Fungal Diversity (2020) 102:205–224 https://doi.org/10.1007/s13225-020-00451-9

Evolution of non‑lichenized, saprotrophic species of Arthonia (Ascomycota, Arthoniales) and resurrection of Naevia, with notes on Mycoporum

Vinodhini Thiyagaraja1,2,3,4 · Robert Lücking5 · Damien Ertz6,7 · Dhanushka N. Wanasinghe1,4 · Samantha C. Karunarathna1,4 · Erio Camporesi8,9,10 · Kevin D. Hyde1,2,4

Received: 20 January 2020 / Accepted: 2 June 2020 / Published online: 3 July 2020 © MUSHROOM RESEARCH FOUNDATION 2020

Abstract Fungi that are barely lichenized or non-lichenized and closely related to lichenized taxa, the so-called borderline fungi, are an important element in reconstructing the evolutionary history of lichenized lineages. Arthoniaceae is a prime example includ- ing non-lichenized, saprotrophic lineages which potentially were precursors to lichenized taxa. In this study, we focused on saprotrophic species of Arthonia sensu lato, including new sequence data for Arthonia pinastri. We obtained fresh material of this taxon from a living branch of Fraxinus ornus in Italy to assess its taxonomic status and to elucidate its phylogenetic relationships within Arthonia. Thin sections of the thallus and ascomata of A. pinastri confrmed the absence of a photobiont. Maximum likelihood and Bayesian analyses of combined mtSSU, nuLSU and RPB2 sequence data placed the species close to A. dispersa (barely lichenized or non-lichenized) and A. punctiformis (non-lichenized) in a clade closely related to Arthonia sensu stricto, and the A. pinastri clade is here resurrected under the name Naevia. Ancestral character state analysis within a broader context of Arthoniales does not support the saprotrophic lifestyle to be a plesiomorphic feature, but suggests loss of lichenization in Naevia, as well as loss and possible regain in a second clade containing saprotrophic species and including taxa resembling Mycoporum, underlining the evolutionary plasticity of Arthoniales. These two clades constitute model taxa to further investigate the evolution of alternative biological lifestyles within the context of chiefy lichenized taxa.

Keywords Arthonia susa · Arthothelium · Evolution · Lichenization · Mycarthonia · Pseudoarthonia · Saprobes

Electronic supplementary material The online version of this article (https​://doi.org/10.1007/s1322​5-020-00451​-9) contains supplementary material, which is available to authorized users.

* Kevin D. Hyde 6 Research Department, Meise Botanic Garden, Nieuwelaan [email protected] 38, 1860 Meise, Belgium 7 Service Général de l’Enseignement Supérieur et de la 1 CAS Key Laboratory for Plant Biodiversity Recherche Scientifque, Fédération Wallonie-Bruxelles, Rue and Biogeography of East Asia, Kunming Institute A. Lavallée 1, 1080 Brussels, Belgium of Botany, Chinese Academy of Science, Kunming 650201, Yunnan, People’s Republic of China 8 A.M.B.G. Gruppo Micologico Forlivese “Antonio Cicognani”, Via Roma 18, Forli, Italy 2 Center of Excellence in Fungal Research, Mae Fah Luang University, Chiang Rai 57100, Thailand 9 A.M.B, Circolo Micologico “Giovanni carini”, C.P. 314, Brescia, Italy 3 Department of Entomology and Plant Pathology, Faculty of Agriculture, Chiang Mai University, Chiang Mai 50002, 10 Societa per gli Studi Naturalistici della Romagna, C.P. 144, Thailand Bagnacavallo, RA, Italy 4 World Agro Forestry Centre East and Central Asia, Kunming 650201, Yunnan, People’s Republic of China 5 Botanischer Garten und Botanisches Museum, Freie Universität Berlin, Königin‑Luise‑Str. 6–8, 14195 Berlin, Germany

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Introduction et al. 2014, 2015; Ertz et al. 2018; Van den Broeck et al. 2018). Lichenization has evolved several times independently Due to its versatile biology and the fact that Arthoniales within the Phylum Ascomycota, but its exact origins and forms a separate order and class of chiefy lichenized fungi, the relationships between lichenized and non-lichenized Arthonia sensu lato is an ideal group to investigate the role lineages is often unclear (Gargas et al. 1995; Lutzoni et al. of so-called borderline lichenized fungi in the evolution of 2001, 2004; Nelsen et al. 2009, 2011; Lücking and Nelsen lichenization. Borderline lichenized fungi are characterized 2018). One example is the order Arthoniales, which is by forming autonomous thalli on bark, i.e. not lichenicolous, predominantly lichenized, but contains a number of non- but growing intermingled with other lichens; the presence of lichenized, lichenicolous or saprotrophic taxa, particular a photobiont is ambiguous or a photobiont is absent. Some of in the family Arthoniaceae, which comprises more than these lineages are optionally lichenized or saprotrophic, such 700 species in about 20 genera (Grube 1998; Frisch et al. as in the genera Schizoxylon and Stictis in Ostropales (Wedin 2014; Lücking et al. 2017; Ertz et al. 2018; Wijayawardene et al. 2004; Muggia et al. 2011). Borderline lichenized fungi et al. 2020). Most of the non-lichenized taxa are concen- can be deeply nested within lichenized clades (e.g. Ostro- trated in the collective genus Arthonia sensu lato, one of pales), or they may represent early diverging clades, such as the largest genera of crustose lichens comprising ca. 500 in Trypetheliales (Nelsen et al. 2011; Lücking et al. 2017; species (Acharius 1806; Sundin and Tehler 1998; Sundin Miranda-González et al. 2020). A potential placement as 1999; Lücking et al. 2017). According to Index Fungorum early diverging lineages is of special interest in reconstruct- (2020), more than 1560 names are linked to this genus. ing the evolution of lichenization. Phylogenetically, Arthonia sensu lato forms a largely para- In cases of borderline lichenized fungi currently classifed phyletic clade comprising various distinct lineages (Grube in Arthonia sensu lato, it is unclear whether they are precur- et al. 1995; Grube 2001; Ertz et al. 2009, 2018; Frisch sors to lichenized lineages or are secondarily delichenized. et al. 2014; Van den Broeck et al. 2018). To elucidate their evolution, it is necessary to analyze their Arthonia in its broad sense, including various recent preferred life strategies in a molecular phylogenetic frame- segregates, exhibits a broad biological amplitude: while work (Divakar et al. 2013; Ismail et al. 2016). To this end, comprising mostly lichenized species, about one quarter we obtained fresh material of the borderline lichenized, pre- of the genus (139 species) represents lichenicolous taxa sumably saprotrophic taxon Arthonia pinastri from a living (Grube et al. 1995; Kantvilas and Wedin 2015; Dieder- branch of Fraxinus ornus in Italy. We generated morpho- ich et al. 2018) and some species are non-lichenized and anatomical, microchemical and molecular data in order to saprotrophic on bark (Sundin 1999; Grube 2007; Smith (1) infer the placement of this species using maximum like- et al. 2009). In historical classifcations, saprotrophic lihood and Bayesian analyses of combined sequence data species have variously been separated in genera such within a broad phylogenetic framework of Arthoniaceae; as Celidiopsis, Celidium, Conida, Conidella, Lecideop- (2) document morpho-anatomical and chemical characteris- sis, Mycarthonia, and Naevia (Fries 1824, 1825; Reinke tics of this taxon, particularly its biological lifestyle; and (3) 1895; Schneider 1897; Vainio 1901; Engler 1903; Ser- perform ancestral character analysis to reconstruct whether nander 1907; Zahlbruckner 1907; Petrak 1953; von Arx the species is primarily or secondarily non-lichenized. By 1954; Sundin and Tehler 1998; Grube 2007). Lichenized including a broad set of Arthoniaceae comprising other pre- species are associated chiefy with trentepohlioid algae, sumably saprotrophic lineages, we also expected to clarify with the exception of the Bryostigma clade and Arthonia lifestyle shifts in this family at a more general level. mediella, which feature chlorococcoid algae (Frisch et al. 2014). However, the phylogenetic position of several taxa with chlorococcoid algae and obviously unrelated to these Materials and methods clades such as Arthonia phlyctiformis (Gerstmans and Ertz 2016) still needs to be determined. Notably, lichenicol- Fresh material of Arthonia pinastri was collected from Passo ous species are also often associated with hosts having del Carnaio Bagno di Romangna, Forli-Cesena Province, chlorococcoid algae (Sundin and Tehler 1998; Wedin and Italy, in September 2017. Samples were examined using a Hafellner 1998; Frisch and Holien 2018; Diederich et al. Motic SMZ 168 Series dissecting microscope. Hand sec- 2018). Species of Arthonia sensu lato occupy a wide range tions of the ascomata were mounted on water, 10% KOH and of habitats, occurring in dry to wet environments, from lit- Lugol’s solution. Sections of ascomata and other micro-mor- toral to alpine regions (Sundin 1999; Grube 2007; Smith phological characteristics were photographed using a Nikon et al. 2009). Even after the removal of various recent seg- ECLIPSE 80i compound microscope ftted with a Canon regates, the genus remains highly heterogenous (Frisch 550D digital camera. Microscopic measurements were made with Tarosoft Image Frame Work 0.9.0.7 and images

