Macropodia and Helvella species from Germany and the rest of the European continent. s.str., for what was later merged into a broadly defined Helvella The development of molecular systematics and the possibility 1 Department of Biosciences, University of Oslo, P.O. Box 1066, Blindern, of employing DNA barcode sequences as a more robust tool to 0316 Oslo, Norway; corresponding author e-mail: [email protected]. identify specimens of closely related species have recently and © 2017 Naturalis Biodiversity Center & Westerdijk Fungal Biodiversity Institute You are free to share - to copy, distribute and transmit the work, under the following conditions: Attribution: You must attribute the work in the manner specified by the author or licensor (but not in any way that suggests that they endorse you or your use of the work). Non-commercial: You may not use this work for commercial purposes. No derivative works: You may not alter, transform, or build upon this work. For any reuse or distribution, you must make clear to others the license terms of this work, which can be found at http://creativecommons.org/licenses/by-nc-nd/3.0/legalcode. Any of the above conditions can be waived if you get permission from the copyright holder. Nothing in this license impairs or restricts the author’s moral rights. 202 Persoonia – Volume 39, 2017 to some extent been applied to taxonomic studies of Helvella. Dissing & Lange (1967), Eckblad (1968), Weber (1972, 1975) Landvik et al. (1999) used nrDNA sequences to characterise a and Korf (1973b). small subset of Helvella species from Norway and emphasized We use sequence data from four loci to obtain an initial esti- the general limitation of single locus analyses and the unsuit- mate of the genetic diversity represented by 432 collections of ability of ITS to infer phylogeny and discriminate species across dried and fresh specimens of Helvella, each annotated by a the breadth of the genus. Nguyen et al. (2013) used ITS and ‘H’ number. In addition to a broad sample of European Helvella LSU nrDNA sequences and morphology to discriminate among collections, we included some collections from the American at least four distinct species of the H. lacunosa species complex and Asian continents in order to evaluate and better understand in western North American, and Landeros et al. (2015) used the intra- and intercontinental variations and distributions of the partial LSU sequences to study infrageneric groups of Helvella pertinent species. from Europe and North America. Recently, Ariyawansa et al. (2015) used the ITS, Zhao et al. (2015) ITS and a concatenated DNA extraction and PCR multilocus dataset of ITS, LSU, tef, rpb2 and mcm7, and Zhao et DNA was extracted using the E.Z.N.A HP Fungal DNA kit al. (2017) a dataset of ITS, LSU and tef to discriminate and de- (Omega Bio-Tek, Norcross, GA, USA) protocol for dried sam- scribe new species of the H. lacunosa, H. crispa and H. mona- ples, except that tissue was not ground, but frozen and thawed chella morphospecies complexes in China. To this array of genes we add hsp as an informative additional gene of utility two times in the extraction buffer, and subsequently vortexed in species identification in Helvella. thoroughly with one tungsten bead. Samples collected by the authors were stored directly in extraction buffer and thus, were We use sequence data and a simplified genealogical concor- not dried before DNA extraction, but extracted using the same dance phylogenetic species recognition (GCPSR) (Avise & protocol as above. Ball 1990, Taylor et al. 2000, Dettman et al. 2003) approach to resolve species-level lineages and phylogenetic species of Efforts were made to PCR amplify parts (270–700 bp) of four Helvella in Europe. By using this molecular approach in com- genetic loci that had been found useful in resolution of lower bination with morphological data, we reassess species limits level relationships in other fungal groups; i.e., the translation within Helvella in Europe. We hypothesize
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