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A First Phylogenetic Assessment of Dictyonema S.Lat. in Southeastern North America Reveals Three New Basidiolichens, Described in Honor of James D

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A First Phylogenetic Assessment of Dictyonema S.Lat. in Southeastern North America Reveals Three New Basidiolichens, Described in Honor of James D © 2019 W. Szafer Institute of Botany Polish Academy of Sciences Plant and Fungal Systematics 64(2): 383–392, 2019 ISSN 2544-7459 (print) DOI: 10.2478/pfs-2019-0025 ISSN 2657-5000 (online) A first phylogenetic assessment of Dictyonema s.lat. in southeastern North America reveals three new basidiolichens, described in honor of James D. Lawrey Manuela Dal Forno1,2*, Laurel Kaminsky 3, Roger Rosentreter 4, R. Troy McMullin5, André Aptroot 6 & Robert Lücking7,8 Abstract. Three species of lichenized basidiomycetes in the Dictyonema clade from south- Article info eastern North America are described as new to science: Cyphellostereum georgianum, Received: 21 May 2019 C. jamesianum and Dictyonema lawreyi, all with a crustose-filamentous growth form. Revision received: 23 Aug. 2019 Based on ITS sequences, the species form well-supported monophyletic clades in a phy- Accepted: 25 Aug. 2019 logeny and are represented by at least two specimens each. They are also distinguishable Published: 2 Dec. 2019 by morphological and anatomical characters. These new findings emphasize the importance Associate Editor of lichenological studies in North America, especially in historically understudied taxo- Adam Flakus nomic groups, such as basidiolichens. This study is dedicated to James D. Lawrey on the occasion of his 70th birthday. Key words: Lichen systematics, Hygrophoraceae, United States, biodiversity Introduction The Dictyonema clade is the largest group of basidiolichens 2013; Lücking et al. 2014, 2017b). The clade currently (Lücking et al. 2017a). It belongs to tribe Arrheniae, sub- has 137 accepted species in five genera: Acantholichen, family Lichenomphaloideae and family Hygrophoraceae Cora, Corella, Cyphellostereum and Dictyonema (s.str.); in the order Agaricales (Lawrey et al. 2009; Lodge et al. however, a few historical genus names that have an uncer- 2014). Hygrophoraceae comprises over 600 species, most tain taxonomic status persist (Lücking et al. 2013). All five of which are non-lichenized, except for the Dictyonema of the accepted genera occur in the New World, whereas clade and the genus Lichenomphalia (Lodge et al. 2014). other regions almost exclusively feature Cyphellostereum Species in the Dictyonema clade occur worldwide but the and Dictyonema. highest diversity is in the Neotropics (Dal Forno et al. Aside from Mexico, the Dictyonema clade is sparsely represented in North America. In the ‘Cumulative Check- list for the Lichen-forming, Lichenicolous and Allied 1 Department of Botany, Smithsonian Institution, National Museum of Fungi of the Continental United States and Canada’ th Natural History, 10 St & Constitution Ave NW, Washington, DC, (Esslinger 2018), four taxa from this clade are listed: 20560, USA 2 Research Associate, Botanical Research Institute of Texas, Fort Worth, Cora glabrata [syn.: C. pavonia, Dictyonema glabratum, TX, 76107, USA D. pavonium], D. moorei, D. phyllogenum and D. seri- 3 Digitization Coordinator, McGuire Center for Lepidoptera and Bio- ceum. Two additional names on the list are considered diversity, Florida Museum of Natural History, University of Florida, synonyms or misidentifications: Dictyonema guadalu- Gainesville, FL 32611, USA 4 Dept of Biology, Boise State University, 1910 University Ave, Boise pense [= D. sericeum] and D. irpicinum (Esslinger 2018). ID, 83725 The genera Acantholichen, Corella and Cyphellostereum 5 Canadian Museum of Nature, Research and Collections, PO Box 3443, were not reported in Esslinger’s list but D. phyllogenum Station D, Ottawa, ON, K1P 6P4, Canada is now classified in Cyphellostereum (Lücking et al. 6 Laboratório de Botânica / Liquenologia, Instituto de Biociências, Universidade Federal de Mato Grosso do Sul, Avenida Costa e Silva 2013), so this genus is recognized from North America. s/n, Bairro Universitário, CEP 79070-900, Campo Grande, MS, Brazil. The taxonomic status of D. guadalupense is unclear but 7 Botanical Garden and Botanical Museum Berlin, Königin-Luise-Straße certainly it is not a synonym of D. sericeum (Lücking 6–8, 14195 Berlin, Germany et al. 2013). Given that the Dictyonema clade has been 8 Research Associate, Science & Education, The Field Museum, 1400 South Lake Shore, Chicago, IL, 60605, USA shown to contain many more species than proposed by * Corresponding author e-mail: [email protected] Parmasto (1978), including several hundred alone in the This work is licensed under the Creative Commons BY-NC-ND 4.0 License 384 Plant and Fungal Systematics 64(2): 383–392, 2019 genera Cora and Dictyonema (Lücking et al. 2014, 2017b; and obtained molecular data to aid