1 3 Fungal Diversity (2020) 102:205–224 207 used for fgures were processed with Adobe Photoshop CS6 Phylogenetic trees were reconstructed based on mtSSU, Extended 10.0 (Adobe Systems, USA). The material was nuLSU and RPB2 sequence data of a broad set of Artho- deposited in the Mae Fah Luang University (MFLU) Her- niales focusing on arthonioid clades. Representatives of barium, Chiang Rai, Thailand. The species description was Roccellaceae, Chrysotrichaceae and the Felipes clade were structured based on recommendations by Ariyawansa et al. selected as outgroup taxa following Frisch et al. (2014) and (2015). We could not obtain a pure culture of this fungus Van den Broeck et al. (2018). Reference sequences were and the morphological characteristics and phylogenetic data retrieved from GenBank (Table 1). Multiple sequence align- were obtained from fresh fruiting and thallus structures. The ments were generated with MAFFT 7 (http://maft​.cbrc.jp/ newly sequenced taxon linked with Faces of Fungi (Jayasiri align​ment/serve​r/index​.html) (Katoh and Standley 2013) et al. 2015) and Index Fungorum (2020)(http://www.index​ and manually inspected using Bioedit 7.0.5.2 (Hall 1999). fungorum.org/Names​ /Names​ .asp​ ; accessed 2 January 2020). Terminal ends of sequences were deleted manually and excluded from the dataset. The fnal concatenated alignment DNA extraction, PCR amplifcation and gene comprised 3281 nucleotide positions. sequencing Phylogenetic analyses of both individual and combined aligned data were performed under maximum-likelihood DNA was extracted directly from fruiting bodies of the fun- (ML) and Bayesian criteria. The single-marker phylogenies gus as outlined by Wanasinghe et al. (2018). The E.Z.N.A.® resulted in non-conficting topologies and the three mark- Forensic DAT (D3591-01, Omega Bio-Tek) DNA extraction ers were therefore combined following Frisch et al. (2014) kit was used to extract DNA following the manufacturer’s and Van den Broeck et al. (2018). The phylogeny web tool instructions. DNA samples that were intended for use as “ALTER” (Glez-Peña et al. 2010) was used to convert the a template for PCR were stored at 4 °C for use in regu- sequence alignments from FASTA to PHYLIP for RAxML lar work and duplicated at − 20 °C for long-term storage. analysis and from FASTA to NEXUS format for Bayes- DNA sequence data were obtained from partial sequences of ian analysis. The estimated model of maximum likelihood mitochondrial and ribosomal coding genes. The mitochon- was determined using MrModeltest v.2.2 (Nylander 2004). drial small subunit (12S, mtSSU) was amplifed with the Maximum likelihood trees were generated using RAxML- primers mtSSU1 and mtSSU3R (Zoller et al. 1999), while HPC2 on XSEDE (8.2.8) (Stamatakis 2014; Stamatakis et al. the partial large subunit nuclear rDNA (28S, nuLSU) was 2008) in the CIPRES Science Gateway platform (Miller amplifed with the primers LROR and LR5 (Vilgalys and et al. 2010). A Bayesian tree sample was generated by using Hester 1990). MCMC in MrBayes 3.1.2 (Huelsenbeck and Ronquist 2001; PCR was performed in a 25 μl reaction mixture consist- Zhaxybayeva and Gogarten 2002), with 1000,000 MCMC ing of 2.0 μl of DNA template, 1 μl of each primer, 12.5 μl generations using four chains and partitioned analysis with of Taq PCR Master Mix (Bioteke Co., China) and 8.5 μl of a sample frequency of each 100th tree, producing 10,000 sterilized water. The PCR amplifcation was performed for trees. The frst 1000 (10% from total) trees were discarded mtSSU with an initial denaturing step of 94 °C for 3 min, as burn-in, and the remaining 9000 trees were used to com- followed by 35 amplifcation cycles of 94 °C for 3 min, pute posterior probabilities. Trees were displayed in FigTree 52 °C for 1 min and 72 °C for 1 min and a fnal extension 1.4.0 (Rambaut 2014), Microsoft PowerPoint 2013 and fur- step of 72 °C for 10 min. PCR amplifcation was performed ther edited in Adobe Photoshop CS6 Extended 10.0 (Adobe for LSU with an initial denaturing step of 94 °C for 3 min, Systems, USA). followed by 35 amplifcation cycles of 95 °C for 30 s, 55 °C for 50 s and 72 °C for 90 s and a fnal extension step of 72 °C Ancestral character state analyses for 10 min. We failed to amplify the RPB2 protein-coding gene following Liu et al. (1999). Finally, the PCR products RASP 3.2.1 (Reconstruct Ancestral State in Phylogenies) were checked on 1% agarose gel stained with ethidium bro- was used to construct ancestral character analysis, using the mide. PCR purifcation and sequencing of PCR products two approaches of BayesTraits and Bayesian Binary MCMC were carried out at Shanghai Sangon Biological Engineering (Yu et al. 2015, 2019). Both analyses were performed on Technology & Services Co., China. The nucleotide sequence a time-calibrated maximum clade credibility tree recon- data acquired were deposited in GenBank and alignments structed in BEAST. Divergence time analysis were carried and the trees were submitted to TreeBASE (ID 25688). out using BEAST 1.10.4 and the XML fle was constructed using BEAUTI 1.10.4. (Drummond et al. 2012). Single Phylogenetic analyses gene alignments were imported as separate partitions. The GTR + G+I substitution model was used for all three gene The newly generated sequences were checked using regions as suggested by MrModeltest 2.2 (Nylander 2004). NCBI BLAST search (https​://www.ncbi.nlm.nih.gov). We ran four independent Monte Carlo Markov Chains of 120

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Table 1 Taxa used in this study for the analysis of combined mtSSU, nuLSU and RPB2 sequence data and their GenBank accession numbers Species Specimen voucher mtSSU nuLSU RPB2

Arthonia apatetica 2 UPS:Svensson 2017 KJ850992 KJ851045 KJ851125 Arthonia apatetica 3 UPS:Svensson 1939 KJ850993 KJ851056 KJ851126 Arthonia apotheciorum UPS:Frisch 11/Se23 KJ850970 – KJ851148 Arthonia atra L10170 KY983978 – KY983985 Arthonia biatoricola UPS:Thor 24350 KJ850990 – KJ851149 Arthonia calcarea 1 UPS:Thor 11/6a KJ850974 – KJ851105 Arthonia calcarea 2 Ertz 7545 (BR) EU704063 – EU704027 Arthonia didyma 1 Ertz 7587 (BR) EU704047 EU704083 EU704010 Arthonia didyma 2 UPS:Frisch 11/Se41 – KJ851081 KJ851106 Arthonia dispersa 2 taxon:242232 AY350570 AY350578 – Arthonia granithophila UPS:Frisch 10/Se74 KJ850981 KJ851049 KJ851107 Arthonia graphidicola UPS:Frisch 10/Jp102 KJ850980 KJ851034 – Arthonia ilicina UPS:McCune 31067 KJ850982 KJ851069 – Arthonia incarnata 1 Frisch 10/Jp94 KY983972 – KY983980 Arthonia incarnata 2 Frisch 12/Jp289 KY983973 – KY983981 Arthonia incarnata 3 Frisch 13/Jp215 KY983974 – KY983982 Arthonia lapidicola UPS:Westberg Frisch 11/Se47 KJ850997 KJ851070 KJ851119 Arthonia lobariicola 1 UPS:Frisch 10/Jp737 KJ851002 KJ851036 KJ851127 Arthonia lobariicola 2 UPS:Frisch 10/Jp737 KJ851001 KJ851035 KJ851128 Arthonia maculiformis UPS:Wedin 9393b – KF707635 KF707658 Arthonia mediella 1 UPS:Thor 12/8 KJ851015 KJ851032 KJ851132 Arthonia mediella 2 UPS:Frisch 11/Se22 KJ851014 KJ851031 KJ851133 Arthonia molendoi 1 UPS:Frisch 11/Se36 KJ851000 KJ851051 KJ851117 Arthonia molendoi 2 Frisch 17/No10 (TRH) MH177777 MH177781 MH177770 Arthonia neglectula UPS:Frisch 10/Se91 KJ850989 KJ851037 KJ851118 Arthonia parietinaria Frisch 17/No25 (TRH) MH177778 MH177782 MH177771 Arthonia peltigerina UPS:Westberg Frisch 11/Se46 KJ850998 – KJ851122 Arthonia phaeophysciae UPS:Ertz 11/2 – KJ851067 KJ851112 Arthonia physcidiicola UPS:Frisch 11/Ug318 KF707646 – KF707657 Arthonia radiata 1 UPS:Frisch 10/Se29 KJ850968 – KJ851108 Arthonia radiata 2 UPS:Frisch 11/Se25 KJ850969 – KJ851109 Arthonia sp. 1 UPS:Svensson 2324 KJ851019 KJ851082 KJ851123 Arthonia sp. 2 UPS:Svensson 2148 KJ850995 KJ851046 KJ851120 Arthonia stereocaulina UPS:Westberg Frisch 11/Se48 KJ850999 KJ851062 – Arthonia subfuscicola 1 UPS:Thor 11/1 KJ850971 – KJ851110 Arthonia subfuscicola 2 UPS:Frisch 11/Se15 KJ850972 – KJ851111 Arthonia susa taxon:2488734 – MH887470 – Arthonia thoriana 1 Sanderson 2176 (BR) MG207687 – – Arthonia thoriana 2 Sanderson 2174 (herb. Sanderson) MG207685 – – Arthonia toensbergii 1 Frisch N4-2-Pa4-1 (TRH) MH177775 MH177779 – Arthonia toensbergii 2 Frisch N4-2-Pa4-1 (TRH) MH177776 MH177780 – Arthonia vinosa UPS:Frisch 10/Jp816 – KY983979 – Arthothelium galapagoense 1 Ertz 11790 (BR) – HQ454516 HQ454657 Arthothelium galapagoense 2 Ertz 11654 (BR) – HQ454515 HQ454658 Arthothelium norvegicum UPS:McCune 31061 – KJ851038 KJ851114 Arthothelium orbilliferum TRH-L-15449 KY983977 – – Arthothelium punctatum 1 KoLRI 044205 MF616614 MF616616 – Arthothelium punctatum 2 KoLRI 044206 MF616615 MF616617 – Arthothelium ruanum 1 KoLRI 038018 MF616609 – MF616619 Arthothelium ruanum 2 KoLRI 038257 MF616610 – MF616620

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Table 1 (continued) Species Specimen voucher mtSSU nuLSU RPB2

Arthothelium ruanum 3 KoLRI 038261 MF616611 – MF616621 Arthothelium ruanum 4 KoLRI 038275 MF616612 – – Arthothelium ruanum 5 KoLRI 038275 MF616613 – – Arthothelium ruanum 6 Zimmerman 1117 (F) GU327683 – – Arthothelium spectabile TNS:Frisch12Jp179a KP870144 – KP870160 Arthothelium sp. 2 UPS:Joensson Guyana 10 KJ850957 – KJ851094 Arthothelium sp. 3 UPS:Joensson Guyana 8 KJ850958 – KJ851095 Arthothelium spectabile TNS:Frisch12Jp179a KP870144 – KP870160 Briancoppinsia cytospora 1 Diederich 16849 (herb. Diederich) JF830771 JF830769 – Briancoppinsia cytospora 2 Ertz 15244 (BR) JF830772 JF830770 – Bryostigma muscigenum UPS:Thor 26206 KJ850991 KJ851052 KJ851124 Bryostigma sp. 1 SK L06 MH510022 – MH510019 Bryostigma sp. 2 SK L04 MH510023 – MH510020 Chiodecton natalense Ertz 6576 (BR) EU704051 EU704085 EU704014 Chiodecton sorediatum UPS:Frisch 11/Ug447 KF707648 KF707638 KF707661 Chrysothrix favovirens UPS:Thor 26751 KJ851017 KJ851030 – Chrysothrix sp. UPS:Thor 25993 KJ851018 KJ851079 – Coniangium spadiceum 1 UPS:Thor 26200 – KJ851071 KJ851116 Coniangium spadiceum 2 UPS:Frisch 11/Se31 – KJ851029 KJ851115 Coniarthonia eos UPS:Thor 26000 KJ850987 KJ851053 KJ851134 Coniarthonia pulcherrima 1 Cáceres & Aptroot 11731 (ISE) KP843610 – – Coniarthonia pulcherrima 2 Cáceres & Aptroot 11731 (ISE) KP843609 – – Coniarthonia rosea 1 Cáceres & Aptroot 11716 (ISE) KP843607 – – Coniarthonia rosea 2 Cáceres & Aptroot 11952 (ISE) KP843608 – – Coniocarpon af cinnabarinum 2 UPS:Frisch 11/Ug3 KJ850978 HQ454509 KJ851102 Coniocarpon cinnabarinum 2 UPS:Johnsen111003 KJ850976 KJ851059 KJ851103 Coniocarpon cinnabarinum 4 UPS:Frisch11Ug296 KP870158 KP870143 KP870170 Coniocarpon fallax LD:L10075 KJ850979 – KJ851101 Coniocarpon rubrocinctum Nelsen 4010 (F) GU327684 – – Crypthonia af. vandenboomii UPS:Frisch 11/Ug21 KJ850960 – KJ851085 Crypthonia palaeotropica 1 UPS:Frisch 11/Ug457 KJ850961 – KJ851084 Crypthonia palaeotropica 2 UPS:Frisch11Ug26B KP870145 – KP870161 Cryptophaea phaeospora 1 Van den Broeck 5809 (BR) KX077541 – – Cryptophaea phaeospora 2 Van den Broeck 5964 (BR) KX077540 – – Cryptothecia assimilis Lumbsch 19815 l (F) GU327688 – – Cryptothecia austrocoreana 1 KoLRI No.041892 MF769374 – – Cryptothecia austrocoreana 2 KoLRI No.044721 MF769375 – – Cryptothecia punctosorediata F:Nelsen 4038 JX046450 – – Cryptothecia sp. 1 UPS:Frisch 11/Ug39 KJ850954 – KJ851086 Cryptothecia sp. 3 UPS:Frisch 11/Ug18 KJ850955 – KJ851092 Cryptothecia sp. 4 UPS:Frisch 11/Ug194 KJ850956 KJ851058 KJ851093 Cryptothecia sp. 5 Ertz 8472 (BR) – HQ454521 – Cryptothecia subnidulans 1 v.d.Boom 40613 KJ850952 – KJ851087 Cryptothecia subnidulans 2 UPS:Joensson Guyana 6a KJ850953 – KJ851088 Felipes leucopellaeus UPS:Frisch 10/Se34 KJ850984 KJ851033 KJ851130 Felipes sp. 2 UPS:Frisch 11/Ug212 KJ850985 KJ851064 KJ851129 Felipes sp. 3 UPS:Frisch 11/Ug218 KJ850986 KJ851068 KJ851131 Glomerulophoron mauritiae BR Ertz19164 KP870153 – KP870167 Herpothallon inopinatum UPS:Rudolphi 12 KJ850964 – KJ851099 Herpothallon kigeziense UPS:Frisch 11/Ug26 KF707644 – KF707654

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Table 1 (continued) Species Specimen voucher mtSSU nuLSU RPB2

Herpothallon rubrocinctum 1 UPS:Rudolphi 5 KF707643 JX046468 KF707655 Herpothallon rubrocinctum 2 Nelsen 4006 (F) GU327693 – – Herpothallon sp. UPS:Frisch 11/Ug401 KF707645 – KF707653 Inoderma afromontanum UPS:Frisch 11/Ug164 KJ850963 – KJ851090 Inoderma byssaceum 1 UPS:Thor 25952 KJ850962 KJ851040 KJ851089 Inoderma byssaceum 2 UPS:Lif 186 – KJ851041 KJ851091 Inoderma nipponicum 1 TNS:Frisch12Jp227 KP870146 – KP870162 Inoderma nipponicum 2 TNS:Frisch13Jp1 KP870147 – KP870163 Inoderma sorediatum 1 Kukwa 15630 & Lubek (BR) MG207689 – – Inoderma sorediatum 2 Kukwa 15631 & Lubek (BR) MG207690 – – Inoderma subabietinum Ertz16885 (BR) KP870150 – KP870164 Leprantha cinereopruinosa Kukwa 17127 & Lubek (BR) MG207692 – – Melarthonis piceae UPS:Thor 25995 KJ851016 KJ851080 – Naevia af. punctiformis UPS:Thor 24702 KJ850975 KJ851043 – Naevia dispersa 1 UPSC 2583 AY571383 AY571381 – Naevia pinastri MFLU 17-3497 MN842780 MN842779 – Naevia punctiformis UPS:Thor 26158 KJ850973 KJ851044 KJ851113 Myriostigma candidum 1 Ertz 9260 (BR) EU704052 – EU704015 Myriostigma candidum 2 UPS:Frisch 11/Ug125 KJ850959 – KJ851096 Myriostigma candidum 3 Ertz 9260 (BR) – HQ454520 – Myriostigma miniatum Silva T2A29 (ISE) KP843606 – – Pachnolepia pruinata 1 Tehler 9139 (S) – – HQ454650 Pachnolepia pruinata 2 UPS:Frisch 11/Se34 KJ850967 – KJ851098 Reichlingia leopoldii 1 Ertz 13293 (BR) JF830773 HQ454581 HQ454722 Reichlingia leopoldii 2 Ertz 13294 (BR) JF830774 HQ454582 HQ454723 Reichlingia syncesioides UPS:Frisch 11/Ug14 KF707651 KF707636 KF707656 Reichlingia zwackhii 1 UPS:Thor 11/3 KF707652 KF707637 KF707662 Reichlingia zwackhii 2 Ertz 10928 (BR) – HQ454514 HQ454655 Snippocia nivea 1 Ertz 17437 (BR) MG207695 – – Snippocia nivea 2 Sanderson 2180 (herb. Sanderson) MG207694 – – Snippocia nivea 3 Sanderson 2179 (herb. Sanderson) MG207693 – – Sporodophoron cretaceum 1 UPS:Thor27720 KP870159 – – Sporodophoron cretaceum 2 BR Ertz17592 KP870152 – – Sporodophoron gossypinum 1 TNS:Frisch12Jp186 KP870154 – KP870168 Sporodophoron gossypinum 2 TNS:Frisch12Jp197 KP870156 – – Sporodophoron primorskiense 1 TNS:Y.Ohmura10607 LC086299 – – Sporodophoron primorskiense 2 TNS:Ohmura10509 KP870157 – KP870169 Stirtonia neotropica Cáceres & Aptroot 11112 (ISE) KP843611 – – Stirtonia sp. UPS:Frisch 11/Ug325 KJ850965 KJ851073 – Synarthonia albopruinosa BR:VDB 6086 MH251873 – – Synarthonia aurantiacopruinosa BR:VDB 5764 MH251874 – – Synarthonia fuscata BR:VDB 6101 MH251875 – – Synarthonia inconspicua 1 BR:VDB 7013B MH251881 – – Synarthonia inconspicua 2 BR:ERTZ 19739A MH251879 – – Synarthonia josephiana BR:ERTZ 19739B MH251876 – – Synarthonia muriformis 1 UPS:Frisch 11/Ug41 KJ851025 – – Synarthonia muriformis 2 BR:ERTZ 19344 MH251877 – – Synarthonia ochracea BR:VDB 6653 MH251884 – – Synarthonia pilosella BR:ERTZ 7808 MH251883 – – Tylophoron crassiusculum F:Luecking 18006 – EU670258 –

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Table 1 (continued) Species Specimen voucher mtSSU nuLSU RPB2

Tylophoron galapagoense 1 Bungartz 8749 (CDS) JF830776 JF295078 – Tylophoron galapagoense 2 Bungartz 8750 (CDS) JF830777 JF295079 – Tylophoron hibernicum 4 Diederich 16335 (h. P. Diederich) JF830779 JF295084 – Tylophoron hibernicum 5 UPS:Frisch 11/Ug220 KJ850966 KJ851065 KJ851097 Tylophoron moderatum 1 Ertz 14504 (BR) JF830780 JF295085 – Tylophoron moderatum 2 F:Luecking 15081a – EU670256 – Tylophoron protrudens F:Lumbsch 19557 – EU670257 – Tylophoron stalactiticum Ertz 10880 (BR) JF830781 JF295086 –