in their classification. Dal Forno 2015), it is safe to say that, with the possible We detected three distinct lineages, all new to science exception of D. moorei, none of the names listed for North – two in the genus Cyphellostereum and one in Dic- America actually represent an accurate identification of tyonema, which are described here. the taxa occurring in this region. th As of February 20 , 2019, the ‘Consortium of North Material and methods American Lichen Herbaria’ (CNALH; http://lichenportal. org/) contained 111 records of continental United States Taxon sampling and phylogenetic analysis. This specimens identified as Cora or Dictyonema, with the study is part of a broad systematics study of the Dic- exception of one misidentification ofAcantholichen , which tyonema clade. Most specimens from North America we revised. All collections are from the southeastern United included here were already sequenced and included in States and the majority of them are from Florida (FL, 90 prior phylogenetic studies (Dal Forno 2015; Dal Forno total, 31 in Cora and 59 in Dictyonema), with a few speci- et al. 2017). However, to account for newly available ITS mens from North Carolina (NC, 2), South Carolina (SC, 7), sequences not included in previously published datasets, Georgia (GA, 4), and Louisiana (LA, 5), all in Dictyonema. we generated new MAFFT v1.3.7 alignments (Katoh A single specimen (Dictyonema sp.) is mentioned from & Toh 2005) on Geneious v11.1.5 (Kearse et al. 2012; Texas, and two samples lack information regarding their File S1 and File S2) and ran new phylogenetic analyses state provenance. Different names have been applied to on RAxML-HPC2 on XSEDE (v8.2.10) in the CIPRES identify these specimens: Cora glabrata and C. pavonia portal (Miller et al. 2010), following the same laboratorial (FL), ‘Dictyonema cincinnatum’ (as ‘Dichonema cincin- and computational procedures as described in Dal Forno natum’; FL, SC), D. glabratum (FL, ≡ Cora glabrata), (2015) and Dal Forno et al. (2013, 2017). Generated trees D. guadalupense (FL), D. irpicinum (FL, GA), D. moorei were visualized in FigTree v1.4.3 and edited in Photoshop (FL), D. pavonium (FL, ≡ Cora pavonia), D. reticulatum Illustrator. GenBank numbers for the new species are (SC), D. sericeum (FL, GA, LA, NC, SC) and D. spon- listed in the taxonomy section and in Table S1. giosum (FL). Dictyonema sericeum is also cited for Ala- bama by Parmasto (1978). These names agree with those Morphological analysis. Morphological characters were included in Esslinger’s list (2018), with the exception analyzed under a Leica M165 C stereoscope following of D. spongiosum and the apparently unpublished name standard procedures for the group (Lücking et al. 2013). ‘Dichonema cincinnatum’, interpreted in CNALH as ‘Dic- Anatomical thallus characters were investigated by light tyonema cincinnatum’. The latter is based on two collec- microscopy using a Leica DM4 B compound microscope, tions by the same collector (B. M. Davis) from FL and with thallus pieces mounted in tap water. Microscopic SC and likely a herbarium-working name. It should not be measurements were made at 400× and 1000× in water. confused with the cyanobacterium Scytonema cincinnatum Images were taken with the aforementioned microscopes described from France, neither is it derived from the city of with a Leica DFC450 digital camera and processed with Cinncinati in Ohio; rather, the epithet cincinnatum (Latin) Leica Application Suite (LAS) X software. In addition, refers to ‘curly hair’, i.e. the typical morphology of many we used an Olympus DSX 100 compound microscope filamentous Dictyonema species. with Microscope Control v2.1.5 software to generate Given the much-revised phylogenetic classification stacked images. of genera and species in the Dictyonema clade (Lücking et al. 2013, 2017b; Dal Forno et al. 2013, 2017; Dal Results and discussion Forno 2015) and that identifications of North American material rely almost entirely on Parmasto’s (1978) out- Maximum likelihood phylogenetic analysis based on dated monograph, virtually nothing is known about the the ITS fungal barcoding marker grouped the sequenced diversity and range of this clade in the United States. material into three distinct, strongly supported lineages The only reported species that might actually be present (Figs. 1, 2). Two lineages belong to the genus Cyphelloste- in North America north of Mexico is the demonstrably reum, and the two form a strongly supported sister group widespread Dictyonema moorei, which is well charac- relationship (Fig. 1), indicating a strong geographic signal terized by 2–3 rows of cyanobacterial cells inside the for this clade. The closest relative is C. imperfectum from fungal sheath. Dictyonema irpicinum is restricted to the Guatemala but this relationship is not well supported. The Paleotropics and D. guadelupense likely to the Caribbean, third lineage is a new species in Dictyonema
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