The newly generated sequences are indicated in black boldface million generations with 10,000 sampling for every genera- model of the combined mtSSU, nuLSU and RPB2 data set tions. The log fles were checked in Tracer 1.5 (Rambaut and were as follows: estimated base frequencies: A = 0.278540, Drummond 2009) to ensuring that efective sample sizes C = 0.224004, G = 0.251037, T = 0.246419; substitution (ESS) was above 200. After removal of a proportion of each rates: AC = 0.893196, AG = 3.792168, AT = 1.855097, run as burn-in, the remaining trees were summarized as CG = 1.020469, CT = 5.165432, GT = 1.000000; propor- maximum clade credibility (MCC) trees in TreeAnnotator tion of invariable sites: I = 0.001000; gamma distribution (part of the BEAST-package) and the tree fle was exported shape parameter: α = 0.652756. to RASP 3.2.1. Each terminal in the tree was coded for either The topology was largely congruent with that of earlier lichenized with a trentepohlioid photobiont, lichenized with studies (Frisch et al. 2014, 2015; Ertz et al. 2018; Van den a chlorococcoid photobiont, lichenicolous, or saprotrophic. Broeck et al. 2018). The backbone was rather well supported BayesTraits and Bayesian Binary MCMC trees were per- and resolved into numerous clades within Arthoniaceae. formed and visualized in RASP 3.2.1 using default settings Arthoniaceae sensu stricto appears to be defned by exclud- as follows: 1,010,000 iterations for BayesTraits with a burn- ing the Bryostigma and Coniangium clades; besides Artho- in of 10,000, sampling 1000 trees and with 10 ML trees; nia sensu stricto, Arthothelium sensu stricto, Cryptothecia 50,000 generations for Bayesian Binary MCMC, with 10 sensu stricto and Stirtonia, Arthoniaceae also contains the chains, a sample frequency of 100, a temperature of 0.1, genera Briancoppinsia, Coniocarpon, Herpothallon, Ino- state frequencies fxed (JC), and among-site rate variation derma, Myriostigma, Pachnolepia, Reichlingia, Snippocia, equal. Sporodophoron, Synarthonia and Tylophoron. The target group with Arthonia pinastri formed a strongly supported clade also including A. dispersa and A. punctiformis, in the Results vicinity of Arthonia sensu stricto but not part of that genus. This clade deserves generic status and the name Naevia Fr. Phylogenetic analysis sensu (Fries 1824, 1825) is reinstated for it below.

Phylogenetic trees were obtained from maximum likeli- Ancestral character state analysis hood and Bayesian analyses using concatenated mtSSU, nuLSU and RPB2 sequence data (Fig. 1; Supplementary Ancestral character state analysis regarding life strategies Figs. 1–6). We analyzed 157 sequences including new data gave quite diferent results based on either BayesTraits or for Arthonia pinastri and data from the genera Arthonia Bayesian Binary MCMC. Bayesian Binary MCMC recon- sensu lato, Arthothelium sensu lato, Briancoppinsia, Bry- structed the basal nodes of Arthoniales, Arthoniaceae sensu ostigma, Chiodecton, Chrysothrix, Coniangium, Coniartho- lato and Arthoniaceae sensu stricto all as lichenized with a nia, Coniocarpon, Crypthonia, Cryptophaea, Cryptothecia trentepohlioid photobiont, with a switch to chloroccocoid sensu lato, Felipes, Glomerulophoron, Herpothallon, Ino- algae at the base of the Bryostigma clade and in the out- derma, Leprantha, Melarthonis, Myriostigma, Pachnole- group (Fig. 2). As a result, the two early diverging, largely pia, Reichlingia, Snippocia, Sporodophoron, Stirtonia, saprotrophic clades in the frst subclade of Arthoniaceae Synarthonia and Tylophoron. The best scoring RAxML sensu stricto were reconstructed as derived from lichenized tree was selected to represent the relationships among ancestors with a trentepohlioid photobiont. The Bryostigma, taxa, with a final ML optimization likelihood value of Arthonia sensu stricto, Arthonia didyma and Reichlingia − 52686.346267 (Fig. 1). Parameters for the GTR + I + G clades included both lichenized and lichenicolous lifestyles.

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Fig. 1 Best-scoring RAxML Melarthonispiceae 100/1.00 tree reconstructed based on 100/1.00 Arthonia mediella 2 100/1.00 Arthonia mediella 1 Chrysotrichaceae analysis of a combined dataset 100/1.00 Chrysothrix sp. clade of mtSSU, nuLSU and RPB2 100/1.00 Chrysothrix flavovirens 100/1.00 Felipes leucopellaeus sequence data. Bootstrap sup- Felipes sp. 2 port values for ML equal to or 100/1.00 93/0.94 Felipes sp.3 Coniarthonia eos Felipes clade greater than 60 and Bayesian 100/1.00 100/1.00 Coniarthonia pulcherrima 2 posterior probabilities (PP) 100/1.00 Coniarthonia pulcherrima 1 equal to or greater than 0.95 Coniarthoniarosea 2 88/0.97 Coniarthoniarosea 1 are defned as ML/BP above 100/1.00 Chiodecton natalense Chiodecton clade the nodes. Clades recognized Chiodecton sorediatum 80/- Arthonia neglectula as genera (or likely to be Arthonia apatetica 3 recognized in the future) are 100/1.00 Arthonia apatetica 2 83/1.00 Arthonia sp. 1 separated by colors 100/1.00 Arthonia lapidicola 99/1.00 Arthonia stereocaulina 100/1.00 Arthonia sp. 2 72/- Arthonia peltigerina 87/1.00 Bryostigmamuscigenum 95/1.00 100/1.00 Arthonia toensbergii 1 Bryostigma clade Arthonia toensbergii 2 91/1.00 100/1.00 100/1.00 Arthonia lobariicola 1 Arthonia lobariicola 2 Arthonia biatoricola

87/1.00 Arthonia phaeophysciae 100/1.00 Bryostigma sp. 1 100/1.00 Bryostigma sp.2 99/0.97 Arthonia parietinaria 100/1.00 Arthonia molendoi 2 100/1.00 Arthonia molendoi 1 100/1.00 Arthotheliumnorvegicum 100/1.00 Coniangiumspadiceum 1 Coniangium clade 100/1.00 Coniangiumspadiceum 2 Arthothelium orbilliferum

88/1.00 Arthonia susa 100/1.00 Arthotheliumpunctatum 1 Arthotheliumpunctatum 2 Mycoporoid clade 100/0.97 Arthonia thoriana 1 Arthonia thoriana 2 96/- Cryptothecia austrocoreana 1 99/0.96 Cryptothecia austrocoreana 2 81/- Naevia aff. punctiformis 95/- 99/1.00 Naevia punctiformis Naevia pinastri Naevia clade 100/1.00 Naevia dispersa 1 100/0.96 Naevia dispersa 2 100/1.00 Arthonia atra Arthonia calcarea 2 100/1.00 100/1.00 Arthonia calcarea 1 100/1.00 Arthonia radiata 2 Arthoniasensu stricto 73/- 97/0.99 Arthonia radiata 1 100/1.00 clade 100/1.00 Arthonia subfuscicola 1 Arthonia apotheciorum 71/- Arthonia subfuscicola 2

96/1.00 Arthotheliumruanum 3 99/0.99 Arthothelium ruanum 1 100/0.99 Arthotheliumruanum 4 Arthotheliumruanum Arthothelium ruanum 2 clade 99/1.00 -/0.95 Arthotheliumruanum 5 100/1.00 Arthothelium ruanum 6

BayesTraits was more conservative, with the result that secondarily lichenized (Fig. 2). The two clades correspond the ancestral state for Arthoniales and Arthoniaceae sensu to Naevia, reinstated below, and the Arthothelium punctatum lato remained unresolved, almost equally likely lichenized group, also discussed below. with either trentepohlioid or chlorococcoid algae or alterna- tively lichenicolous or saprotrophic (Fig. 2). Arthoniaceae Taxonomy sensu stricto was reconstructed as most likely lichenized with a trentepohlioid photobiont, but with a likelihood of Naevia Fr., Sched. Crit. Lich. Exs. Suec: 21 (1824). only 60%. The two large subclades comprising Arthonia Index Fungorum number: IF3414 sensu stricto to Synarthonia and Snippocia to Inoderma Type species: Naevia orbicularis Fr. [= N. punctiformis were reconstructed as likely lichenized with a trentepohlioid (Ach.) A. Massal.]. photobiont; neither clade contained saprotrophic taxa. The Syn.: Mycarthonia Reinke, Jahrb. Wissenschaftl. Botanik latter were concentrated in two early diverging clades of the 28: 137 (1895). frst subclade of Arthoniaceae sensu stricto, rendering the Index Fungorum number: IF3296 basal node of this subclade saprotrophic with a higher likeli- Type species: Mycarthonia dispersa (Schrad.) Petr. [= N. hood and lichenized species within these clades as possibly dispersa (Schrad.) Thiyagaraja., Lücking & K.D. Hyde].

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Fig. 1 (continued)

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Inoderma sorediatum 1 Inoderma sorediatum 2 Inoderma afromontanum Inoderma byssaceum 2 Inoderma byssaceum 1 lichenized Inodermanipponicum 1 Inodermanipponicum 2 (trentepohlioid) Inodermasubabietinum Sporodophoron primorskiense 1 Sporodophoron primorskiense 2 Sporodophoron gossypinum 1 Sporodophoron gossypinum 2 lichenized Sporodophoron cretaceum 1 Sporodophoron cretaceum 2 (chlorococcoid) Cryptothecia subnidulans 1 Cryptothecia subnidulans 2 Cryptothecia punctosorediata Cryptothecia sp. 1 Cryptothecia sp. 3 lichenicolous Cryptothecia sp. 4 Cryptothecia sp. 5 Cryptophaea phaeospora 1 Cryptophaeaphaeospora 2 Glomerulophoronmauritiae Stirtonia sp. Arthothelium galapagoense 2 non-lichenized Arthothelium galapagoense 1 Herpothallon rubrocinctum 2 (saprotrophic) Herpothallon rubrocinctum 1 Herpothallon inopinatum Herpothallon kigeziense Herpothallon sp. Cryptothecia assimilis Myriostigma candidum 2 Myriostigma candidum 1 Stirtonianeotropica Myriostigma miniatum Myriostigma candidum 3 Crypthonia palaeotropica 2 Crypthonia aff. vandenboomii Crypthonia palaeotropica 1 Arthothelium sp. 3 Arthothelium sp. 2 Arthonia incarnata 3 Arthonia incarnata 2 Arthonia incarnata 1 Briancoppinsia cytospora 1 Briancoppinsia cytospora 2 Leprantha cinereopruinosa Arthonia ilicina Tylophoron protrudens Tylophoron crassiusculum Tylophoron moderatum 2 Tylophoronmoderatum 1 Tylophoronhibernicum 4 Tylophoron hibernicum 5 Tylophoron galapagoense 1 Tylophoron galapagoense 2 Tylophoronstalactiticum Pachnolepiapruinata 1 Pachnolepiapruinata 2 Arthothelium spectabile Snippocianivea 3 Snippocianivea 2 Snippocianivea 1 Synarthoniamuriformis 2 Synarthoniamuriformis 1 Synarthoniainconspicua 1 Synarthoniainconspicua 2 Synarthoniapilosella Synarthoniaalbopruinosa Synarthoniajosephiana Synarthoniaaurantiacopruinosa Synarthoniafuscata Synarthoniaochracea Reichlingiazwackhii 2 Reichlingiazwackhii 1 Reichlingiasyncesioides Reichlingialeopoldii 2 Reichlingialeopoldii 1 Arthoniagraphidicola Coniocarpon cinnabarinum 2 Coniocarpon cinnabarinum 4 Coniocarpon aff. cinnabarinum Coniocarpon fallax Coniocarponrubrocinctum Arthotheliumruanum 4 Arthotheliumruanum 1 Arthotheliumruanum 3 Arthotheliumruanum 6 Arthotheliumruanum 5 Arthotheliumruanum 2 Arthonia didyma 1 Arthonia didyma 2 Arthoniavinosa Arthoniamaculiformis Arthonia physcidiicola Arthoniagranithophila Arthoniaapotheciorum Arthoniasubfuscicola 2 Arthoniasubfuscicola 1 Arthonia radiata 1 Arthonia radiata 2 Arthoniacalcarea 1 Arthoniacalcarea 2 Arthonia atra Naevia dispersa 1 Naevia dispersa 2 Naevia pinastri Naevia aff. punctiformis Naevia punctiformis Arthonia thoriana 1 Arthonia thoriana 2 Cryptothecia austrocoreana 1 Cryptothecia austrocoreana 2 Arthothelium punctatum 2 Arthothelium punctatum 1 Arthonia susa Arthothelium orbilliferum Coniangium spadiceum 2 Coniangium spadiceum 1 Arthotheliumnorvegicum Arthonia molendoi 2 Arthonia molendoi 1 Arthonia parietinaria Bryostigma sp. 1 Bryostigma sp. 2 Arthonia phaeophysciae Arthonia biatoricola Arthonialobariicola 2 Arthonialobariicola 1 Arthonia toensbergii 2 Arthonia toensbergii 1 Bryostigmamuscigenum Arthoniapeltigerina Arthonia sp. 2 Arthoniastereocaulina Arthonia lapidicola Arthonia sp. 1 Arthonia apatetica 2 Arthonia apatetica 3 Arthonia neglectula Chiodecton sorediatum Chiodecton natalense Coniarthoniarosea 1 Coniarthoniarosea 2 Coniarthoniapulcherrima 1 Coniarthoniapulcherrima 2 Coniarthoniaeos Felipes sp. 2 Felipes sp. 3 Felipes leucopellaeus Chrysothrix flavovirens Chrysothrix sp. Arthonia mediella 1 Arthonia mediella 2 Bayesian MCMC Melarthonispiceae BayesTraits

Fig. 2 Ancestral character state analysis focusing on life strategies in Arthoniaceae sensu lato, using Bayesian Binary MCMC and BayesTraits as alternative methods

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Syn.: Pseudoarthonia Marchand, Énumération Massal., N. celtidis (A. Massal.) A. Massal., N. gyrosa méthodique et raisonnée des familles et des genres de la (Ach.) A. Massal. [= Arthonia reniformis (Pers.) Röhl.], classe des Mycophytes (Champignons & Lichens): 160 N. populina (A. Massal.) A. Massal., and N. punctiformis (1896). (Ach.) A. Massal. Beltramini de Casati (1858) placed Nae- Index Fungorum number: IF4412 via close to Arthonia, treating four species: N. atomaria, Type species: Pseudoarthonia punctiformis (Ach.) N. bassanensis Beltr., N. galactites (DC.) Flot., and N. Marchand [= N. punctiformis (Ach.) A. Massal.]. punctiformis. Notably, he gave both N. galactites and N. Syn.: Xerodiscus Petr., in Rechinger, Denkschr. Kaiserl. punctiformis as his combinations, although they had been Akad. Wiss. Wien, Math.-Naturwiss. Kl. 105: 16 (1943). published before. Almquist (1880) was apparently the frst Index Fungorum number: IF5829 to consider Naevia a synonym of Arthonia, placing it as Xerodiscus rechingeri Petr., Denkschr. Kaiserl. Akad. Arthonia sect. Naevia (Fr.) Almq. within the latter. He Wiss. Wien, Math.-Naturwiss. Kl. 105(2,1): 16 (1943) [= N. included a number of unrelated species in this section, but dispersa (Schrad.) Thiyagaraja., Lücking & K.D. Hyde]. considered Naevia orbicularis and N. atomaria synonyms Non-lichenized but often forming thallus-like, whitish of Arthonia punctiformis. In later works, this synonymy to greyish patches on the substrate. Prothallus sometimes was expanded to also include N. celtidis and N. populina, present. Photobiont absent. Sexual morph: Ascomata among other names (Sundin 1999; Nimis 2016), thus apothecial, black, circular to irregular to almost stellate including almost all species treated by Massalongo (1855) in outline, adnate, emarginate. Hymenium hyaline, gel in a single taxon. Vainio (1901) kept Naevia separate from I + blue, KI + blue. Epithecium olive-brown, K + olive- Arthonia on account of the absence of a photobiont. green. Hypothecium hyaline to pale yellowish. Asci ovoid Unfortunately, mycologists adopted the name Naevia in to clavate, bitunicate, fssitunicate, without distinct stipe, a sense very diferent from its type. This was based on Fries I−, with KI + ring-shaped structure in tholus, 4–8-spored. himself, who had established an unrelated taxon under the Ascospores hyaline, 1–5-septate. Asexual morph: Pyc- same name, Naevia Fr. (Fries 1849), an illegitimate later nidia black, semi immersed to immersed. conidia aseptate, homonym that was later given a replacement name, Nae- bacilliform. vala (Hein 1976). Rehm (1896) described Naevia sensu Naevia as here defned is overall similar to Arthonia sensu Fries (1849) as having hemiangiocarpous ascomata with stricto to which it is rather closely related, forming a clade pale discs and producing non-septate ascospores, and most branching of just below the latter (Fig. 1). It agrees with other species subsequently included in the genus were based Arthonia sensu stricto in ascoma morphology and anatomy, on this character combination (e.g. Kirschstein 1935; Hein including the paraphysoids forming an olive-brown epithe- 1976). cium layer, and the ascus with a KI + , blue ring structure Given this confusion, we had frst ignored Naevia and in the tholus (Sundin and Tehler 1998; Wedin and Hafell- had considered the name Mycarthonia as suitable for the ner 1998; Sundin 1999; Grube 2007). Based on the species clade centered around Arthonia pinastri. Mycarthonia was sequenced so far, a minor diference can be found in the originally published by Reinke (1895, p. 137), stating: “Auch amyloid (I + blue, KI + blue) in Naevia versus to hemia- die Gattung Arthonia ist teils gonidienlos – für diese schlage myloid (I + blue turning reddish, KI + blue) hymenial jelly ich den Namen Mycarthonia vor.” [“Also Arthonia partially in Arthonia sensu stricto (e.g. A. atra, A. radiata; Sundin lacks gonidia – for those I propose the name Mycarthonia”]. and Tehler 1998; Sundin 1999; Grube 2007). Apart from Reinke did not include any species in the genus nor did he forming a phylogenetically distinct clade, the other principal designate a type. According to ICN Art. 38 and Art. 39, the diference towards Arthonia sensu stricto thus far appears to protologue includes a valid (German) description, namely be in the absence of a photobiont. non-lichenized species of Arthonia, and designation of a The genus Naevia was established by Fries (1824) type was not required at the time (ICN Art. 40). The genus based on a single species, N. orbicularis, indicated as name was frst adopted by Schneider (1897), in a summary similar to Arthonia punctiformis Ach. and A. melantera of Reinke’s system, and subsequently by Engler (1903), Ser- Ach. but not lichenized. Shortly after, Fries (1825) also nander (1907), Zahlbruckner (1907), and later by von Arx included A. melantera in Naevia, without a formally pro- (1954) and Sundin and Tehler (1998). However, none of posed combination. The genus was accepted by Flotow these authors designated a type for the genus or included (1849), Massalongo (1855) and Beltramini de Casati any species in it. The frst author to include species in this (1858), but partly in a diferent sense, since Massalongo genus was Petrak (1953), namely M. culmicola (Petr.) Petr., (1855) compared it to the pyrenocarpous Arthopyrenia, M. dispersa (Schrad.) Petr., and M. punctiformis (Ach.) Petr. rather than Arthonia. Massalongo (1855) included fve Since M. culmicola was described after Reinke’s protologue species, presumably in addition to N. orbicularis, which (1895), either M. dispersa or M. punctiformis are suitable as was not mentioned, namely N. atomaria (A. Massal.) A. type, and here we designate the former, to avoid confict with

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M. punctiformis being the type of Naevia and hence making dalmatica and A. neglecta, and so it would not be surpris- Mycarthonia a heterotypic synonym of the latter. ing if A. culmicola also belonged here. On the other hand, Marchand (1896) established Pseudoarthonia 1 year after detailed phylogenetic studies may well show that this is a Reinke (1895), besides P. punctiformis also including P. complex of separate, phenotypically cryptic lineages. Moen dispersa (Schrad.) Marchand, P. varians (Davies) Nyl. and (2019) found that A. punctiformis in Norway alone repre- P. subvarians (Nyl.) Marchand (= Arthonia apotheciorum sented at least four distinct species, with an additional unde- (A. Massal.) Almq.). Notably, the three latter names are scribed species in Japan (Frisch et al. 2014). not registered in Index Fungorum or MycoBank, although Based on literature data, we investigated the possibility the combinations are valid (ICN Art. 41.3). Sundin et al. of further non-lichenized species of Arthonia sensu lato (2012) selected P. punctiformis as generic type, which is to belong in Naevia. A number of non-lichenized species in accordance with the protologue, as Marchand (1896) did have been described that ft the sequenced taxa in overall not provide a written description but an illustration of the morphology, the amyloid (I + blue, KI + blue) hymenial genus based on that species. Whereas P. dispersa is closely jelly, and the KI + blue ring structure in the tholus of the related to P. punctiformis, both now included in Naevia, the asci; some species were established following the concept of other two species are lichenicolous: whereas A. apothecio- Naevia sensu Fries (1824, 1825), but we have not checked rum is included in Arthonia sensu stricto while P. varians is the underlying type material. These include Arthonia albop- included in Arthonia without molecular data. When estab- ulverea Nyl., A. beccariana (Bagl.) Stizenb., A. pruinascens lishing Mycarthonia and Pseudoarthonia, neither Reinke (Zahlbr.) Grube, A. rhoidis Zahlbr., A. samdykeana Lend- (1895) nor Marchand (1896) or Petrak (1953) were aware emer & D.Ray, A. sexlocularis Zahlbr., A. quintaria Nyl., A. that Fries’s name Naevia was to be adopted for a genus subastroidea Anzi, A. tetramera (Stizenb.) Hasse, Naevia including Arthonia punctiformis. benguellensis Vain., N. mozambica Vain., N. mozambica A total of 95 species names have been associated with var. simplicior Vain., and N. rotundata Vain., among others the name Naevia; most of these correspond to Naevia sensu (Vainio 1901; Sundin 1999; Grube 2007; Lendemer and Ray Fries (1849) and have been redispositioned in other genera, 2017. Further, non-lichenized species, such as A. glaucella mostly in unrelated families outside Arthoniomycetes (e.g. Nyl., A. pruinosella Nyl., and A. stictoides (Desm.) Nyl., dif- Hein 1976). Approximately a dozen names represent genu- fer in the hemiamyloid hymenial jelly (I + blue turning red- ine Arthoniales and about half of these have been established dish, KI + blue; Grube 2007) and based on this feature may as synonyms of N. punctiformis (see above). Morphological belong in Arthonia s.str. We summarized the main features and molecular revision of the remaining names is required of these taxa in comparison to Naevia dispersa, N. pinastri, to elucidate their phylogenetic relationships. Notably, based and N. punctiformis (Table 2). on the available data analyzed here, besides N. punctiformis, Limiting formal changes to sequenced species only, the the species to be included in Naevia sensu Fries (1824, following new combinations are proposed: 1825), as well as their potential synonyms, had previously Naevia pinastri (Anzi) Thiyagaraja., Lücking & K.D. not been associated with that genus. We currently include Hyde, comb. nov. three species here confrmed by molecular data, namely Index Fungorum number: IF557646; Faces of Fungi num- N. dispersa, N. pinastri and N. punctiformis (see below). ber: FoF 07974 Naevia punctiformis is set apart by the larger, 3(−5)-sep- Basionym: Arthonia pinastri Anzi, Comm. Soc. Crittog, tate ascospores (up to 25 × 8 μm) and the often irregular Ital. 1 (Fasc. 3): 159 (1862). to almost stellate ascomata (Sundin 1999; Moen 2019), Index Fungorum number: IF376745 whereas the other three species have smaller, regularly 1- Thallus greyish white, with pruinose, thick, corticol- or 3-septate ascospores and more or less rounded to some- ous, crustose, epiphloedal, poorly developed prothallus, what irregular ascomata. Naevia dispersa difers in the very photobiont not detected. Sexual morph: Ascomata apo- small (10–13 × 3–4 μm), 1-septate ascospores. A further thecial, approximately 200–250 μm wide, black, circular species, Arthonia culmicola Petr., is doubtfully separated to ellipsoidal, adnate, slightly erumpent from the thallus. from N. pinastri by substrate (bark vs. dead grass leaves), Epihymenium 20–25 μm tall, olivaceous brown. Hyme- and Petrak (1941) was apparently not aware of A. pinastri nium 30–45 μm tall, hyaline. Paraphysoids 1–1.5 μm wide, when he described A. culmicola. Both have similarly sized pale yellowish, densely arranged, tip swollen with pig- (12–17 × 4–6 μm) ascospores with more or less isodiametric ments, 1.5–2 μm wide. Hypothecium 5–15 μm tall, hya- cells. Arthonia subgyrosa Nyl., described from India (Roy- line to pale yellowish, indistinct. Asci 20–50 × 10–20 μm chowdhury 1979) and also reported from Korea (Lee and ( x̄ = 35 × 17 μm, n = 40), hyaline, broadly clavate to Hur 2016), also agrees in morphology and ascospore dimen- ovoid, 8-spored, bitunicate, fssitunicate, tholus thick- sions. Naevia pinastri is rather widespread in the Northern ened, concave, tip blunted, without distinct stipe, ascus hemisphere and already has several synonyms, including A. wall apically thickened with a wide ocular chamber.

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Table 2 Summary of diagnostic features of non-lichenized species of Arthonia sensu lato including those here accepted in Naevia Species Septa Ascospore size Ascoma shape Pruina Hymenium Asci Range

Naevia dispersa 1 9–15 × 3–5 μm Irregular-lirellate ± Absent I+ blue KI+ NA, EU KI+ blue ring Arthonia rhoidis 2 10–14 × 3–5 μm Rounded-irregular Absent I+ blue KI+ NA KI+ blue ring Naevia benguellensis 2 9–12 × 3 μm Rounded-elongate Absent I+ blue [–] AF KI+ blue Arthonia pruinosella 3 12–15 × 4–5 μm Rounded-irregular Present I+ blue(-red), KI+ NA, EU Calcium oxalate KI+ blue ring Arthonia stictoides 3 9–12 × 3–4 μm Irregular-lirellate Absent I+ blue(-red) KI+ EU KI+ blue ring Arthonia tetramera 3 10–14 × 3–5 μm Lirellate-stellate ± Absent I+ blue KI+ NA KI+ blue ring Arthonia culmicola 3 11–16 × 4–6 μm Rounded-elongate ± Absent [–] [–] ME Naevia pinastri 3 11–17 × 4–6 μm Rounded-irregular ± Absent I+ blue KI+ NA, EU KI+ blue ring Arthonia glaucella 3(−4) 13–20 × 4–6 μm Rounded-irregular- ± Absent I+ blue(-red) KI+ NA lirellate KI+ blue ring Naevia rotundata 3 11–12 × 3–4 μm Rounded-elongate Absent I+ blue [–] AF KI+ blue Naevia mozambica 3 13 × 4 μm Irregular-lirellate Absent [–] [–] AF Naevia mozambica var. 3 13–14 × 5–6.5 μm Irregular Absent [–] [–] AF simplicior Naevia punctiformis 3–5 13–25 × 4–6 μm Rounded-irregular- ± Absent I+ blue KI+ NA, EU lirellate KI+ blue ring Arthonia sexlocularis 5–7 15–20 × 5–6.5 μm, Punctiform-lirellate ± Absent I+ blue KI+ NA microcephalic KI+ blue ring Arthonia quintaria 5 17–24 × 6–8 μm, macro- Punctiform-lirellate ± Absent I+ blue [–] NA cephalic KI+ blue Arthonia samdykeana 5–9 20–35 × 6–11 μm, mac- Rounded-irregular ± Absent I+ blue [–] NA rocephalic KI+ blue Arthonia albopulverea muri 13–20 × 4–6 μm Punctiform-lirellate- Absent I+ blue KI+ NA, EU, AF stellate KI+ blue ring Arthonia beccariana muri 18–23 × 9–12 μm Rounded-irregular Absent, orange I+ blue KI+ NA, EU K+ purple pigment KI+ blue ring Arthonia pruinascens muri 20–25 × 10–12 μm Rounded-irregular Present I+ blue KI− NA KI+ blue Arthonia subastroidea muri 20–30 × 9–13 μm Elongate ± Absent I+ blue KI+ NA, EU KI+ blue ring

Muri muriform, NA North America, EU Europe, ME Middle East, AF Africa

̄ Ascospores 11–17 × 5–6 μm ( x = 15 × 6 μm, n = 40), Naevia dispersa (Schrad.) Thiyagaraja., Lücking & K.D. hyaline, smooth–walled, fusoid to obvoid, 0–3 septate, Hyde, comb. nov. locules almost of equal size, not constricted at the septa. Index Fungorum number: IF557647; Faces of Fungi num- Asexual morph: Pycnidia black, semi immersed, up to ber: 08041 0.1 mm. Conidia not observed (Fig. 3). Basionym: Opegrapha dispersa Schrad., Annalen der Material examined: Italy, Passo del Carnaio-Bagno di Botanik (Usteri) 22: 86 (1797); Arthonia dispersa (Schrad.) Romagna, Province of Forli-Cesena, on living branch of Dufour, J. Phys. Chim. Hist. Nat. 87: 203 (1818); Lecideop- Fraxinus ornus (Oleaceae), 25 September 2017, Erio Camp- sis dispersa (Schrad.) Rehm, Rabenh. Krypt.-Fl. 2, 1.3(34): oresi IT3497 (MFLU 17-1696) 418 (1891); Pseudoarthonia dispersa (Ach.) Marchand, Chemistry: Epihymenium KI+ blue. Hymenium I+ blue, Énum. Méth. Rais Fam. Genres Mycophytes (Paris): 160 KI+ blue. Asci I−, KI+ blue (ring-shaped structure in tho- (1896); Tomaselliella dispersa (Schrad.) Cif., Arch. Bot. lus). Lichen substances not investigated by thin-layer chro- Ital. 28: 3 (1952); Mycarthonia dispersa (Schrad.) Petr., matography (TLC). Sydowia 7: 28 (1953)

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Fig. 3 Naevia pinastri (MFLU17-1696) a–c, Ascomata on bark. d, e, Lugol’s solution. s–u, Ascospores in 10% KOH stained with Lugol’s Cross sections of ascomata in tap water. f–k, Asci in tap water. l, m, solution. Scale bars: a = 200 μm, b, c = 100 μm, d, e, n = 20 μm, Ascospores in tap water. n, Cross section of ascomata in 10% KOH f–k, o–r = 30 μm, l, m, s–u = 5 μm stained with Lugol’s solution. o–r, Asci in 10% KOH stained with

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Synonym: Arthonia cytisi A. Massal., Nuovi Ann. Sci. Mycophytes (Paris): 160 (1896); Mycarthonia punctiformis Nat. Bologna 7: 216 (1853) (Ach.) Petr., Sydowia 7(1-4): 28 (1953). Description and illustration: Sundin and Tehler (1998); Synonyms: Arthonia melantera Ach., K. Vetensk-Acad. Sundin (1999) Nya Handl. 29: 131 (1808); Naevia orbicularis Fr., Sched. There is much confusion with the name Arthonia dispersa. Crit. Lich. Exs. Suec.: 21 (1824); Arthonia atomaria Index Fungorum (2020) lists four presumed homonyms, A. Massal., Ric. Auton. Lich. Crost.: 50, Fig. 89 (1852); namely Arthonia dispersa Dufour (Dufour 1818; IF122034), Arthonia insinuata Stirt., Trans. Glasgow Soc. Fld Nat. 4: 89 A. dispersa A. Massal. (Massalongo 1852, p. 121862), A. (1876); Opegrapha microscopica Sm. in Smith & Sowerby, dispersa (Schrad.) Nyl. (Nylander 1861, p. 140137), and A. Engl. Bot. 27: tab. 1911 (1808). dispersa Rabenh. (Rabenhorst 1870, p. 121967). In addition, Description and illustration: Sundin and Tehler (1998); there are two presumed homonyms of Opegrapha dispersa, Sundin (1999). namely O. dispersa Schrad. (Schrader 1797; IF201253) and O. Mycarthonia punctiformis provides a similar case as M. dispersa DC. (de Lamarck and de Candolle 1805; IF463798). dispersa. The name Naevia punctiformis Beltr., listed as such Only one of these names actually exists, namely Opegrapha in Index Fungorum (2020) and likely based on Zahlbruckner dispersa Schrad. de Lamarck and de Candolle (1805, p. 308) (1923), does not exist, as Beltramini de Casati (1858) based did not establish a new name but under the number 835 explic- this combination explicitly on Arthonia punctiformis Ach. itly cited O. dispersa Schrad. Likewise, Dufour (1818, p. 203) However, Massalongo (1855) had already made that very did not introduce a new species under Arthonia but based his same combination. The name Pseudoarthonia Marchand, name explicitly on “O. dispersa, Fl. Fr., no. 835”, which is a erroneously given as based on “Naevia punctiformis Beltr.”, direct reference to de Lamarck and de Candolle and by exten- is therefore a synonym of Naevia, as its type is by default sion an indirect reference (ICN Art. 41.3) to Schrader (1797). Arthonia punctiformis Ach. Thus, the valid combination of O. dispersa into Arthonia was published by Dufour (1818), as A. dispersa (Schrad.) Dufour. Also, the entry of A. dispersa by Massalongo (1852, p. 51) Discussion explicitly refers to “Arthonia dispersa Duf.” and Opegrapha dispersa Schrad., thus not to be understood as the introduc- The evolutionary origin of non-lichenized, presumably tion of a new name. Nylander (1861, p. 261) treated the taxon saprotrophic members in Arthoniaceae is of interest for the in his Lichenes Scandinaviae, as “A. dispersa (Schrad., non evolution of lichenization in Arthoniales. Two competing Duf.)”, with additional reference to Opegrapha dispersa hypotheses can be envisioned: non-lichenized lineages are Schrad. This means that Nylander was of the opinion that plesiomorphic and gave rise to lichenized forms, or non- the material seen by Dufour (1818) was not identical with lichenized lineages are derived from lichenized ancestors. Schrader’s O. dispersa; however, Dufour’s valid combination This mirrors evolutionary models of lichenization in fungi of Schrader’s O. dispersa into Arthonia is not afected by this as a whole: while Gargas et al. (1995) found that the lichen (ICN Art. 7.3). ICN Art. 48.1 does not apply to Nylander’s symbiosis evolved several times independently, Lutzoni entry, since Dufour’s explicitly excluded material is not the et al. (2001) recovered the largely non-lichenized class Euro- type of an established name, and so Nylander’s combination tiomycetes, which includes economically important fungi Arthonia dispersa must be interpreted as A. dispersa (Schrad.) such as Aspergillus and Penicillium, within the lichenized Dufour, even if Dufour’s material did not represent that spe- Lecanoromycetes. However, it was recently found that this cies. Finally, Rabenhorst (1870) made explicit reference to “A. topology was caused by a single contaminant sequence dispersa Schrad…. (non Duf.)” and “A. dispersa Nyl.”, citing (Lücking and Nelsen 2018). It is now widely accepted that Schrader (1797) and Nylander (1861). As a consequence, the lichenization evolved many times independently in various valid name is A. dispersa (Schrad.) Dufour, based on Ope- classes, with few examples of secondary delichenization grapha dispersa Schrad., and it should be cited as such, and (Lücking et al. 2017). all the above names are homotypic variations. Arthonia cytisi For Arthoniales and Arthoniaceae, our analysis gave A. Massal. was placed in synonymy with N. dispersa by von ambiguous results. Whereas non-lichenized, saprotrophic Arx (1954). lineages were reconstructed as secondarily delichenized using the Bayesian Binary MCMC approach, BayesTraits Naevia punctiformis (Ach.) A. Massal., Framm. Lichenogr.: reconstructed the deeper nodes as ambiguous regarding life 8 (1855). strategy. The thus far sequenced, presumably saprotrophic Index Fungorum number: IF395831 species clustered in two clades which together form a grade Basionym: Arthonia punctiformis Ach., K. Vetensk- rather deeply nested within various lichenized lineages, sug- Acad. Nya Handl. 29: 130 (1808); Pseudoarthonia punc- gesting that secondary delichenization is more likely. How- tiformis (Ach.) Marchand, Énum. Méth. Rais Fam. Genres ever, a broader sampling of non-lichenized, saprotrophic

1 3 220 Fungal Diversity (2020) 102:205–224 species is required to further elaborate on this emerging 1825), whereas most species at some point associated pattern. In any case, it appears that presumably saprotrophic with the name Naevia represent unrelated lineages outside lineages within Arthoniaceae are rather closely related. Arthoniomycetes. Regarding lichenicolous lineages, the Bayesian Binary Besides Naevia, our phylogeny included a second clade MCMC reconstruction agreed well with previous hypoth- (the mycoporoid clade) with several non-lichenized and pre- eses on the polyphyletic origins of parasitic fungi in Artho- sumably saprotrophic species. This clade, which was not nia (Grube and Giralt 1996). Frisch et al. (2014) showed supported, comprised the species Arthonia susa R.C. Harris that a parasitic or parasymbiontic lifestyle appeared at least and Lendemer, A. thoriana Ertz and Sanderson, Arthothe- four times in Arthoniaceae and there were no larger clades lium orbilliferum (Almq.) Hasse, A. punctatum J.S. Park containing exclusively parasitic or parasymbiontic species. and J.-S. Hur, and Cryptothecia austrocoreana J.-J. Woo, Also Grube and Giralt (1996) stated that saprotrophic life- L. Lőkös, E. Farkas and J.-S. Hur. Except for A. orbillif- styles have multiple independent origins in Arthoniaceae. erum, all species were recently described (Lendemer et al. In their broad analysis of Arthoniaceae, Frisch et al. (2014) 2013; Park et al. 2017; Woo et al. 2017; Ertz et al. 2018) included only two saprotrophic taxa, Arthonia punctiformis and never analysed jointly in a comprehensive phylogeny, and A. af. punctiformis, which both clustered near to Artho- so their possible relationships were not recognized. Artho- nia sensu stricto. They considered A. dispersa lichenized, nia thoriana was described as non-lichenized and Cryp- but the species is usually given as non-lichenized or weakly tothecia austrocoreana is clearly lichenized, whereas the lichenized (Sundin 1999). Although our own analysis was other three species are at best doubtfully lichenized, with not conclusive, we found no support indicating that the sap- no apparent photobiont layer. Arthonia susa and Arthothe- rotrophic lifestyle could be ancestral and plesiomorphic in lium punctatum are closely related and agree in most fea- Arthoniaceae. tures, except that the ascospores in the latter are slightly Arthonia was originally introduced by Acharius (1806) larger (30–45 × 12–18 μm vs. 24–36 × 10–14 μm). Nota- as a convolute of unrelated taxa, later identifed as e.g., A. bly, three of these species resemble Mycoporum, namely radiata, Lecanographa lyncea (Sm.) Egea and Torrente, Arthonia susa, Arthothelium orbilliferum and A. punctatum. Solorina crocea (L.) Ach., and S. saccata (L.) Ach. Shortly The isotype material of Arthothelium orbilliferum in Brit- after, Acharius (1808) included the now conserved type, A. ish Museum (BM) was annotated as ‘Mycoporum orbillif- radiata (Pers.) Ach. and added a non-lichenized species, A. erum’ by B.J. Coppins in 1977, although this combination punctiformis Ach. (syn.: A. melantera Ach., described in the was never published. Both Arthonia susa and Arthothelium same work). Opegrapha dispersa was known to Acharius, punctatum were compared to species of Mycoporum, in par- but based on its original description grouped into the idi- ticular M. pycnocarpoides Müll.Arg., which according to othalami, having ascomata with a proper margin, and not the protologue (Müller 1895) and the type material appears associated with Arthonia at the time (Acharius 1803). Fries to difer from Arthothelium punctatum chiefy in the larger (1824, 1825) was the frst to recognize non-lichenized spe- ascospores (45–55 × 18–23 μm). Notably, M. pyrenocarpum cies in a separate genus, Naevia, including in that genus a Nyl. (often cited as ‘pycnocarpum’), to which Müller (1895) new species, N. orbicularis (Fries 1824), and later A. melan- compared his M. pycnocarpoides, has ascospores around tera (Fries 1825). Massalongo (1855) took up Fries’s name 35 × 15 μm (Nylander 1858; Harris 1995), somewhat at the but compared it to the pyrenocarpous genus Arthopyrenia, border between Arthonia susa and Arthothelium punctatum. one of the reasons why this name was subsequently not con- Lumbsch (1999) studied M. elabens (A. Massal.) Flot. ex sidered as an option for non-lichenized arthonioid species, Nyl., the type species of Mycoporum, and found that it does the other reason being that Fries himself established the not form perithecia with a genuine peridium, but a covering name Naevia again for an unrelated lineage of fungi (Fries roof on the ascomata that ruptures into pores to release the 1849; Rehm 1896; Hein 1976). While Almquist (1880) syn- ascospores. The asci develop into cavities (locules) formed onymized Naevia sensu Fries (1824, 1825) under Arthonia, by a dense layer of anastomosing pseudoparaphyes; they Reinke (1895) and Marchand (1896) almost simultaneously have a thick tholus with narrow ocular chamber and lack an proposed to again separate non-lichenized species in dif- I− or KI− reaction. The I− or KI− reaction of the hamathe- ferent genera, Mycarthonia and Pseudoarthonia. This con- cium is not given. Lumbsch (1999) stated Mycoporum is cept was also taken up again by Vainio (1901), using the properly placed within Dothideomycetes and specifcally name Naevia sensu Fries (1824, 1825), while mycologists Dothideales, but did not discuss the remarkable similarity independently established numerous new species under the of ascoma development between Mycoporum elabens and name Naevia sensu Fries (1849), causing much confusion Arthothelium spectabile A. Massal. (Henssen and Jahns (Hein 1976). However, it is clear that the non-lichenized 1973; Henssen and Thor 1994), a species deeply nested clade encompassing Arthonia punctiformis and related within Arthoniaceae, although in a clade diferent from the species must bear the name Naevia sensu Fries (1824, taxa above, closely related to Pachnolepia pruinata (Torss.)

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Frisch and G. Thor. The anatomical similarities between their phenotypical separation a challenge; (b) both lineages Mycoporum elabens as depicted in Lumbsch (1999) on one difer in ascoma anatomy (perithecioid vs. roof-like), but hand and Arthonia susa, depicted in Lendemer et al. (2013), Lumbsch (1999) studied material not actually conspecifc and Arthothelium punctatum, depicted in Park et al. (2017), with the type; (c) there may be two unrelated lineages in are even more striking, particularly the covering roof. Lend- Dothideomycetes and Arthoniomycetes, but M. elabens is emer et al. (2013) distinguished M. pycnocarpoides from A. actually a representative of Arthoniomycetes. Harris (1995, susa by the “fused perithecioid” ascomata, the I− hamathe- p. 61) stated: “The hamathecium in Mycoporum consists of cium, and the ascospores becoming brown. Park et al. (2017) very irregular, slightly gelatinizing and somewhat disarticu- separated Mycoporum in being “pyrenocarpous” and having lating physes which are almost entirely obscured by irregular pseudoparaphyses. However, according to Lumbsch (1999), oil droplets. (If you can make out the physes clearly, it prob- the ascomata of M. elabens are not perithecioid, and there ably isn’t a Mycoporum).” For none of the above species, appears to be no discernable diference in the development including M. elabens, hymenial inspersion was mentioned, of the hamathecium in M. elabens vs. Arthothelium specta- and in all cases the hamathecial flaments are discernable. bile, although termed pseudoparaphyses in one case and This lends support to the hypothesis that even if two unre- paraphysoids in the other (Henssen and Thor 1994; Lumbsch lated mycoporoid lineages exist, one in Dothideomycetes 1999). While Lendemer et al. (2013) gave the hamathecium and one in Arthoniomycetes, several taxa currently placed of Arthonia susa as I + orange and KI + blue (hemiamyloid) in Mycoporum, including perhaps its type, may belong in and that of M. pycnocarpoides as I−, the hamathecium of Arthoniomycetes, which would result in a nomenclatural Arthothelium punctatum was described as I−. Müller (1895) conundrum. (2) All mycoporoid taxa are related and belong described the ascospores of M. pycnocarpoides as in M. pyc- in Arthoniomycetes. Given the available evidence and the nocarpum Nyl. (a synonym of Mycoporum compositum (A. enormous phenotypical variation in this family, the latter Massal.) R.C. Harris), who described the ascospores of the alternative would not come as a surprise. To resolve this latter as “... incolorae.” (Nylander 1858). One notable dif- issue, detailed phylogenetic, anatomical and ontogenetic ference is found between the asci of Arthonia susa and those studies are required of all species currently included in of Mycoporum elabens, the frst having a shallow ocular Mycoporum, as far as possible also comprising the types. chamber and amyloid ring structure in the tholus (Lendemer et al. 2013), the second a long and narrow ocular chamber Acknowledgements We thank the Thailand Research Fund (“The future of specialist fungi in a changing climate: baseline data for gen- and no amyloid structures (Lumbsch 1999). However, both eralist and specialist fungi associated with ants, Rhododendron species ascus types are characteristic of various confrmed members and Dracaena species DBG6080013” and “Impact of climate change of Arthoniales, even between closely related taxa such as in on fungal diversity and biogeography in the Greater Mekong Sub- Bryostigma. Thus, there is either considerably ambiguity region RDG6130001”) and “The 2019 high-end foreign expert intro- duction plan to Kunming Institute of Botany (granted by the Ministry in the diagnostic value of hamathecium amyloidity, ascus of Science and Technology of the People’s Republic of China (Grant type and ascospore pigmentation, or there are problems in Number G20190139006)) for funding this research. S.C. Karunarathna observation, including ontogenetic patterns (ascospore pig- would like to thank the CAS President’s International Fellowship Initia- mentation, ascus type?) or mix-up of possibly unrelated taxa. tive (PIFI) under the following grant: 2018PC0006 and the National M pycnocarpoides Science Foundation of China (NSFC, project code 31851110759). We Thus, while . was described from Africa also thank Udeni Jayalal, Nalin Wijayawardene, Ming-Ying Zhang, (Müller 1895), Lendemer et al. (2013) based their observa- Mohammed Warris, Lee B.G and Eleni Gentekaki for their support tions on North American material identifed with that name. during this research. Dhanushka Wanasinghe would like to thank CAS Also, ascospores remaining hyaline and becoming brown President’s International Fellowship Initiative (PIFI) for funding his Arthoni- postdoctoral research (Number 2019PC0008), the National Science only in late stages is a rather frequent feature in Foundation of China and the Chinese Academy of Sciences for fnan- ales. In the recent treatment of families of Dothideomycetes, cial support under the following Grants: 41761144055, 41771063 and Hyde et al. (2013) included Mycoporum in an unresolved Y4ZK111B01. We also extend our gratitude to Teuvo Ahti, David taxonomic position, whereas Liu et al. (2017) did not include Hawksworth, Pier-Luigi Nimis and Rikard Sundin and Mats Wedin who helped to clarify the nomenclatural status of the genus Naevia. the genus due to lack of molecular data and Wijayawardene et al. (2017) placed the genus and the family Mycoporaceae in Pleosporales. This intriguing situation ofers two explanations: (1) Two References unrelated mycoporoid lineages are involved, one in Doth- ideomycetes and one in Arthoniomycetes. Since Lumb- Acharius E (1803) Methodus qua omnes detectos lichenes. Marquard, sch (1999) demonstrated a roof-like cover for M. elabens, Stockholm this scenario would imply three possible alternatives: (a) Acharius E (1806) Arthonia, novum genus Lichenum, quod descripsit both lineages agree in ascoma anatomy and the ascomata Erik Acharius, M.D. et Profess. etc. Neues J Bot 1:1–23 of Mycoporum are not genuinely perithecioid, which make

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